Article

Mutualistic interactions between vitamin B12 -dependent algae and heterotrophic bacteria exhibit regulation

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

Many algae are auxotrophs for vitamin B12 (cobalamin), which they need as a cofactor for B12-dependent methionine synthase (METH). Because only prokaryotes can synthesize the cobalamin, they must be the ultimate source of the vitamin. In the laboratory, a direct interaction between algae and heterotrophic bacteria has been shown, with bacteria supplying cobalamin in exchange for fixed carbon. Here we establish a system to study this interaction at the molecular level. In a culture of a B12-dependent green alga Chlamydomonas nivalis, we found a contaminating bacterium, identified by 16S rRNA analysis as Mesorhizobium sp. Using the sequenced strain of M. loti (MAFF303099), we found that it was able to support the growth of B12-dependent Lobomonas rostrata, another green alga, in return for fixed carbon. The two organisms form a stable equilibrium in terms of population numbers, which is maintained over many generations in semi-continuous culture, indicating a degree of regulation. However, addition of either vitamin B12 or a carbon source for the bacteria perturbs the equilibrium, demonstrating that the symbiosis is mutualistic and facultative. Chlamydomonas reinhardtii does not require B12 for growth because it encodes a B12-independent methionine synthase, METE, the gene for which is suppressed by addition of exogenous B12. Co-culturing C. reinhardtii with M. loti also results in reduction of METE expression, demonstrating that the bacterium can deliver the vitamin to this B12-independent alga. We discuss the implications of this for the widespread distribution of cobalamin auxotrophy in the algal kingdom.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Interactions between algae and bacteria consortium hold the promise of commercializing these bioproducts and understanding their associations involving cross talk between primary metabolites including carbon dioxide (CO 2 )-oxygen (O 2 ) exchange, growth mediators such as phytohormones and/or vitamins, and recycling of essential nutrients (such as phosphorous, nitrogen) in the aquatic ecosystems (Higgins et al. 2018a, b;Cirri and Pohnert 2019;Yao et al. 2019;Fallahi et al. 2021). Exogenous compounds produced by bacteria have raised interest among the community to understand their role in microalgal growth and production of biorenewables such as vitamin B (Croft et al. 2005;Kazamia et al. 2012;Grant et al. 2014;Durham et al. 2015;Higgins et al. 2018a, b), phytohormones (De-Bashan et al. 2008;Choix et al. 2014;Amin et al. 2015;Segev et al. 2016;Peng et al. 2021), and siderophore complex (Leyva et al. 2014;Villa et al. 2014;Rajapitamahuni et al. 2019;Peng et al. 2021) (Table 8.1). For example, most of the microalgal strains are autotrophs and depend on vitamins synthesized by bacteria (Tandon et al. 2017;. ...
... Additionally, Ruegeria pomeroyi DSS-3 restored B12 depleted in Thalassiosira pseudonana, enhancing growth rates when supplemented with vitamin B12 exogenously . Also, the metE gene expression was reduced in co-cultured studies with Chlamydomonas reinhardtii and Mesorhizobium loti (Kazamia et al. 2012). In conclusion, this study demonstrates that the C. reinhardtii does not require vitamin B12 for growth since it expresses a B12-independent methionine synthase metE gene which is inhibited by exogenous B12 (Kazamia et al. 2012). ...
... Also, the metE gene expression was reduced in co-cultured studies with Chlamydomonas reinhardtii and Mesorhizobium loti (Kazamia et al. 2012). In conclusion, this study demonstrates that the C. reinhardtii does not require vitamin B12 for growth since it expresses a B12-independent methionine synthase metE gene which is inhibited by exogenous B12 (Kazamia et al. 2012). Thiamine is required by green algae to produce vitamin B1 thiamine pyrophosphate (TPP), a well-known mediator in the metabolism of carbohydrates and amino acids (Lonsdale 2006). ...
Chapter
Full-text available
Carotenoids are pigments having a proven role as food colorants, antioxidants, health-promoting substances, food additives, feed additives, vitamins, pharmaceuticals, etc. After experiencing the hazard of synthetic entities in human life, people are again trying to “go natural.” Being natural and part of a healthy ecosystem, microalgae may have immense potential to provide many such entities. In the present scenario, microalgal systems are among the top-ranked bioresources to meet the demands of the fast-growing world population. In addition, being grown in natural water resources provides opportunities to socially backward classes to manage their lifestyle for economic upliftment and nutritional well-being. Carotenoids may be divided into primary and secondary groups. The secondary carotenoids are present in the lipid vesicles in the cytosol or plastids. Also, phycobiliproteins, phycocyanin, phycoerythrins, β-carotenes, lutins, and astaxanthins are the pigments which are commonly produced by microalgae. Many microalgal systems have been investigated so far to produce different pigments, for instance, diatoms and members of Phaeophyceae for fucoxanthins, dinoflagellates for peridinin, cryptophytes for alloxanthins, Porphyridium spp. for β-carotenes, Tetraselmis spp. for lutein, and so on. This chapter aims to provide an overview of the potential of microalgal systems to generate valuable carotenoids and pigments.
... Interkingdom interactions between microalgae and bacteria for B12 have been reported in the literature for instance for chlorophytes [15], where a facultative interaction between the freshwater alga Lobomonas rostrata and the bacterium Mesorhizobium loti was observed. In this system, algae delivered organic carbon, probably amino acids [16], to bacteria in return for cobalamin. ...
... Only select species of bacteria and archaea are able to perform the vitamin B12 synthesis, which requires a complex set of around 20 genes [2,11]. Following a recent surge of interest [63], interactions between microalgae and bacteria for B12 have been unevenly investigated for important microalgal groups such as chlorophytes [15] and dinoflagellates [17,21]. Haptophyte microalgae, which are suspected to constitute an exclusively B12 auxotrophic taxon [22], are also ubiquitous and important contributors to primary productivity [23,28,64] and present a diverse range of interactions with bacterial communities [65,66]. ...
... One major issue is how many bacteria are needed to sustain microalgal growth. Several studies [15,17,21] observed bacteria/algae ratios ranging from 1:1 to 400:1 for mutualistic algal-bacterial co-cultures for cobalamin. This discrepancy can be explained by the large difference in size between the studied species. ...
Article
Full-text available
Haptophyte microalgae are key contributors to microbial communities in many environments. It has been proposed recently that members of this group would be virtually all dependent on vitamin B12 (cobalamin), an enzymatic cofactor produced only by some bacteria and archaea. Here, we examined the processes of vitamin B12 acquisition by haptophytes. We tested whether co-cultivating the model species Tisochrysis lutea with B12-producing bacteria in vitamin-deprived conditions would allow the microalga to overcome B12 deprivation. While T. lutea can grow by scav-enging vitamin B12 from bacterial extracts, co-culture experiments showed that the algae did not receive B12 from its associated bacteria, despite bacteria/algae ratios supposedly being sufficient to allow enough vitamin production. Since other studies reported mutualistic algae-bacteria interactions for cobalamin, these results question the specificity of such associations. Finally, cultivating T. lutea with a complex bacterial consortium in the absence of the vitamin partially rescued its growth, highlighting the importance of microbial interactions and diversity. This work suggests that direct sharing of vitamin B12 is specific to each species pair and that algae in complex natural communities can acquire it indirectly by other mechanisms (e.g., after bacterial lysis).
... Further, the system has been extensively studied in the laboratory. Previous studies of a closely related system comprising the naturally B 12 -dependent alga Lobomonas rostrata, have demonstrated mutualistic growth dynamics predicated on the exchange of vitamin B 12 and organic carbon photosynthate [38,40]. The relative proportions of the two organisms are stably maintained over hundreds of generations, but can be perturbed by supplementation with cobalamin or an organic carbon source like glycerol [40]. ...
... Previous studies of a closely related system comprising the naturally B 12 -dependent alga Lobomonas rostrata, have demonstrated mutualistic growth dynamics predicated on the exchange of vitamin B 12 and organic carbon photosynthate [38,40]. The relative proportions of the two organisms are stably maintained over hundreds of generations, but can be perturbed by supplementation with cobalamin or an organic carbon source like glycerol [40]. The effect of environment geometry on the mutualistic dynamics of spatially separated populations was also recently modelled mathematically, and realised experimentally [41]. ...
... The algal and bacterial carbon yields were estimated from dry mass measurements and EA-IRMS analysis. The carrying capacity for axenic bacteria was obtained from fitting a logistic growth equation to data obtained by [40] for M. japonicum grown axenically with 0.1% glycerol. The few remaining parameters were obtained from fitting the model to the main stable isotope experiments in this work, see Results. ...
Article
Full-text available
Microbial communities are of considerable significance for biogeochemical processes, for the health of both animals and plants, and for biotechnological purposes. A key feature of microbial interactions is the exchange of nutrients between cells. Isotope labelling followed by analysis with secondary ion mass spectrometry (SIMS) can identify nutrient fluxes and heterogeneity of substrate utilisation on a single cell level. Here we present a novel approach that combines SIMS experiments with mechanistic modelling to reveal otherwise inaccessible nutrient kinetics. The method is applied to study the onset of a synthetic mutualistic partnership between a vitamin B 12 -dependent mutant of the alga Chlamydomonas reinhardtii and the B 12 -producing, heterotrophic bacterium Mesorhizobium japonicum , which is supported by algal photosynthesis. Results suggest that an initial pool of fixed carbon delays the onset of mutualistic cross-feeding; significantly, our approach allows the first quantification of this expected delay. Our method is widely applicable to other microbial systems, and will contribute to furthering a mechanistic understanding of microbial interactions.
... O. tauri picoplanktonic cells (<2 µm) are auxotrophic for vitamin B1 (thiamine) and vitamin B12 (cobalamin). They depend on exogenous sources of vitamin or vitamin precursors for growth [16][17][18][19][20]. O. tauri possesses the metH gene coding for vitamin B12 methionine synthase but lacks the metE gene coding for B12-independent methionine synthase which allows growth in the absence of vitamin B12 [21]. ...
... It is intriguing that many oligotrophic species such as O. tauri are nonetheless vitamin auxotrophs [20,24] and so must be able to obtain a ready source of these organic micronutrients from their surroundings. Specific biotic interactions between algae and bacteria have been shown to take place for B12 acquisition to the algae from the bacteria [18,19] that in exchange benefit from algal exudates [18,22]. Recent studies have demonstrated that heterotrophic bacteria can satisfy microalgal requirements for B12 via mutualistic interactions [6,18]. ...
... The M. algicola OT growth phase matched the decline in O. tauri cells, suggesting that the bacteria fed on the exudates or dead cells of the algae. A study by Trombetta and collaborators during bloom period in mediterranean coast [7] revealed evidence of positive interactions between phytoplankton and bacteria that suggest that vitamin-synthesising bacteria would provide vitamins to phytoplankton in exchange for organic carbon [19,66,67]. Our results show that without an adequate carbon source, M. algicola is difficult to cultivate and grows particularly well in phytoplanktonic cultures in which it probably finds additional nutrients provided by living and/or dead algal cells. ...
Article
Full-text available
Although interactions between microalgae and bacteria are observed in both natural environment and the laboratory, the modalities of coexistence of bacteria inside microalgae phyco-spheres in laboratory cultures are mostly unknown. Here, we focused on well-controlled cultures of the model green picoalga Ostreococcus tauri and the most abundant member of its phycosphere, Marinobacter algicola. The prevalence of M. algicola in O. tauri cultures raises questions about how this bacterium maintains itself under laboratory conditions in the microalga culture. The results showed that M. algicola did not promote O. tauri growth in the absence of vitamin B12 while M. algicola depended on O. tauri to grow in synthetic medium, most likely to obtain organic carbon sources provided by the microalgae. M. algicola grew on a range of lipids, including triacylglycerols that are known to be produced by O. tauri in culture during abiotic stress. Genomic screening revealed the absence of genes of two particular modes of quorum-sensing in Marinobacter genomes which refutes the idea that these bacterial communication systems operate in this genus. To date, the 'opportunistic' behaviour of M. algicola in the laboratory is limited to several phytoplanktonic species including Chlorophyta such as O. tauri. This would indicate a preferential occurrence of M. algicola in association with these specific microalgae under optimum laboratory conditions.
... There are several possible hypotheses for bacterial B 12 excretion, ranging from as simple as B 12 release on bacterial cell death (Haines and Guillard, 1974;Droop, 2007), to B 12 export systems that may be regulated by algae (Kazamia et al., 2012;Grant et al., 2014;Cruz-L opez and Maske, 2016;Peaudecerf et al., 2018). The BtuBFCD complex in Gram-negative bacteria and the BtuFCD complex in Gram-positive bacteria are the best characterized prokaryotic systems for B 12 uptake (Rodionov et al., 2003;Degnan et al., 2014a), but although there is speculation that many vitamin transporters may be bidirectional, this has not been confirmed for cobalamin (Romine et al., 2017). ...
... In P. putida, however, which unlike the rhizobial strains encodes the outer membrane B 12 transporter btuB, a substantially smaller portion of detectable B 12 was in the media. Considering that the proportion of B 12 in the medium was highest for M. loti, as well the fact that stable co-cultures form between M. loti and the C. reinhardtii relative, Lobomonas rostrata (Kazamia et al., 2012), we chose M. loti for further axenic and co-culture experiments. ...
... A similar study of the symbiosis between the B 12dependent alga L. rostrata and M. loti found that B 12 production increased in the presence of L. rostrata (Kazamia et al., 2012;Grant et al., 2014). To determine whether the same was true with metE7 we collected further data from axenic cultures of M. loti grown in TP medium with glycerol or co-cultures of metE7 and M. loti in TP medium alone. ...
Article
Full-text available
Cobalamin (vitamin B 12) is a cofactor for essential metabolic reactions in multiple eukaryotic taxa, including major primary producers such as algae, and yet only prokaryotes can produce it. Many bacteria can colonize the algal phycosphere, forming stable communities that gain preferential access to photosynthate and in return provide compounds such as B 12. Extended coexistence can then drive gene loss, leading to greater algal-bacterial interdependence. In this study, we investigate how a recently evolved B 12-dependent strain of Chlamydomonas reinhardtii, metE7, forms a mutual-ism with certain bacteria, including the rhizobium Mesorhizobium loti and even a strain of the gut bacterium E. coli engineered to produce cobalamin. Although metE7 was supported by B 12 producers, its growth in co-culture was slower than the B 12-independent wild-type, suggesting that high bacterial B 12 provision may be necessary to favour B 12 auxotrophs and their evolution. Moreover, we found that an E. coli strain that releases more B 12 makes a better mutualistic partner, and although this trait may be more costly in isolation, greater B 12 release provided an advantage in co-cultures. We hypothesize that, given the right conditions, bacteria that release more B 12 may be selected for, particularly if they form close interactions with B 12-dependent algae.
... Overall, the eukaryote community composition was relatively less affected by the additions of B vitamins and inorganic nutrients than the prokaryote community composition in this productive region. This suggest that eukaryotes may obtain B vitamins through biotic relationships being more dependent on the existence of close interactions among other microorganisms (such as mutualism or predation) than on exogenous inputs (7,(45)(46)(47)(48). Among the heterotrophic bacteria, the addition of vitamin B 12 mostly had a negative effect on Rhodobacterales (presumably prototrophic [32]) and Flavobacteriales (presumably auxotrophic [5]) populations. ...
... The fact that the negative impact of B vitamins was particularly pronounced among relatively abundant taxa points to an indirect effect, implying a stimulation of bacterivores that in turn would forage on the most abundant groups. The decrease in Rhodobacterales when B-vitamin concentrations are high could subsequently affect autotrophic algae by altering mutualistic interactions whereby bacteria supply B 12 to the algae in exchange for fixed carbon (46,49). ...
Article
Full-text available
B vitamins are essential cofactors for practically all living organisms on Earth that are produced by a selection of microorganisms. An imbalance between high demand and limited production, in concert with abiotic processes, may explain the low availability of these vitamins in marine systems. Natural microbial communities from surface shelf water in the productive area off NW Spain were enclosed in mesocosms in winter, spring and summer 2016. In order to explore the impact of B-vitamin availability on microbial community composition (16S and 18S rRNA gene sequence analysis) and bacterial function (metatranscriptomics analysis) in different seasons, enrichment experiments were conducted with seawater from the mesocosms. Our findings revealed that significant increases in phytoplankton or prokaryote biomass associated with B12 and/or B1 amendments were not accompanied by significant changes in community composition, suggesting that most of the microbial taxa benefited from the external B-vitamin supply. Metatranscriptome analysis suggested that many bacteria were potential consumers of B12 and B1 vitamins, although the relative abundance of reads related to synthesis was ca. 3.6-fold higher than that related to uptake. Alteromonadales and Oceanospirillales accounted for important portions of B1 and B12 vitamin synthesis gene transcription, despite accounting for only minor portions of the bacterial community. Flavobacteriales appeared to be mostly involved in B12 and B1 vitamin uptake and Pelagibacterales expressed genes involved in B1 vitamin uptake. Interestingly, the relative expression of B12 and B1 vitamin synthesis genes among bacteria strongly increased upon inorganic nutrient amendments. Collectively, these findings suggest that upwelling events intermittently occurring during spring and summer in productive ecosystems may ensure an adequate production of these cofactors to sustain high levels of phytoplankton growth and biomass. Importance Section B-vitamins are essential growth factors for practically all living organisms on Earth that are produced by a selection of microorganisms. An imbalance between high-demand and limited-production may explain the low concentration of these compounds in marine systems. In order to explore the impact of B-vitamin availability on bacteria and algae in the coastal waters off NW Spain, six experiments were conducted with natural surface water enclosed in winter, spring and summer. Our findings revealed that increases in phytoplankton or bacteria growth associated with B12 and/or B1 amendments were not accompanied by significant changes in community composition, suggesting that most microorganisms benefited from the B-vitamin supply. Our analyses confirmed the role of many bacteria as consumers of B12 and B1 vitamins, although the relative abundance of genes related to synthesis was ca. 3.6-fold higher than that related to uptake.Interestingly, prokaryote expression of B12 and B1-synthesis genes strongly increased when inorganic nutrient were added. Collectively, these findings suggest that upwelling of cold and nutrient-rich waters occurring during spring and summer in this cooastal area may ensure an adequate production of B vitamins to sustain high levels of algae growth and biomass.
... Moreover, it is found that the heterotrophic bacterium Mesorhizobium sp. promotes the biomass productivity of the vitamin B12-dependent alga, Lobomonas rostrata [47]. Chlamydomonas reinhardtii encodes for a B12-independent methionine synthase (MetE) so it does not need vitamin B12 for growth. ...
... The presence of C. reinhardtii with Mesorhizobium sp. leads to a reduction in MetE expression, indicating that vitamin B12 can be transported from the B12-independent algae by the bacterium [47]. In 1995 it was reported that an oligotrophic and halophilic bacterium, Halomonas sp., enhanced the iron available to Dunaliella bardawil through the ability of this bacterium to give siderophores which increase the solubility of Fe, thus enhancing its availability to Dunaliella and promoting its survival under insufficient Fe conditions [48]. ...
Chapter
Great attention has been received with regard to carbon dioxide (CO2) sequestration and water contamination removal. Much research has been done to study this topic, although the ecofriendly, economics, and sustainability of these technologies are considered a concern for bioremediation and CO2 sequestration. Algae, as a green technology, are good performance tools for these purposes because of their low cost and large available quantities. There is integration between CO2 sequestration rate and wastewater bioremediation, where the algal biomass production can be enhanced by adding CO2 which improves treatment efficiency. The bioremediation can be categorized according to the nature of the wastewater into two types: industrial and domestic. The first type proceeds by either bioaccumulation or a biosorption mechanism, while the second is achieved by algal bacterial symbiosis. The present chapter will discuss the integration roles of algae toward the CO2 sequestration process, wastewater bioremediation, and biomass accumulation for possible use in biofuel production.
... In corals, the microbial community performs critical functions for the coral holobiont including pathogen protection, sulfur, and nitrogen cycling as well as beneficial modulations of the host microhabitat (Rosenberg et al. 2009;Ceh et al. 2013;Krediet et al. 2013). Benefits of bacterial communities for an algal host have been documented in free-living algae as well (e.g., Kazamia et al. 2012). Some bacteria can provide a local supply of essential nutrient compounds required by the algae, including nitrogen, inorganic carbon, vitamin B 12 (cobalamin), and growth-promoting hormones (Kouzuma and Watanabe 2015). ...
... Previous research into immobilized algae-bacteria co-cultures have observed similar formations of aggregates and biofilms, which resulted in improved growth and stability (de-Bashan et al. 2011(de-Bashan et al. , 2016. This proximity, in a gel compared to liquid culture, may facilitate and/or stabilize the interactions between the algae and bacteria for provision of photosynthate from the algae and in return growth-enhancing micronutrients (e.g., vitamins) and gases (e.g., CO 2 ) from bacteria (Kazamia et al. 2012;Paerl et al. 2015;Higgins et al. 2016;Helliwell 2017). ...
Article
Full-text available
Photosynthetic microalgae are an attractive source of food, fuel, or nutraceuticals, but commercial production of microalgae is limited by low spatial efficiency. In the present study we developed a simple photosynthetic hydrogel system that cultivates the green microalga, Marinichlorella kaistiae KAS603, together with a novel strain of the bacteria, Erythrobacter sp. We tested the performance of the co-culture in the hydrogel using a combination of chlorophyll-a fluorimetry, microsensing, and bio-optical measurements. Our results showed that growth rates in algal-bacterial hydrogels were about threefold enhanced compared to hydrogels with algae alone. Chlorophyll-a fluorimetry-based light curves found that electron transport rates were enhanced about 20% for algal-bacterial hydrogels compared to algal hydrogels for intermediate irradiance levels. We also show that the living hydrogel is stable under different environmental conditions and when exposed to natural seawater. Our study provides a potential bio-inspired solution for problems that limit the space-efficient cultivation of microalgae for biotechnological applications.
... Bacteria act as the exogenous source for these compounds, explaining this tight-knit association between algae and bacteria. Such a vitaminbased symbiotic association was observed between green alga Lobomonas rostrate and bacterium Mesorhizobium loti in a binary culture system and between bacterium Sinorhizobium meliloti 1021 and Chlamydomonas reinhardtii (Kazamia et al., 2012;Grant et al., 2014). The biosynthetic pathways for these compounds are present in a vast array of bacterial species (Croft et al., 2005;Grant et al., 2014;Helliwell et al., 2014) and are also readily available for consumption. ...
... Microalgae-bacterial symbiosis provides various advantages over algal monocultures, such as primarily algae provide with oxygen via photosynthesis, different organic exudates promoting bacterial growth, and secreted various toxic metabolites inhibiting undesired bacterial growth hence preventing competition among bacterial partner in the co-culture system (Riquelme and Avendaño-Herrera, 2003) (Fig. 1), whereas, the ecological niche being already occupied by the prevailing bacterial species also prevented other undesirable bacteria from invading the system. This phenomenon could be explained by the competitive exclusion principle of community ecology (Kazamia et al., 2012). Therefore, this approach could be beneficial at a large scale and additionally in places where maintaining a sterile environment is challenging. ...
Article
There is a growing global recognition that microalgae-based biofuel are environment-friendly and economically feasible options because they incur several advantages over traditional fossil fuels. Also, the microalgae can be manipulated for extraction of value-added compounds such as lipids (triacylglycerols), carbohydrates, polyunsaturated fatty acids, proteins, pigments, antioxidants, various antimicrobial compounds, etc. Recently, there is an increasing focus on the co-cultivation practices of microalgae with other microorganisms to enhance biomass and lipid productivity. In a co-cultivation strategy, microalgae grow symbiotically with other heterotrophic microbes such as bacteria, yeast, fungi, and other algae/microalgae. They exchange nutrients and metabolites; this helps to increase the productivity, therefore facilitating the commercialization of microalgal-based fuel. Co-cultivation also facilitates biomass harvesting and waste valorization, thereby help to build an algal biorefinery platform for bioenergy production along with multivariate high value bioproducts and simultaneous waste bioremediation. This article comprehensively reviews various microalgae cultivation practices utilizing co-culture approaches with other algae, fungi, bacteria, and yeast. The review mainly focuses on the impact of several binary culture strategies on biomass and lipid yield. The advantages and challenges associated with the procedure along with their respective cultivation modes have also been presented and discussed in detail.
... Experiments assessing the SOM without the effects of heterotrophic bacteria have so far been scarce. In return for utilization of the organic carbon fixed by cyanobacteria, the heterotrophic bacteria benefit them by providing complex and unidentified substances like vitamins and bioavailable trace metals (Amin et al., 2009;Kazamia et al., 2012). Because of this, rendering axenic cyanobacteria is difficult for laboratorial cultures. ...
... It was worth noting that the final cell density of Synechococcus at 15 • C was insignificant between Syn and SynB cultures. This may be explained that the heterotrophic bacteria may have activated the growth of Synechococcus through providing them essential micronutrients (Hayashi et al., 2011;Kazamia et al., 2012), but such an activated function just started when temperature is over a threshold of e.g., higher than 18 • C (Figure 1). ...
Article
Full-text available
Synechococcus is one group of main primary producers and plays a key role in oceanic carbon fixation and transformation. To explore how the temperature rise affects the bioavailability of Synechococcus -derived dissolved organic matter (SOM) and whether this effect would be altered by the involvement of heterotrophic bacteria, we compared the optical and molecular properties of the SOM of axenic Synechococcus sp. PCC7002 culture ( Syn ) to that with associated heterotrophic bacteria ( Syn B) under 15, 18, and 21 ° C growth temperatures at exponential and decay growth phases. Our results showed that the temperature rise increased the bioavailability of the SOM of both Syn and Syn B cultures by lowering the proportion of the hydrogen-poor and double-bond structure-rich humus-like components and highly unsaturated substances, as indicated by the increase of spectral slope ratio (S R ) and biological index (BIX) and decrease of humification index (HIX). Moreover, the involvement of heterotrophic bacteria modified the Synechococcus -derived SOM, together with its intracellular dissolved organic matter (DOM) excludes, lowering the SOM bioavailability. Our results indicated that the warming in climate change scenario may enhance the bioavailability of the Synechococcus -derived SOM although it may be tempered by the involvement of heterotrophic bacteria, providing an insight for preservation of the organic carbon pool in global oceans.
... Coculture works of algae and bacteria had demonstrated that vitamin B 12 is indispensable in maintaining the host-microbe symbioses, in which B 12 is exclusively produced by bacteria in exchange for carbon source from the algal host (Croft et al., 2005;Croft et al., 2006;Kazamia et al., 2012;Grant et al., 2014). Although eukaryotes do not produce vitamin B 12 , genomic surveys showed that approximately half of algal species across different phyla are predicted to obligately require exogenous B 12 for growth, as one of their essential enzymes, methionine synthase (MetH), requires such micronutrient as a coenzyme (Helliwell et al., 2011). ...
... Indeed, selection experiments on a B 12 -independent alga showed that constant provisioning of sufficient B 12 can drive functional loss of MetE in a short run, and ultimately lead to the evolution of B 12 auxotroph, highlighting the influence of altering B 12 dependency in cellular physiology and evolutionary trajectory (Helliwell et al., 2015). Therefore, B 12 metabolism not only can create specific reciprocal exchange networks but also acts as a crucial driver of symbiotic partnerships (Kazamia et al., 2012;Kazamia et al., 2016) and microbial community dynamics (Joglar et al., 2021), which manifest the importance of elucidating the genetic attributes underpinning the metabolism of such essential micronutrient. ...
Article
Full-text available
Cobalamin (vitamin B12) is an essential micronutrient required by both prokaryotes and eukaryotes. Nevertheless, with high genetic and metabolic cost, de novo cobalamin biosynthesis is exclusive to a subset of prokaryotic taxa. Many Cyanobacterial and Archaeal taxa have been implicated in de novo cobalamin biosynthesis in epi- and mesopelagic ocean respectively. However, the contributions of Gammaproteobacteria particularly the family ‘Psychromonadaceae’ is largely unknown. Through phylo-pangenomic analyses using concatenated single-copy proteins and homologous gene clusters respectively, the phylogenies within ‘Psychromonadaceae’ recapitulate both their taxonomic delineations and environmental distributions. Moreover, uneven distribution of cobalamin de novo biosynthetic operon and cobalamin-dependent light-responsive regulon were observed, and of which the linkages to the environmental conditions where cobalamin availability and light regime can be varied respectively were discussed, suggesting the impacts of ecological divergence in shaping their disparate cobalamin-related metabolisms. Functional analysis demonstrated a varying degree of cobalamin dependency for both central metabolic processes and cobalamin-mediated light-responsive regulation, and underlying sequence characteristics of cis- and trans- regulatory elements were revealed. Our findings emphasized the potential roles of cobalamin in shaping the ecological distributions and driving the metabolic evolution in the marine bacterial family ‘Psychromonadaceae’, and have further implications for an improved understanding of nutritional interdependencies and community metabolism modulated by cobalamin.
... Une amélioration de la croissance des micro-algues par la présence des bactéries est possible via l'échange de métabolites ou de macronutriments (vitamine, carbone, azote, phosphore, etc.) [134,135,136,137,26,138], la réduction de stress [139], ou encore via l'exclusion d'agents compétiteurs ou pathogènes opportunistes potentiels [140,141]. Un exemple typique d'une relation mutualiste entre les micro-algues et les bactéries serait de considérer que les micro-algues utilisent le CO 2 par la photosynthèse pour générer de l'O 2 , qui pourrait être utilisé par les bactéries hétérotrophes pour assimiler et dégrader le carbone, l'azote et le phosphore à l'état organique. En outre, le CO 2 , l'azote inorganique et le phosphore, libérés après le métabolisme aérobie des bactéries, pourraient être utilisés comme nutriments par les micro-algues pour la photosynthèse ultérieure [87,28]. ...
... Les interactions micro-algues-bactéries sont généralement classées comme des interactions de type mutulalisme/commensalisme (e.g. [141,137]) ou encore de type facilitation (e.g. [145,139]). ...
Thesis
Dans le contexte de l’utilisation des microalgues pour la bioremédiation d’effluents et la production de biomasse d’intérêt industriel, la stabilité et les performances des systèmes de production sont des enjeux majeurs. Une des voies de recherche privilégiées est la mise à profit de la diversité des microalgues en assemblages (polycultures) pour l’amélioration des performances de la production. Néanmoins, l’exploitation de ces assemblages complexes en système ouvert extérieur est sujette à divers stress biotiques (microalgues indésirables ou bactéries compétitrices) et abiotiques (limitation des ressources, notammentl’azote et la lumière) qui influencent les interactions au sein des assemblages, rendant difficiles la prédictionet l’optimisation de la production. L’objectif de la présente thèse est de proposer des méthodes etdes outils permettant de comprendre, prédire et optimiser la production de biomasse d’un assemblage algal(consortium microbien naturel ou artificiellement composé) sous la fluctuation des ressources et desconditions de culture. Plus particulièrement, nous avons développé des modèles mathématiques baséssur des systèmes dynamiques, qui peuvent être confrontés à des expériences en laboratoire et à l’échellepilote.Les premiers travaux de cette thèse ont consisté à choisir une méthode expérimentale pour lacaractérisation de la vitesse de croissance spécifique des microorganismes photosynthétiques en fonctionde la ressource limitante. Par ailleurs, une nouvelle méthode d’estimation fonctionnelle est proposée produisantdeux courbes de croissance qui encadrent les données de vitesse de croissance et permettant ainsides estimations dynamiques des variables d’état par intervalles garantis. Dans un deuxième temps, la nature des interactions entre deux microalgues Chlorella sorokiniana et Scenedesmus pectinatus, qui se succèdent classiquement dans les bassins extérieurs utilisés pour le traitement des eaux usées urbaines, a été caractérisée en fonction de la fluctuation des différentes formes de l’azote (NH4+/NH3) et ensuite de la lumière disponible. Les modèles mathématiques associés aux expérimentations menées au cours de cette thèse ont permis de démontrer que le développement initial d’une espèce microalgale de type opportuniste, plus résistante aux fortes teneurs en NH4+/NH3 était nécessaire pour que puisse s’établir ensuite une espèce microalgale plus efficace vis-à-vis de la faible lumière disponible dans ces procédés très turbides. Dans un troisième temps, nous avons exploré les interactions paradoxales qui existent entre les microalgues et les bactéries hétérotrophes. En effet, les microalgues stimulent, à travers l’exsudation du carbone, leurs compétiteurs pour une ressource commune : l’azote ou le phosphore. Nous avons étudié l’influence de ce phénomène en proposant un modèle dynamique en dimension quatre. L’analyse mathématique a révélé l’unicité de l’équilibre de coexistence et la robustesse de l’installation des bactéries, car il a été démontré que l’équilibre en absence de bactéries est répulsif. Nous montrons que lorsque laconcentration de la ressource minérale alimentant en continu le bioréacteur est suffisamment grande, il existe des valeurs du taux de renouvellement du réacteur pour lesquelles il y a coexistence, alors que les bactéries ne pourraient pas se développer en l’absence de microalgues dans ces mêmes conditions opératoires.Enfin, il a été montré à l’aide de simulations que lors de la coexistence, leur biomasse respectives peut osciller.Ces résultats témoignent de la complexité des interactions biotiques, fournissent des méthodes applicables à d’autres organismes modèles permettant de les étudier, et soulèvent des possibilités d’application prometteuses pour l’optimisation et le contrôle des systèmes dynamiques de procédés pour les travaux futurs.
... Compilation of the requirements of fifty-four diatom species demonstrated that 32, 7, and 0 species required cobalamin, thiamine, and biotin, respectively (Croft et al. 2005). As only certain prokaryotes are capable of its biosynthesis (Shelton et al. 2019), vitamin B 12 (Fig. 4, top panel) is considered to be a particularly pertinent exchange molecule mediating algal-bacteria interactions (Croft et al. 2005;Kazamia et al. 2012). This vitamin is necessary as a cofactor to the B 12 -dependent isoform of methionine synthase (METH). ...
... These findings highlight the importance of vitamin B 12 in chemical exchanges between diatoms and bacteria in large areas of the ocean. The evidence for the role of vitamin B 12 in underpinning a range of mutualistic interactions between bacteria and diverse algal taxa (Kazamia et al. 2012;Wagner-Döbler et al. 2010) emphasizes the importance of vitamin cycling in cross-kingdom microbial interactions more broadly. ...
... The bacteria supplied vitamin B 12 , used primarily as a cofactor for the vitamin B 12 -dependent methionine synthase, in return for fixed carbon (Croft et al. 2005). A coculture composed of the green microalga Lobomonas rostrata, auxotrophic for vitamin B 12 , and the bacterium Mesorhizobium loti, provided further insight into mutualism based on vitamin B 12 provision at biochemical and molecular levels (Kazamia et al. 2012). Experiments on semisolid medium showed that direct physical contact is not required for supplying vitamin B 12 to microalgae (Kazamia et al. 2012). ...
... A coculture composed of the green microalga Lobomonas rostrata, auxotrophic for vitamin B 12 , and the bacterium Mesorhizobium loti, provided further insight into mutualism based on vitamin B 12 provision at biochemical and molecular levels (Kazamia et al. 2012). Experiments on semisolid medium showed that direct physical contact is not required for supplying vitamin B 12 to microalgae (Kazamia et al. 2012). ...
Article
Interactions amongst marine microalgae and heterotrophic bacteria drive processes underlying major biogeochemical cycles and are important for many artificial systems. These dynamic and complex interactions span the range from cooperative to competitive and it is the diverse and intricate networks of metabolites and chemical mediators that are predicted to principally dictate the nature of the relationship at any point in time. Recent advances in technologies to identify, analyze, and quantify metabolites have allowed for a comprehensive view of the molecules available for exchange and/or reflective of organismal interactions, setting the stage for development of mechanistic understanding of these systems. Here, we (i) review the current knowledge landscape of microalgal-bacterial interactions by focusing on metabolomic studies of selected, simplified model systems; (ii) describe the state of the field of metabolomics, with specific focus on techniques and approaches developed for microalga-bacterial interaction studies; (iii) outline the main approaches for development of mathematical models of these interacting systems, which collectively have the power to enhance interpretation of experimental data and generate novel testable hypotheses. We share the viewpoint that a comprehensive and integrated series of -omics approaches that include theoretical formulations are necessary to develop predictive and mechanistic understanding of these biological entities.
... Cobalamin has an important role in microbial interactions and is regularly considered as a model metabolite exchanged in beneficial microbial interactions (Ramanan et al., 2016). Auxotrophic phytoplankton can acquire cobalamin through sustaining obligate or facultative interactions with B 12 -producing bacteria and/or archaea or by uptake of the vitamin from its surrounding environment, referred to as scavenging (Amin et al., 2012;Kazamia et al., 2012;Bertrand et al., 2015). However, the strategy an organism uses to obtain sufficient cobalamin is likely affected by the availability of the nutrient or associated producer. ...
... The factors that influence methods of cobalamin acquisition and the regulation of cobalamin transfer or exchange between organisms are still poorly understood although relevant for understanding CIC. Interactions between cobalamin producers and consumers can be selected for and strengthened, in part, by the reciprocal transfer of nutrients and/or the active selection of beneficial bacteria through secondary metabolites (Kazamia et al., 2012;Grant et al., 2014;Shibl et al., 2020). In particular, the exchange of organic, labile carbon for cobalamin is relatively well documented, and it is expected that other nutrients, such as nitrogen species, amino acids, sulfonates, sugar derivatives or specific growth factors like indol-3-acetic acid could be exchanged as well (Amin et al., 2012;Ramanan et al., 2016;Durham et al., 2019). ...
Article
Full-text available
The simultaneous limitation of productivity by two or more nutrients, commonly referred to as nutrient co-limitation, affects microbial communities throughout the marine environment and is of profound importance because of its impacts on various biogeochemical cycles. Multiple types of co-limitation have been described, enabling distinctions based on the hypothesized mechanisms of co-limitation at a biochemical level. These definitions usually pertain to individuals and do not explicitly, or even implicitly, consider complex ecological dynamics found within a microbial community. However, limiting and co-limiting nutrients can be produced in situ by a subset of microbial community members, suggesting that interactions within communities can underpin co-limitation. To address this, we propose a new category of nutrient co-limitation, community interaction co-limitation (CIC). During CIC, one part of the community is limited by one nutrient, which results in the insufficient production or transformation of a biologically produced nutrient that is required by another part of the community, often primary producers. Using cobalamin (vitamin B12) and nitrogen fixation as our models, we outline three different ways CIC can arise based on current literature and discuss CIC’s role in biogeochemical cycles. Accounting for the inherent and complex roles microbial community interactions play in generating this type of co-limitation requires an expanded toolset – beyond the traditional approaches used to identify and study other types of co-limitation. We propose incorporating processes and theories well-known in microbial ecology and evolution to provide meaningful insight into the controls of community-based feedback loops and mechanisms that give rise to CIC in the environment. Finally, we highlight the data gaps that limit our understanding of CIC mechanisms and suggest methods to overcome these and further identify causes and consequences of CIC. By providing this framework for understanding and identifying CIC, we enable systematic examination of the impacts this co-limitation can have on current and future marine biogeochemical processes.
... A model interaction for the exchange of vitamin B12 is the one created between the soil rhizobiaceae Mesorhizobium loti and the freshwater green microalga Lobomonas rostrata, where M. loti supplies vitamin B12, and in return, the bacterium receives fixed carbon from the microalga [45][46][47]. Mathematical models that analyze the nutrient exchange between the microorganisms showed that M. loti regulates the production of cobalamin according to the requirements of the microalga rather than simply releasing nutrients to the medium, in this way creating a true mutualistic interaction with L. rostrata [46]. Using quantitative isobaric tagging proteomics (iTRAQ), the proteome of L. rostrata growing axenically with the addition of exogenous vitamin B12 or in co-culture with M. loti was analyzed [47]. ...
... Chlamydomonas reinhardtii is a B12-independent microalga that encodes a B12independent methionine synthase gene (METE) that is suppressed with the addition of exogenous B12. In another synthetic interaction with M. loti, it showed a reduction of METE expression, due to the supply of the vitamin by the bacterium [45]. ...
Article
Full-text available
Engineered mutualistic consortia of microalgae and bacteria may be a means of assembling a novel combination of metabolic capabilities with potential biotechnological advantages. Microalgae are promising organisms for the sustainable production of metabolites of commercial interest, such as lipids, carbohydrates, pigments, and proteins. Several studies reveal that microalgae growth and cellular storage of these metabolites can be enhanced significantly by co-cultivation with growth-promoting bacteria. This review summarizes the state of the art of microalgae–bacteria consortia for the production of microalgal metabolites. We discuss the current knowledge on microalgae–bacteria mutualism and the mechanisms of bacteria to enhance microalgae metabolism. Furthermore, the potential routes for a microalgae–bacteria biorefinery are outlined in an attempt to overcome the economic failures and negative energy balances of the existing production processes.
... For instance, in the most famous research on the interaction of Emiliania Huxleyi, known as single cell marine microalgae, with Roseobacter, the mutual interactions were formed between the specific species since the microenvironment of each microalgal cell was not similar; thus, the nutrient exchange between the microalgae and bacteria was the main contributor to spur microalgal growth [148]. Micronutrients such as vitamins [149,150] and macronutrients such as nitrogen and carbon [150][151][152][153] are frequently exchanged between the microalgae and bacteria. Bacteria also excrete EPS, similar to the SAPs from microalgae and plant hormones [150], which can increase the growth rate of microalgal cells in forming attachment [154]. ...
Article
Third-generation biofuels that are derived from microalgal biomass have gained momentum as a way forward in the sustainable production of biodiesel. Such efforts are propelled by the intention to reduce our dependence on fossil fuels as the primary source of energy. Accordingly, growing microalgal biomass in the form of suspended cultivation has been a conventional technique for the past few decades. To overcome the inevitable harvesting shortcomings arising from the excessive energy and time needed to separate the planktonic microalgal cells from water medium, researchers have started to explore attached microalgal cultivation systems. This cultivation mode permits the ease of harvesting mature microalgal biomass, circumventing the need to employ complex harvesting techniques to single out the cells, and is economically attractive. However, the main bottleneck associated with attached microalgal growth is low biomass production due to the difficulties the microalgal cells have in forming attachment and populating thereafter. In this regard, the current review encompasses the novel techniques adopted to promote attached microalgal growth. The physicochemical effects such as the pH of the culture medium, hydrophobicity, as well as the substratum surface properties and abiotic factors that can determine the fate of exponential growth of attached microalgal cells, are critically reviewed. This review aims to unveil the benefits of an attached microalgal cultivation system as a promising harvesting technique to produce sustainable biodiesel for lasting applications.
... Many algae, including some cyanobacteria [96][97][98], require vitamin B 12 for growth yet are unable to produce it and must rely on exogenous B 12 [97]. Microcystis requires vitamin B 12 for the methionine biosynthesis pathway. ...
Article
Full-text available
Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates ( Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were sequenced on a PacBio Sequel system. These genomes ranged in size from 3.1 Mbp ( Exiguobacterium sp. JMULE1) to 5.7 Mbp ( Enterobacter sp. JMULE2). The genomes were analyzed for genes relating to critical metabolic functions, including nitrogen reduction and carbon utilization. All five of the sequenced genomes contained genes that could be used in potential signaling and nutrient exchange between the bacteria and cyanobacteria such as Microcystis . Gene expression signatures of algal-derived carbon utilization for two isolates were identified in Microcystis blooms in Lake Erie and Lake Tai ( Taihu ) at low levels, suggesting these organisms are active and may have a functional role during Microcystis blooms in aggregates, but were largely missing from whole water samples. These findings build on the growing evidence that the bacterial microbiome associated with bloom-forming algae have the functional potential to contribute to nutrient exchange within bloom communities and interact with important bloom formers like Microcystis .
... Most Rhodophyta, including the Florideophyceae -to which A. vermiculophyllum belongs-express the cobalamin-dependent methionine synthase (METH, Provasoli and Carlucci 1974) but are cobalamin auxotroph and depend on microbial symbionts to acquire this vitamin (Croft et al. 2005). Cobalamin auxotrophs may obtain the vitamin in exchange for fixed carbon (e.g., glycerol, Kazamia et al. 2012). Also Gracilariopsis chorda, the closest relative of A. vermiculophyllum of which a genome sequence is currently available, encodes METH and is thus dependent on the acquisition of cobalamin from microbial sources. ...
Article
Full-text available
This work introduces Waterburya agarophytonicola Bonthond and Shalygin gen. nov., sp. nov, a baeocyte producing cyanobacterium that was isolated from the rhodophyte Agarophyton vermiculophyllum (Ohmi) Gurgel et al., an invasive seaweed that has spread across the northern hemisphere. The new species genome reveals a diverse repertoire of chemotaxis and adhesion related genes, including genes coding for type IV pili assembly proteins and a high number of genes coding for filamentous hemagglutinin family (FHA) proteins. Among a genetic basis for the synthesis of siderophores, carotenoids and numerous vitamins, W. agarophytonicola is potentially capable of producing cobalamin (vitamin B12), for which A. vermiculophyllum is an auxotroph. With a taxonomic description of the genus and species and a draft genome, this study provides as a basis for future research, to uncover the nature of this geographically independent association between seaweed and cyanobiont.
... Analogous to rhizosphere in plants, phycosphere is proposed, but it is not studied systematically in commercial production (Wirth et al., 2020). Besides parasitic microbes, many microbes observed in the cultivation have a mutualistic relationship with microalgae and provide essential vitamins for microalgal growth (Kazamia et al., 2012;Yao et al., 2019;Kaur Nagi et al., 2021). Thus, careful management of microbial food-web structure can maximize crop protection and improve crop yield for industrial algal biofuels production (Yun et al., 2016). ...
Article
Full-text available
Microalgae offer a great potential to contribute significantly as renewable fuels and documented as a promising platform for algae-based bio refineries. They provide solutions to mitigate the environmental concerns posed by conventional fuel sources; however, the production of microalgal biofuels in large scale production system encounters few technical challenges. High quantity of nutrients requirements and water cost constrain the scaling up microalgal biomass to large scale commercial production. Crop protection against biomass losses due to grazers or pathogens is another stumbling block in microalgal field cultivation. With our existing technologies, unless coupled with high-value or mid-value products, algal biofuel cannot reach the economic target. Many microalgal industries that started targeting biofuel in the last decade had now adopted parallel business plans focusing on algae by-products application as cosmetic supplements, nutraceuticals, oils, natural color, and animal feed. This review provides the current status and proposes a framework for key supply demand, challenges for cost-effective and sustainable use of water and nutrient. Emphasis is placed on the future industrial market status of value added by products of microalgal biomass. The cost factor for biorefinery process development needs to be addressed before its potential to be exploited for various value-added products with algal biofuel.
... C. calcitrans and T. suecica are tropical marine microalgae widely used in aquaculture hatcheries due to their nutritional value suitable for most marine filter feeders since they serve as live food for early larval stages. Furthermore, bacteria produce secondary metabolites such as nitrogen and carbon (Kim et al., 2014), vitamins (Kazamia et al., 2012;Kuo & Lin, 2013) and phytohormones (Teplitski & Rajamani, 2011) that rapidly increase the growth of specific microalgae in co-culture conditions. However, in this work, no changes in the microalgae density of C. calcitrans, T. suecica, Nannochloropsis sp. and T. weissflogii that were inoculated with both V. parahaemolyticus strains was observed. ...
Article
Full-text available
Marine microalgae are potential producers of antimicrobial compounds. Monospecific, vibrio‐free co‐cultures of marine microalgae, Chaetoceros calcitrans, Tetraselmis suecica, Nannochloropsis sp. and Thalassiosira weissflogii, at the exponential phase of growth were inoculated with two Vibrio parahaemolyticus (Vp) strains. Vp M0904, a highly virulent strain responsible for acute hepatopancreatic necrosis disease (AHPND), and Vp M0702, a non‐pathogenic strain, both at 1 × 105 CFU ml−1. Microalgae and bacterial growth, total lipids and carbohydrates were obtained at 1, 2 and 3 days post inoculation with bacteria. Ethanolic (EE) and seawater extracts (SE) of C. calcitrans were also obtained to evaluate the inhibitory activity against Vp M0904. Microalgae cellular growth was not affected by any tested bacteria throughout the experiment; in contrast, Vp M0904 was significantly (p < 0.05) inhibited in co‐culture with C. calcitrans and T. suecica. Meanwhile, Vp M0702 was significantly (p < 0.05) inhibited by all microalgae except for Nannochloropsis sp. Minor, non‐significant variations were found in the lipids and carbohydrate metabolism of all microalgae inoculated with both strains. Low CFU ml−1 of Vp M0904 was registered when it was incubated with SE of C. calcitrans at concentrations over 75 µg ml−1, however, EE did not show any antibacterial activity. The bacteriostatic effect was dependent of microalgae type and Vibrio strain. Hydrophilic compounds of C. calcitrans cells possess antibiotic activities on the highly virulent Vp M0904 responsible for AHPND, a devastating disease for farmed shrimp around the world.
... Metabolic interactions between microalgae and their associated bacteria, the latter sometimes referred to as the algal microbiome, have been recognized as an important contribution to carbon cycling in natural [1] and engineered [2] algal-dominated ecosystems. Heterotrophic bacteria consume up to 50% of the carbon fixed by algae [3], and this mineralization process often leads to an exchange of metabolites from bacteria to algae, providing a variety of micronutrients such as trace metals [4], vitamins [5][6][7], and phytohormones [8], which can be scarce in nature yet are essential for algal growth. ...
Article
Full-text available
Photosynthetic microalgae are responsible for 50% of the global atmospheric CO2 fixation into organic matter and hold potential as a renewable bioenergy source. Their metabolic interactions with the surrounding microbial community (the algal microbiome) play critical roles in carbon cycling, but due to methodological limitations, it has been challenging to examine how community development is influenced by spatial proximity to their algal host. Here we introduce a copolymer-based porous microplate to co-culture algae and bacteria, where metabolites are constantly exchanged between the microorganisms while maintaining physical separation. In the microplate, we found that the diatom Phaeodactylum tricornutum accumulated to cell abundances ~20 fold higher than under normal batch conditions due to constant replenishment of nutrients through the porous structure. We also demonstrate that algal-associated bacteria, both single isolates and complex communities, responded to inorganic nutrients away from their host as well as organic nutrients originating from the algae in a spatially predictable manner. These experimental findings coupled with a mathematical model suggest that host proximity and algal culture growth phase impact bacterial community development in a taxon-specific manner through organic and inorganic nutrient availability. Our novel system presents a useful tool to investigate universal metabolic interactions between microbes in aquatic ecosystems.
... Bacteria-microalgae synergy might also involve the production of exudates by microalgae that can support bacterial growth, possibly accelerating their oil-degrading activity [118]. On the other hand, microalgae could benefit from bacterial-mediated increase of the bioavailability of trace elements, nutrients, and growth-promoting factors [118,168,169]. For instance, as shown for a freshwater consortium of algae and bacteria [170], pyrene-degrading bacteria could both enhance microalgal growth (through the supply of phytohormones) and be stimulated by microalgal activity, in turn accelerating hydrocarbon degradation. ...
Article
Full-text available
Petroleum hydrocarbons (PHCs) are one of the most widespread and heterogeneous organic contaminants affecting marine ecosystems. The contamination of marine sediments or coastal areas by PHCs represents a major threat for the ecosystem and human health, calling for urgent, effective, and sustainable remediation solutions. Aside from some physical and chemical treatments that have been established over the years for marine sediment reclamation, bioremediation approaches based on the use of microorganisms are gaining increasing attention for their eco-compatibility, and lower costs. In this work, we review current knowledge concerning the bioremediation of PHCs in marine systems, presenting a synthesis of the most effective microbial taxa (i.e., bacteria, fungi, and microalgae) identified so far for hydrocarbon removal. We also discuss the challenges offered by innovative molecular approaches for the design of effective reclamation strategies based on these three microbial components of marine sediments contaminated by hydrocarbons.
... fixed nitrogen) and micro-nutrients (e.g. vitamin B 12 ) for algal growth 27,28 . Due to such close phytoplankton-bacteria interactions, phytoplankton biomass and bacterial biomass are tightly coupled 23 . ...
Article
Full-text available
Increasing occurrence of harmful algal blooms across the land–water interface poses significant risks to coastal ecosystem structure and human health. Defining significant drivers and their interactive impacts on blooms allows for more effective analysis and identification of specific conditions supporting phytoplankton growth. A novel iterative Random Forests (iRF) machine-learning model was developed and applied to two example cases along the California coast to identify key stable interactions: (1) phytoplankton abundance in response to various drivers due to coastal conditions and land-sea nutrient fluxes, (2) microbial community structure during algal blooms. In Example 1, watershed derived nutrients were identified as the least significant interacting variable associated with Monterey Bay phytoplankton abundance. In Example 2, through iRF analysis of field-based 16S OTU bacterial community and algae datasets, we independently found stable interactions of prokaryote abundance patterns associated with phytoplankton abundance that have been previously identified in laboratory-based studies. Our study represents the first iRF application to marine algal blooms that helps to identify ocean, microbial, and terrestrial conditions that are considered dominant causal factors on bloom dynamics.
... Other chrysophytes such as Dinobryon can supplement their growth with prey ingestion under low light conditions (Caron et al., 1993), consistent with being found during the ice-covered season. Uroglena americana is an example of an obligate phagotroph using prey to obtain growth factors (Sanders, 2011;Kazamia et al., 2012). ...
Article
Full-text available
Across much of the Arctic, lakes and ponds dominate the landscape. Starting in late September, the lakes are covered in ice, with ice persisting well into June or early July. In summer, the lakes are highly productive, supporting waterfowl and fish populations. However, little is known about the diversity and ecology of microscopic life in the lakes that influence biogeochemical cycles and contribute to ecosystem services. Even less is known about the prevalence of species that are characteristic of the seasons or whether some species persist year-round under both ice cover and summer open-water conditions. To begin to address these knowledge gaps, we sampled 10 morphometrically diverse lakes in the region of Ekaluktutiak (Cambridge Bay), on southern Victoria Island (NU, Canada). We focused on Greiner Lake, the lakes connected to it, isolated ponds, and two nearby larger lakes outside the Greiner watershed. The largest lakes sampled were Tahiryuaq (Ferguson Lake) and the nearby Spawning Lake, which support commercial sea-run Arctic char ( Salvelinus alpinus ) fisheries. Samples for nucleic acids were collected from the lakes along with limnological metadata. Microbial eukaryotes were identified with high-throughput amplicon sequencing targeting the V4 region of the 18S rRNA gene. Ciliates, dinoflagellates, chrysophytes, and cryptophytes dominated the lake assemblages. A Bray–Curtis dissimilarity matrix separated communities into under-ice and open-water clusters, with additional separation by superficial lake area. In all, 133 operational taxonomic units (OTUs) occurred either in all under-ice or all open-water samples and were considered “core” microbial species or ecotypes. These were further characterized as seasonal indicators. Ten of the OTUs were characteristic of all lakes and all seasons sampled. Eight of these were cryptophytes, suggesting diverse functional capacity within the lineage. The core open-water indicators were mostly chrysophytes, with a few ciliates and uncharacterized Cercozoa, suggesting that summer communities are mixotrophic with contributions by heterotrophic taxa. The core under-ice indicators included a dozen ciliates along with chrysophytes, cryptomonads, and dinoflagellates, indicating a more heterotrophic community augmented by mixotrophic taxa in winter.
... Mesorhizobium sp. promotes the growth of green algae (Lobomonas rostrata) by producing B12 in the reaction medium [138]. Bacterial activity is primarily enhanced by the algal secretion of polymeric compounds rich in carbohydrates, proteins, and transparent exopolymer particles [137]. ...
Article
Microalgae-based technologies mitigate the adverse impact of greenhouse gases (GHGs) by facilitating CO2 consumption. The pollutants in wastewater can be efficiently utilized for algal growth to recover resources, reduce GHGs, produce bioenergy, and achieve zero-liquid wastewater discharge. However, algal cell separation, prolonged retention time, evaporation, excess amount of sludge, low-efficiency of organic matter removal, and release of particulate matter in the treated effluent hinder the implementation of this technology. This review comprehensively discusses these issues and proposes technology based on biofilm producing algae as sustainable solutions to overcome these barriers. Furthermore, the challenges and limitations of the bacterial and microalgae synergy for removing xenobiotics are discussed. Photo degradation, bioaccumulation, and biodegradation in the algae-bacteria system are the primary mechanisms of xenobiotic removal. Additionally, emphasis is placed on algal biomass harvesting for recovery of bioenergy (such as bio-ethanol, bio-hydrogen, biogas, and bio-diesel), improved metabolism, and removal of excess nutrients. Algal cells produce enzymes for biodegradation and transformation of toxic contaminants into less harmful metabolites/moieties. Techno-economic limitations and microalgae-based CO2 bio-fixation to minimize GHG emissions are also discussed. The GHG abatement credits would help overcome high energy prices and high costs of the wastewater treatment technologies and make the algal culture technologies economically viable.
... STPKs have the capability to sense a wide array of signals and coordinate multiple cellular processes in order to generate an appropriate response [120]. A small number of transport genes and vitamin B12 genes were also detected the presence indicate that associated microbiota produces regulatory compounds and transport them to algal host it is stated previously in many studies that algae acquire vitamin B12 through a symbiotic relationship with bacteria [121][122][123]. ...
Article
Full-text available
Pyropia yezoensis is the most important commercial edible red algae in China, carrying a variety of resident microbes at its surface. To understand microbiome diversity, community structure, interactions and functions with hosts in this regard, thalli and seawater sampleswere collected from Yantai and Rizhao cultivation farms in the Yellow Sea. The thalli and seawater samples (n = 12) were collected and studied using an Illumina NovaSeq 6000 platform and 16S ribosomal RNA (rRNA) gene sequencing, along with the consideration of environmental factors. Bacterial communities in association with P. yezoensis and surrounding seawater were predominated by Cyanobacteria, Proteobacteria, and Bacteroidetes. The variability of bacterial communities related to P. yezoensis and seawater were predominantly shaped by nitrate (NO3), ammonium (NH4), and temperature. Cluster analysis revealed a close relationship between thalli (RTH and YTH) and seawater (RSW and YSW) in terms of the residing bacterial communities, respectively. PICRUSt analysis revealed the presence of genes associated with amino acid transportation and metabolism, which explained the bacterial dependence on algal-provided nutrients. This study reveals that the diversity of microbiota for P. yezoensis is greatly influenced by abiotic factors and algal organic exudates which trigger chemical signaling and transportation responses from the bacterial community, which in turn activates genes to metabolize subsequent substrates.
... Whereas inter-kingdom communication distantly resulted in the highest number of compounds. In distant and direct communication conditions, an exchange of oxygen from Chlorella and carbon dioxide from bacteria could have helped for higher productivities (Kazamia et al., 2012). In a study, when A. brasilense and B. pumilus were cultivated in close proximity of the Chlorella spp. with alginate bead via co-immobilization showed supportive effects on growth and metabolism as well as it caused higher pigment and lipid productivities (De-Bashan et al., 2002). ...
Article
In the present study, bacterial mixture (of Rhizobium and Agrobacterium) and axenic Chlorella were cultivated individually, in a mixed (co-cultured) form, and through headspace connections to study volatile organic compounds (VOCs) profiling and its effect on growth. Results indicated that VOCs produced by the axenic microalgae and microalgae co-cultured with bacteria were significantly different. Axenic Chlorella predominantly produced a flavouring organic compound 2-pentadecanone (69.54%), bacterial mixed culture produced 1-decanone, 1,2,3-butanetriol, and quinoline (15-20%), and direct co-culturing of Chlorella with bacteria predominantly produced 2-pentadecanone (32.4 %). When they were allowed to communicate distantly through headspace connection, highly diversified VOCs in large numbers but low quantities were noted, predominantly 1,2-propanediol (28.82 %). In addition, growth of the co-cultured Chlorella was 1.5 times higher, while Chlorella in headspace connection with bacterial mixture exhibited ∼3.2 times increase in growth compared to the axenic Chlorella, indicating the essential role of VOCs in growth and communication.
... (Kim et al., 2014) and Mesorhizobium sp. (Kazamia et al., 2012;Wei et al., 2020). For I. galbana, there was an increase in algal biomass accumulation and growth rate in the presence of Alteromonas sp. and Labrenzia sp. ...
Article
Full-text available
Phycospheric bacteria may be the key biological factors affecting the growth of algae. However, the studies about interaction between Isochrysis galbana and its phycospheric bacteria are limited. Here, we show that a marine heterotrophic bacterium, Alteromonas macleodii , enhanced the growth of I. galbana , and inhibited non-photochemical quenching (NPQ) and superoxide dismutase (SOD) activities of this microalgae. Further, we explored this phenomenon via examining how the entire transcriptomes of I. galbana changed when it was co-cultured with A. macleodii . Notable increase was observed in transcripts related to photosynthesis, carbon fixation, oxidative phosphorylation, ribosomal proteins, biosynthetic enzymes, and transport processes of I. galbana in the presence of A. macleodii , suggesting the introduction of the bacterium might have introduced increased production and transport of carbon compounds and other types of biomolecules. Besides, the transcriptome changed largely corresponded to reduced stress conditions for I. galbana , as inferred from the depletion of transcripts encoding DNA repair enzymes, superoxide dismutase (SOD) and other stress-response proteins. Taken together, the presence of A. macleodii mainly enhanced photosynthesis and biosynthesis of I. galbana and protected it from stress, especially oxidative stress. Transfer of fixed organic carbon, but perhaps other types of biomolecules, between the autotroph and the heterotroph might happen in I. galbana - A. macleodii co-culture. The present work provides novel insights into the transcriptional consequences of I. galbana of mutualism with its heterotrophic bacterial partner, and mutually beneficial associations existing in I. galbana - A. macleodii might be explored to improve productivity and sustainability of aquaculture algal rearing systems.
... Heterotrophs utilize the organic carbon fixed by autotrophs. In return, they benefit photoautotrophs by providing essential micronutrients, such as vitamins, bioavailable trace metals, and amino acids [55][56][57], as well as reducing the levels of toxic reactive oxygen [58,59]. The co-culture system proved that the interaction between strictly heterotrophic bacteria and autotrophic strains played a crucial role in improving the CO 2 fixing efficiency by eliminating self-restraint of organic compounds and promoting the autotrophic pathway [13]. ...
Article
Full-text available
Threatened by climate change and ocean warming, coral reef ecosystems have been shifting in geographic ranges toward a higher latitude area. The water-associated microbial communities and their potential role in primary production contribution are well studied in tropical coral reefs, but poorly defined in high-latitude coral habitats to date. In this study, amplicon sequencing of 16S rRNA and cbbL gene, co-occurrence network, and βNTI were used. The community structure of bacterial and carbon-fixation bacterial communities showed a significant difference between the center of coral, transitional, and non-coral area. Nitrite, DOC, pH, and coral coverage ratio significantly impacted the β-diversity of bacterial and carbon-fixation communities. The interaction of heterotrophs and autotrophic carbon-fixers was more complex in the bottom than in surface water. Carbon-fixers correlated with diverse heterotrophs in surface water but fewer lineages of heterotrophic taxa in the bottom. Bacterial community assembly showed an increase by deterministic process with decrease of coral coverage in bottom water, which may correlate with the gradient of nitrite and pH in the habitat. A deterministic process dominated the assembly of carbon-fixation bacterial community in surface water, while stochastic process dominated t the bottom. In conclusion, the structure and assembly of bacterial and carbon-fixer community were affected by multi-environmental variables in high-latitude coral habitat-associated seawater.
... The species with the most numerous sequenced genomes from HGM (available in the GenBank, NCBI) for each group are highlighted in Table A1. The metabolic reconstruction techniques revealed a large number of missing known genes in the Cbl biosynthetic pathways of various environmental bacteria, including those producing B12-dependent methionine synthase (MetH), probably, due to their mutualistic or symbiotic life style [7,12,22,33,65]. Shelton et al. [7] differentiated seven microbial Cba biosynthesis phenotypes based on the presence of complete aerobic biosynthesis (23 genes) or complete anaerobic biosynthesis (25 genes); tetrapyrrole precursor biosynthesis (five genes); combined corrin ring biosynthesis (nine genes); aminopropanol linker (two genes); adenosylation (one gene); nucleotide loop assembly (seven genes); core biosynthesis genes (eight genes). ...
Article
Full-text available
Many microbial producers of coenzyme B12 family cofactors together with their metabolically interdependent pathways are comprehensively studied and successfully used both in natural ecosystems dominated by auxotrophs, including bacteria and mammals, and in the safe industrial production of vitamin B12. Metabolic reconstruction for genomic and metagenomic data and functional genomics continue to mine the microbial and genetic resources for biosynthesis of the vital vitamin B12. Availability of metabolic engineering techniques and usage of affordable and renewable sources allowed improving bioprocess of vitamins, providing a positive impact on both economics and environment. The commercial production of vitamin B12 is mainly achieved through the use of the two major industrial strains, Propionobacterium shermanii and Pseudomonas denitrificans, that involves about 30 enzymatic steps in the biosynthesis of cobalamin and completely replaces chemical synthesis. However, there are still unresolved issues in cobalamin biosynthesis that need to be elucidated for future bioprocess improvements. In the present work, we review the current state of development and challenges for cobalamin (vitamin B12) biosynthesis, describing the major and novel prospective strains, and the studies of environmental factors and genetic tools effecting on the fermentation process are reported.
... Another important role for bacteria in algal growth is supplying vitamin B12, which is a micronutrient needed in algal growth. According to Kazamia et al. (2012), bacteria-as prokaryotic organisms-can synthesize vitamin B12 for microalgae. Decomposing bacteria through metabolism can also convert complex organic compounds into simple organic compounds, which microalgae can directly use as a nutrition source. ...
Article
Full-text available
Energy diversification using microalgae biomass offers a solution to the fossil fuel crisis, which has become a global issue. Chlorella sp. is a microalga that can produce lipids and reduce chemical oxygen demand (COD) in liquid waste. In this research, we used Chlorella sp. to produce lipids and reduce COD in tofu liquid waste. This research aimed to identify the interaction between a complex microorganism, as a decomposer agent, with the addition of the photosynthetic microalgae Chlorella sp. as an oxygen producer to reduce COD in tofu liquid waste. Moreover, we aimed to determine the interaction between Chlorella sp. and a bacterial consortium for microalgae growth and lipid production. This study was conducted in batches with the addition of bacteria at five different concentrations (% v/v): 0 (no addition), up to 0.25, 0.50, 0.75, and 1. Cultivation was conducted for 13 days with solar irradiation in a photobioreactor. As a result, the highest density and the highest growth rate were obtained from the treatment with 1% bacteria, achieving as many as 5.65´106 cell/mL and 0.21/day. The 1% treatment was able to produce lipids and COD removal efficiencies of 20.93% and 96.30% at the best-removing detention times, which both occurred on the 13th day of cultivation.
... Mutualism is a process of ecological interaction in which both species are benefitted from each other. For example, several researchers have reported that the bacteria supplied vitamin B 12 to the microalgae, and in exchange, microalgae supplied the fixed carbon to the bacteria [62][63][64]. In another study, Kim and co-workers [65] showed that Rhizobium sp., when co-cultured with Chlorella Vulgaris, promoted the algal cell count by 72% due to the mutualistic relationship. ...
Article
Full-text available
The scarcity of water resources and environmental pollution have highlighted the need for sustainable wastewater treatment. Existing conventional treatment systems are energy-intensive and not always able to meet stringent disposal standards. Recently, algal-bacterial systems have emerged as environmentally friendly sustainable processes for wastewater treatment and resource recovery. The algal-bacterial systems work on the principle of the symbiotic relationship between algae and bacteria. This paper comprehensively discusses the most recent studies on algal-bacterial systems for wastewater treatment, factors affecting the treatment, and aspects of resource recovery from the biomass. The algal-bacterial interaction includes cell-to-cell communication, substrate exchange, and horizontal gene transfer. The quorum sensing (QS) molecules and their effects on algal-bacterial interactions are briefly discussed. The effect of the factors such as pH, temperature, C/N/P ratio, light intensity, and external aeration on the algal-bacterial systems have been discussed. An overview of the modeling aspects of algal-bacterial systems has been provided. The algal-bacterial systems have the potential for removing micropollutants because of the diverse possible interactions between algae-bacteria. The removal mechanisms of micropollutants - sorption, biodegradation, and photodegradation, have been reviewed. The harvesting methods and resource recovery aspects have been presented. The major challenges associated with algal-bacterial systems for real scale implementation and future perspectives have been discussed. Integrating wastewater treatment with the algal biorefinery concept reduces the overall waste component in a wastewater treatment system by converting the biomass into a useful product, resulting in a sustainable system that contributes to the circular bioeconomy.
... Indeed, microbial communities can perform more functions through the co-ordinated division of labour than their monoculture counterparts with each participating member performing a certain task (niche differentiation), thus creating more productive, stable, and resilient ecosystems (Hays et al. 2015;Gorter et al. 2020). With the advent of the field of synthetic microbial ecology, synthetic ecosystems, which mimic biologically complex environments, but with reduced complexity, are now routinely used to better understand interspecific interactions and their effects on community dynamics (Kazamia et al. 2012b;Hom and Murray 2014;Hays et al. 2015;Germerodt et al. 2016;La Sarre et al. 2017;Li et al. 2017;Ponomarova et al. 2017;Hillesland 2018;Du et al. 2019;Zuñiga et al. 2019;Liao et al. 2020;Zuñiga et al. 2020). ...
Article
Full-text available
The general interest in microbial ecology has skyrocketed over the past decade, driven by technical advances and by the rapidly increasing appreciation of the fundamental services that these ecosystems provide. In biotechnology, ecosystems have many more functionalities than single species, and, if properly understood and harnessed, will be able to deliver better outcomes for almost all imaginable applications. However, the complexity of microbial ecosystems and of the interactions between species has limited their applicability. In research, next generation sequencing allows accurate mapping of the microbiomes that characterise ecosystems of biotechnological and/or medical relevance. But the gap between mapping and understanding, to be filled by “functional microbiomics”, requires the collection and integration of many different layers of complex data sets, from molecular multi-omics to spatial imaging technologies to online ecosystem monitoring tools. Holistically, studying the complexity of most microbial ecosystems, consisting of hundreds of species in specific spatial arrangements, is beyond our current technical capabilities, and simpler model systems with fewer species and reduced spatial complexity are required to establish the fundamental rules of ecosystem functioning. One such ecosystem, the ecosystem responsible for natural alcoholic fermentation, can provide an excellent tool to study evolutionarily relevant interactions between multiple species within a relatively easily controlled environment. This review will critically evaluate the approaches that are currently implemented to dissect the cellular and molecular networks that govern this ecosystem. Key points • Evolutionarily isolated fermentation ecosystem can be used as an ecological model. • Experimental toolbox is gearing towards mechanistic understanding of this ecosystem. • Integration of multidisciplinary datasets is key to predictive understanding. Graphical abstract
... lost via cell lysis) between microbes (D'Souza et al., 2018), including B-vitamins. Exchanges involving vitamins/vitamers and macronutrients are known; for example, bacteria providing B 12 to co-occurring algae and in turn receiving organic carbon (Haines and Guillard, 1974b;Croft et al., 2005;Kazamia et al., 2012;Durham et al., 2015). ...
Article
Full-text available
B-vitamins are essential micronutrients for marine plankton. Additionally, we now know many marine plankton cannot synthesize B-vitamins de novo (from scratch) and thus are reliant on external supplies. Details of B-vitamin exchange, whether ‘active’ or ‘passive’ (i.e. through cell secretion or mortality), are lacking and as a result we struggle to predict microbial physiology, community composition and biogeochemistry. We argue that significant advances in understanding of the impact of B-vitamin exchange and cycling on marine community structure and biogeochemistry can be made by focusing on unknowns related to the ‘in’s and out’s’ of B-vitamin transport, exchange between plankton, and ecosystem scale processing/transformation of B-vitamins. We point out that it is particularly necessary to reach beyond traditional categorization of populations as B-vitamin auxotrophs (requiring supplied vitamin) or prototrophs (de novo vitamin synthesizers) and begin addressing which populations are net ‘providers’ and/or ‘consumers’. This is a particularly interesting problem as organisms cannot be confidently categorized as net ‘providers’ and/or ‘consumers’ based on genome-based prediction, and it is possible the two roles may change over time and environmental conditions. We posit that greater knowledge of B-vitamin exchange, e.g. cross-feeding, acquisition and secretion systems, environmental triggers of ‘provision’ and ‘consumption’, will reveal unforeseen networking and novel niches across marine planktonic communities. Last, we advocate for further experiments tracking the responses of isolates or natural communities relative to vitamin availability, tracing flow of B-vitamins between cells using novel approaches (e.g. isotopic, fluorometric), and greater consideration of altered B-vitamin exchange and cycling under future climate scenarios.
... This occurs, for example, between Chlamydomonas reinhardtii and a heterotrophic bacterium Mesorhizobium sp., which produces vitamin B12, or between Lobomonas rostrata and Mesorhizobium sp. [162]. In the review by Lutzu et al., there is an exhaustive overview of the most important symbiotic partners of microalgae that are useful for biotechnological applications [163]. ...
Article
Full-text available
Marine organisms have been shown to be a valuable source for biologically active compounds for the prevention and treatment of cancer, inflammation, immune system diseases, and other pathologies. The advantage of studying organisms collected in the marine environment lies in their great biodiversity and in the variety of chemical structures of marine natural products. Various studies have focused on marine organism compounds with potential pharmaceutical applications, for instance, as immunomodulators, to treat cancer and immune-mediated diseases. Modulation of the immune system is defined as any change in the immune response that can result in the induction, expression, amplification, or inhibition of any phase of the immune response. Studies very often focus on the effects of marine-derived compounds on macrophages, as well as lymphocytes, by analyzing the release of mediators (cytokines) by using the immunological assay enzyme-linked immunosorbent assay (ELISA), Western blot, immunofluorescence, and real-time PCR. The main sources are fungi, bacteria, microalgae, macroalgae, sponges, mollusks, corals, and fishes. This review is focused on the marine-derived molecules discovered in the last three years as potential immunomodulatory drugs.
Article
Shellfish, in particular bivalves, are an often-overlooked source of vitamin B12 (B12) in the human diet although they have significantly higher tissue levels of B12 than other animal meat or fish sources, including all vertebrates. However, the origins and key metabolic processes involving B12 in bivalves remain largely unknown. In this study, we examined the distribution of B12 in tissues of several adult Australian bivalve species and assessed hypotheses concerning their B12 utilisation and principal uptake, specifically whether it is derived from diet or gut microbiome. Pacific oysters, Crassostrea gigas, and Goolwa cockles, Plebidonax deltoides (‘pipis’), are both high in B12 (28.0–49.4 μg/100 g total per individual). Vitamin B12 tissue distribution, particularly in oysters, varied significantly, with higher amounts in the adductor muscle (44.0–96.7 μg/100 g), and other tissues, such as gonads, were relatively low (12.7–35.9 μg/100 g). In comparison, concentrations of B12 in the adductor muscle and roe of Southern Australian scallops, Pecten fumatus, were appreciably lower (3.4–10.8 μg/100 g). We also demonstrated that microalgal feed commonly grown in aquaculture can be supplemented directly with B12, resulting in an enriched feed. However, the B12-enriched diet did not transfer to a significant increase in oyster larval B12 concentrations, contradicting our theory that vitamin uptake through feed was a primary B12 source. Vitamin B12 concentrations across oyster larval life stages showed a significant decrease post metamorphosis, which indicates a higher utilisation of B12 during this life event. Our findings also provide insight into B12 uptake and tissue distribution in bivalve species, which can aid the aquaculture industry in promotion of bivalves as a valuable source of dietary B12 for human consumers, while also suggesting ways to optimise vitamin supplementation in bivalve hatchery production.
Article
One of the main social and economic challenges of the 21st century will be to overcome the worlds’ water deficit expected by the end of this decade. Microalgae based wastewater treatment has been suggested as a strategy to recover nutrients from wastewater while simultaneously producing clean water. Consortia of microalgae and bacteria are responsible for recovering nutrients from wastewater. A better understanding of how environmental and operational conditions affect the composition of the microalgae-bacteria consortia would allow to maximise nutrient recoveries and biomass productivities. Most of the studies reported to date showed promising results, although up-scaling of these processes to reactors larger than 100 m² is needed to better predict their industrial relevance. The main advantage of microalgae based wastewater treatment is that valuable biomass with unlimited applications is produced as a co-product. The aim of the current paper was to review microalgae based wastewater treatment processes focusing on strategies that allow increasing both biomass productivities and nutrient recoveries. Moreover, the benefits of microalgae based agricultural products were also discussed.
Article
Full-text available
Generally, most eukaryotic organisms form relationships with microbes that are important in mediating host organismal health. Macroalgae are a diverse group of photosynthetic eukaryotic organisms that serve as primary producers and foundational species in many ecosystems.
Preprint
Full-text available
Vitamin B 12 (B 12 ) is an essential micronutrient for all animals, but is not present in plants and is produced de novo only by bacteria or archaea. Accordingly, humans must derive required B 12 from eating animal products or vitamin supplements, as deficiencies can lead to severe health issues including neuropathy. An often overlooked source in the human diet of B 12 is shellfish, in particular bivalves, which have significantly higher levels of B 12 than other animal sources, including all vertebrate meats. Origins and key metabolic processes involving B 12 in bivalves remain largely unknown, despite the exceptionally high levels. In this study, we examined in several Australian bivalve species, hypotheses concerning B 12 utilisation and uptake through diet or microorganism symbiosis. Vitamin B 12 is not distributed evenly across different tissues types of the Pacific oyster, the commercial scallop and Goolwa cockle (pipi), with higher accumulation in the oyster adductor muscle and gill, and mantle and syphons of the Goolwa cockle. Oyster larvae before first feeding already contained high amount of B 12 ; however, a significant decrease in B 12 concentration post metamorphosis indicates a higher utilisation of B 12 during this life event. We demonstrated that microalgal feed can be supplemented with B 12 , resulting in an enriched feed, but this did not result in an increase in larval B 12 concentrations when oyster larvae were fed with this diet relative to controls, thus supporting the theory that a B 12 producing microbiome within bivalves was the potential source of B 12 rather than feed. However, B 12 concentrations in the digestive tract of adult oysters were low compared to other tissue types, which might challenge this theory, at least in adults. Our findings provide insight into B 12 uptake and function in bivalve species, which will aid the promotion of bivalves as suitable B 12 source for humans as well as provide crucial information to the aquaculture industry in relation to optimisation of vitamin supplementation in bivalve hatchery production.
Article
A series of commercial powdered media (Cell-Hi F2P, JWP and WP) and a hydroponics medium (FloraMicroBloom) were investigated for the cultivation of P. tricornutum, and compared with f/2 (a commonly employed laboratory cultivation medium; costlier to scale). Cell-Hi JWP showed good performance characteristics including cost-effectiveness. Outdoor cultivation of P. tricornutum in an airlift photobioreactor, using Cell-Hi JWP in the United Kingdom (UK) during September and October (average daily temperature ranging between 8 and 18 °C and natural sunlight) was comparable to cultivation indoors under controlled temperature and lighting. A strong positive correlation between fucoxanthin and chlorophyll a content, and a weak inverse correlation between eicosapentaenoic (EPA) content and temperature were observed. Commensal bacterial counts revealed a sinusoidal growth profile with a change in community dominance from Halomonas sp. to Marinobacter sp. This investigation reveals for the first time that a multi-product approach can be adopted with P. tricornutum in a UK outdoor environment using commercially viable powdered media.
Preprint
Full-text available
Cobalamin (vitamin B 12 ), is a cofactor for crucial metabolic reactions in multiple eukaryotic taxa, including major primary producers such as algae, and yet only prokaryotes can produce it. Many bacteria can colonise the algal phycosphere, forming stable communities that gain preferential access to exudates and in return provide compounds, such as B 12 . Extended coexistence can then drive gene loss, leading to greater algal-bacterial interdependence. In this study, we investigate how a recently evolved B 12 -dependent strain of Chlamydomonas reinhardtii , metE7, forms a mutualism with certain bacteria, including the rhizobium Mesorhizobium loti and even a strain of the gut bacterium E. coli engineered to produce cobalamin. Although metE7 was supported by B 12 producers, its growth in co-culture was slower than the B 12 -independent wild-type, suggesting that high bacterial B 12 provision may be necessary to favour B 12 auxotrophs and their evolution. Moreover, we found that an E. coli strain that releases more B 12 makes a better mutualistic partner, and although this trait may be more costly in isolation, greater B 12 release provided an advantage in co-cultures. We hypothesise that, given the right conditions, bacteria that release more B 12 may be selected for, particularly if they form close interactions with B 12 -dependent algae. Originality-Significance statement Microalgae are fundamental to the global carbon cycle, and yet despite being photosynthetic they often rely on other organisms for micronutrients. One of these micronutrients is vitamin B 12 (cobalamin), which they receive from bacteria. Many environmental studies support the widespread role of B 12 in algal-bacterial mutualisms, so here we wished to investigate how these mutualisms may arise evolutionarily by using an experimentally evolved B 12 -dependent alga and various B 12 -producers. A B 12 -producing rhizobium, Mesorhizobium loti , could stably support the B 12 -dependent Chlamydomonas reinhardtii metE7 strain, and vice versa, but nutrient supplementation increased growth of both species further. metE7 could also be supported by E. coli strains engineered to produce B 12 , and engineering a strain to release a higher proportion of B 12 led to better algal growth, which increased bacterial growth in turn. We suggest that as B 12 -based mutualisms develop, increased B 12 release may be selected for and therefore lead to more productive symbioses.
Chapter
Huge quantities of domestic and industrial wastewater are annually produced causing severe environmental problems. Fortunately, algal-based wastewater treatment is promising approach for conversions of pollutants into add value products where the harvested algae could be utilized for biofuels production. However, the separation of algae, long retention time, seasonal variation efficiency, evaporation, low removal efficiency of organics and particulate matter represent the major barriers for the implementation and application of such technology in a full scale. However, algae-based wastewater treatment is a low-cost technology and could be suitable for application in arid areas particularly for developing countries. This chapter will comprehensively discuss the challenges and limitations for algae-based wastewater treatment with emphasis on synergy of bacteria and microalgae.
Article
The expanding use of fossil fuels has caused concern in terms of both energy security and environmental issues. Therefore, attempts have been made worldwide to promote the development of renewable energy sources, among which biofuel is especially attractive. Compared to other biofuels, lipid-derived biofuels have a higher energy density and better compatibility with existing infrastructure, and their performance can be readily improved by adjusting the chemical composition of lipid feedstocks. This review thus addresses the intrinsic interactions between lipid feedstocks and lipid-based biofuels, including biodiesel, and renewable equivalents to conventional gasoline, diesel, and jet fuel. Advancements in lipid-associated biofuel technology, as well as the properties and applicability of various lipid sources in terms of biofuel production, are also discussed. Furthermore, current progress in lipid production and profile optimization in the context of plant lipids, microbial lipids, and animal fats are presented to provide a wider context of lipid-based biofuel technology.
Article
Full-text available
Algae-bacteria consortia treatment has been found to be a promising method for the remediation of aqueous systems. Given the scope of previous reviews on algae-bacteria interactions, the sections on chemical signaling between algae and bacteria don’t cover the current knowledge gap, and recent advances of algae-bacteria consortia in aqueous remediation don’t explore the full depth. Accordingly, the specific aim of this review was to thoroughly screen and summarize recent peer-reviewed literature on (1) the mechanism of algal selection and enrichment in wastewater treatment; (2) interactions between algae and bacteria in ecological niche environments; (3) chemical signaling between algae and bacteria; (4) aqueous remediation using the algae-bacteria consortia; and (5) advanced treatment techniques combined with algae-bacteria systems for improved aqueous remediation. The main current challenges and future perspectives in algae-bacteria consortia wastewater treatment are proposed, including: (i) comprehensively establishing the network of interactions between algae and bacteria, especially quorum sensing and phycospheric interactions; (ii) developing a detailed understanding of the chemical exchange between microbial species based on molecular diffusion processes; (iii) tracking complex algae-bacteria interactions in aquatic environments using machine learning (ML), providing a potential tool for the design of beneficial and customizable synthetic microbial communities for wastewater treatment; (iv) integrating advanced treatment techniques (e.g., MBRs, UV photolysis and biological activated carbon) with algae-bacteria consortia systems, increasing the sustainability and applicability of treatment processes. Therefore, this review provides guidance and insights on the future development of algae-bacteria consortia treatment systems and their potential application for aqueous remediation.
Article
A sustainable approach of Desmodesmus sp. GIEC-179 : Klebsiella pneumoniae (DUT-XJR-t-1.2) co-culture ratios were optimized to remove tetracycline (TET) from synthetic wastewater. To enhance the tetracycline removal performance, the effect of microalgae-bacterial co-culture ratio, maximum TET concentration, effective inoculum amount, growth temperature and pH were studied. The optimized ratio 1:2 of Desmodesmus sp.: K. pneumoniae showed the optimal removal percentage at the temperature of 25°C, pH 7 and 10% inoculum amount; and the removal of TET was recorded as 95%. Moreover, this study explored the Desmodesmus sp.: K. pneumoniae (1:2) nutrient (COD, NH4⁺ and PO4³⁻) exchange relationship and their interaction of TET removal to better understand their fundamental mechanism. According to the results of this study, Desmodesmus sp.: K. pneumoniae co-culture could be a green option for bio-removal of tetracycline from wastewater.
Article
Cyanobacteria are an evolutionarily ancient and diverse group of microorganisms. Their genetic diversity has allowed them to occupy and play vital roles in a wide range of ecological niches, from desert soil crusts to tropical oceans. Owing to bioprospecting efforts and the development of new platform technologies enabling their study and manipulation, our knowledge of cyanobacterial metabolism is rapidly expanding. This review explores our current understanding of the genetic and metabolic features of cyanobacteria, from the more established cyanobacterial model strains to the newly isolated/described species, particularly the fast-growing, highly productive, and genetically amenable strains, as promising chassis for renewable biotechnology. It also discusses emerging technologies for their study and manipulation, enabling researchers to harness the astounding diversity of the cyanobacterial genomic and metabolic treasure trove towards the establishment of a sustainable bioeconomy.
Article
In laboratory and industrial cultivation of marine microalgae, it is customary to enrich cultures with macronutrients (N, P), chelated trace metals, and vitamins at ~104× concentrations found in nature to obtain high culture densities. Other naturally occurring growth‐promoting compounds found in local seawater are not enriched and remain at environmental concentrations. Microalgae may thus be deprived of the mutualistic contributions of co‐occurring microorganisms with which they have evolved complex chemical relationships. In the present study, we assess the direct (mixed bacteria–microalgae cultivation) and indirect (exposure to exudates only, without physical contact) effects of 10 bacterial strains on the growth of five marine microalgal strains used as feeds in marine aquaculture hatcheries. Bacterial strains were selected based upon previously reported growth‐promoting characteristics in plants or microalgae, or known release of probiotics. Our experiments demonstrate superior stimulation of microalgal growth by bacterial exudates, and without the presence of the bacteria that produced these exudates. However, response to bacterial exudate enrichment was dependent upon the microalgae strain and bacterial pairing. Exudates from Bacillus, Mesorhizobium, and Phaeobacter strains were most effective, with 22%–69% increases in microalgal specific growth rate. Such findings indicate that bacterial exudates accelerate rate‐limiting processes governing nutrient acquisition, assimilation, or anabolism, and possibly algal release of exopolymeric substances. Maximal cell density, however, remained constrained by macronutrient limitation. Scaled‐up trials in an oyster hatchery confirmed the practical benefit of bacterial exudate culture medium enrichment and demonstrated the suitability of exudate‐enriched microalgae to feed hatchery‐reared bay scallops. This work presents a promising strategy to improve microalgal culture media formulations using bacterial exudate components as growth promoters, and is the first such study to identify specific pairings with relevance for aquaculture production.
Chapter
Algae and bacteria have coexisted from then on the early stages of evolution. This coevolution cannot be adequately understood if taken individually, but they influence ecosystems together and represent all conceivable modes of mutual interactions between different organisms, ranging from mutualism to parasitism. The algal and bacterial cohabitation could synergistically affect each other's physiology and metabolism, a classic case being algae-bacterial interaction. These interactions are ubiquitous and define primary productivity in most ecosystems. Moreover, in recent research, algae have received more attention for industrial exploitation and their interaction with bacteria is often considered as contamination during commercial application. Besides, a few recent reports highlight that bacterial occurrence is not only enhancing algal growth but also help in flocculation; both are essential processes in algal biotechnology. Hence, there is a need to understand algal-bacterial interactions in an evolutionary and ecological standpoint and to integrate this in further industrial applications. In this chapter, we reflect the diversity of bacteria-algae relationships and their associated mechanisms, as well as the habitats that they mutually influence. This chapter also outlines the role of these interactions in key evolutionary events such as endosymbiosis, besides their ecological role in biogeochemical cycles. Finally, we focus on extending such knowledge on algal–bacterial interactions to various environmental and biotechnological applications. This will help to create a better understanding of mechanisms underlying algae-bacteria interactions that will facilitate the development of more knowledge in biotechnology processes.
Article
Full-text available
The scarcity of usable nitrogen frequently limits plant growth. A tight metabolic association with rhizobial bacteria allows legumes to obtain nitrogen compounds by bacterial reduction of dinitrogen (N2) to ammonium (NH4+). We present here the annotated DNA sequence of the alpha-proteobacterium Sinorhizobium meliloti, the symbiont of alfalfa. The tripartite 6.7-megabase (Mb) genome comprises a 3.65-Mb chromosome, and 1.35-Mb pSymA and 1.68-Mb pSymB megaplasmids. Genome sequence analysis indicates that all three elements contribute, in varying degrees, to symbiosis and reveals how this genome may have emerged during evolution. The genome sequence will be useful in understanding the dynamics of interkingdom associations and of life in soil environments.
Article
Full-text available
Eight bacterial strains identified as P1, P2, Y1, Y2, W1, W2, G, and R were isolated from a long-term laboratory culture of the green alga Chlorella ellipsoidea. Although it is unknown how these bacterial strains have been maintained with the C. ellipsoidea culture, all appeared to promote the growth of C. ellipsoidea. Co-inoculation of each bacterial strain with C. ellipsoidea resulted in 0.5–3 times greater algal growth than that of C. ellipsoidea alone. The most effective bacterium (i.e., strain P1) was selected and further characterized. Biochemical analysis and transmission electron microscopy revealed that strain P1 is closely related to the genus Brevundimonas. Sequence analysis of the 16S rRNA of strain P1 showed 99.9 and 99.4% nucleotide sequence identity to that of B. nasdae and B. vesicularis, respectively. In addition to the growth promotion of C. ellipsoidea by strain P1, the growth of strain P1 was also significantly enhanced by co-culturing with C. ellipsoidea, indicating a symbiotic relationship between the bacterium and alga. Scanning electron microscopy showed the direct adhesion of strain P1 cells to the surface of C. ellipsoidea cells, as well as the development of abundant crinkles on the surface of co-cultured C. ellipsoidea cells.
Article
Full-text available
Vitamin B(12) (cobalamin) is a dietary requirement for humans because it is an essential cofactor for two enzymes, methylmalonyl-CoA mutase and methionine synthase (METH). Land plants and fungi neither synthesize or require cobalamin because they do not contain methylmalonyl-CoA mutase, and have an alternative B(12)-independent methionine synthase (METE). Within the algal kingdom, approximately half of all microalgal species need the vitamin as a growth supplement, but there is no phylogenetic relationship between these species, suggesting that the auxotrophy arose multiple times through evolution. We set out to determine the underlying cellular mechanisms for this observation by investigating elements of B(12) metabolism in the sequenced genomes of 15 different algal species, with representatives of the red, green, and brown algae, diatoms, and coccolithophores, including both macro- and microalgae, and from marine and freshwater environments. From this analysis, together with growth assays, we found a strong correlation between the absence of a functional METE gene and B(12) auxotrophy. The presence of a METE unitary pseudogene in the B(12)-dependent green algae Volvox carteri and Gonium pectorale, relatives of the B(12)-independent Chlamydomonas reinhardtii, suggest that B(12) dependence evolved recently in these lineages. In both C. reinhardtii and the diatom Phaeodactylum tricornutum, growth in the presence of cobalamin leads to repression of METE transcription, providing a mechanism for gene loss. Thus varying environmental conditions are likely to have been the reason for the multiple independent origins of B(12) auxotrophy in these organisms. Because the ultimate source of cobalamin is from prokaryotes, the selective loss of METE in different algal lineages will have had important physiological and ecological consequences for these organisms in terms of their dependence on bacteria.
Article
Full-text available
Marine microalgae support world fisheries production and influence climate through various mechanisms. They are also responsible for harmful blooms that adversely impact coastal ecosystems and economies. Optimal growth and survival of many bloom-forming microalgae, including climatically important dinoflagellates and coccolithophores, requires the close association of specific bacterial species, but the reasons for these associations are unknown. Here, we report that several clades of Marinobacter ubiquitously found in close association with dinoflagellates and coccolithophores produce an unusual lower-affinity dicitrate siderophore, vibrioferrin (VF). Fe-VF chelates undergo photolysis at rates that are 10-20 times higher than siderophores produced by free-living marine bacteria, and unlike the latter, the VF photoproduct has no measurable affinity for iron. While both an algal-associated bacterium and a representative dinoflagellate partner, Scrippsiella trochoidea, used iron from Fe-VF chelates in the dark, in situ photolysis of the chelates in the presence of attenuated sunlight increased bacterial iron uptake by 70% and algal uptake by >20-fold. These results suggest that the bacteria promote algal assimilation of iron by facilitating photochemical redox cycling of this critical nutrient. Also, binary culture experiments and genomic evidence suggest that the algal cells release organic molecules that are used by the bacteria for growth. Such mutualistic sharing of iron and fixed carbon has important implications toward our understanding of the close beneficial interactions between marine bacteria and phytoplankton, and the effect of these interactions on algal blooms and climate.
Article
Full-text available
Dinoroseobacter shibae DFL12(T), a member of the globally important marine Roseobacter clade, comprises symbionts of cosmopolitan marine microalgae, including toxic dinoflagellates. Its annotated 4 417 868 bp genome sequence revealed a possible advantage of this symbiosis for the algal host. D. shibae DFL12(T) is able to synthesize the vitamins B(1) and B(12) for which its host is auxotrophic. Two pathways for the de novo synthesis of vitamin B(12) are present, one requiring oxygen and the other an oxygen-independent pathway. The de novo synthesis of vitamin B(12) was confirmed to be functional, and D. shibae DFL12(T) was shown to provide the growth-limiting vitamins B(1) and B(12) to its dinoflagellate host. The Roseobacter clade has been considered to comprise obligate aerobic bacteria. However, D. shibae DFL12(T) is able to grow anaerobically using the alternative electron acceptors nitrate and dimethylsulfoxide; it has the arginine deiminase survival fermentation pathway and a complex oxygen-dependent Fnr (fumarate and nitrate reduction) regulon. Many of these traits are shared with other members of the Roseobacter clade. D. shibae DFL12(T) has five plasmids, showing examples for vertical recruitment of chromosomal genes (thiC) and horizontal gene transfer (cox genes, gene cluster of 47 kb) possibly by conjugation (vir gene cluster). The long-range (80%) synteny between two sister plasmids provides insights into the emergence of novel plasmids. D. shibae DFL12(T) shows the most complex viral defense system of all Rhodobacterales sequenced to date.
Article
Full-text available
5-Methyltetrahydropteroyltriglutamate - homocysteine transmethylase has been purified from a methionine auxotroph of Escherichia coli K12, which was derepressed for the enzyme. The purified transmethylase has been crystallized and appears to be nearly homogeneous by disc gel electrophoresis and by equilibrium and velocity ultracentrifugation. Further evidence for a high degree of purity has been obtained from a dual purification of the enzyme from repressed and derepressed cells. A calculation of the specific activity of pure enzyme from the initial and final specific activities of derepressed and repressed enzymes reveals that the purified derepressed enzyme is at least 94% pure. Since the transmethylase appears nearly homogeneous after only a 20-fold purification, the enzyme must represent 5% of the soluble protein in derepressed cells of E. coli and 3% in wild type cells. The catalytic, physical, and chemical properties of the purified transmethylase have been investigated. The formation of methyl-¹⁴C-methionine from 5-methyl-¹⁴C-tetrahydropteroyltriglutamate is dependent on transmethylase, homocysteine, and Pi and is stimulated by Mg⁺². 5-Methyl¹⁴C-tetrahydropteroylglutamate or 5-methyl-¹⁴C-tetrahydropteroyl-α-glutamylglutamate cannot replace the triglutamate folate derivative as methyl donor in the formation of methionine. The formation of methionine is inhibited by high ionic strength, ethylenediamine tetraacetic acid, and the folate substrate analogues pteroyl-α-glutamylglutamic acid, pteroyl-γ-glutamyl-γ-glutamylglutamic acid, and 5-methyltetrahydropteroyl-α-glutamylglutamate. The transmethylase has a molecular weight of 84,000 and appears to be composed of subunits.
Article
Full-text available
In order to study the Salmonella typhimurium cobalamin biosynthetic pathway, the S. typhimurium cob operon was isolated and cloned into Escherichia coli. This approach has given the new host of the cob operon the ability to make cobalamins de novo, an ability that had probably been lost by this organism. In total, 20 genes of the S. typhimurium cob operon have been transferred into E. coli, and the resulting recombinant strains have been shown to produce up to 100 times more corrin than the parent S. typhimurium strain. These measurements have been performed with a quantitative cobalamin microbiological assay which is detailed in this work. As with S. typhimurium, cobalamin synthesis is only observed in the E. coli cobalamin-producing strains when they are grown under anaerobic conditions. Derivatives of the cobalamin-producing E. coli strains were constructed in which genes of the cob operon were inactivated. These strains, together with S. typhimurium cob mutants, have permitted the determination of the genes necessary for cobalamin production and classification of cbiD and cbiG as cobl genes. When grown in the absence of endogenous cobalt, the oxidized forms of precorrin-2 and precorrin-3, factor II and factor III, respectively, were found to accumulate in the cytosol of the corrin-producing E. coli. Together with the finding that S. typhimurium cbiL mutants are not complemented with the homologous Pseudomonas denitrificans gene, these results lend further credence to the theory that cobalt is required at an early stage in the biosynthesis of cobalamins in S. typhimurium.
Article
Full-text available
Vitamin B12, or cobalamin, is one of the most structurally complex small molecules made in Nature. Major progress has been made over the past decade in understanding how this synthesis is accomplished. This review covers some of the most important findings that have been made and provides the reader with a complete description of the transformation of uroporphyrinogen III into adenosylcobalamin (AdoCbl). 183 references are cited.
Article
Full-text available
Vitamin B12 (cobalamin) was identified nearly 80 years ago as the anti-pernicious anaemia factor in liver, and its importance in human health and disease has resulted in much work on its uptake, cellular transport and utilization. Plants do not contain cobalamin because they have no cobalamin-dependent enzymes. Deficiencies are therefore common in strict vegetarians, and in the elderly, who are susceptible to an autoimmune disorder that prevents its efficient uptake. In contrast, many algae are rich in vitamin B12, with some species, such as Porphyra yezoensis (Nori), containing as much cobalamin as liver. Despite this, the role of the cofactor in algal metabolism remains unknown, as does the source of the vitamin for these organisms. A survey of 326 algal species revealed that 171 species require exogenous vitamin B12 for growth, implying that more than half of the algal kingdom are cobalamin auxotrophs. Here we show that the role of vitamin B12 in algal metabolism is primarily as a cofactor for vitamin B12-dependent methionine synthase, and that cobalamin auxotrophy has arisen numerous times throughout evolution, probably owing to the loss of the vitamin B12-independent form of the enzyme. The source of cobalamin seems to be bacteria, indicating an important and unsuspected symbiosis.
Article
Full-text available
A Halomonas sp., a marine halophilic and oligotrophic bacterium, was grown on exudates of Dunaliella bardawil. The bacteria increased the solubility of Fe, thereby enhancing its availability to the algae. As a result, the algal growth rate increased. Because of these syntrophic relations, growth of the marine alga D. bardawil was facilitated at Fe levels that would otherwise induce Fe deficiency and inhibit algal growth.
Article
Full-text available
Rhizobium leguminosarum is an alpha-proteobacterial N2-fixing symbiont of legumes that has been the subject of more than a thousand publications. Genes for the symbiotic interaction with plants are well studied, but the adaptations that allow survival and growth in the soil environment are poorly understood. We have sequenced the genome of R. leguminosarum biovar viciae strain 3841. The 7.75 Mb genome comprises a circular chromosome and six circular plasmids, with 61% G+C overall. All three rRNA operons and 52 tRNA genes are on the chromosome; essential protein-encoding genes are largely chromosomal, but most functional classes occur on plasmids as well. Of the 7,263 protein-encoding genes, 2,056 had orthologs in each of three related genomes (Agrobacterium tumefaciens, Sinorhizobium meliloti, and Mesorhizobium loti), and these genes were over-represented in the chromosome and had above average G+C. Most supported the rRNA-based phylogeny, confirming A. tumefaciens to be the closest among these relatives, but 347 genes were incompatible with this phylogeny; these were scattered throughout the genome but were over-represented on the plasmids. An unexpectedly large number of genes were shared by all three rhizobia but were missing from A. tumefaciens. Overall, the genome can be considered to have two main components: a 'core', which is higher in G+C, is mostly chromosomal, is shared with related organisms, and has a consistent phylogeny; and an 'accessory' component, which is sporadic in distribution, lower in G+C, and located on the plasmids and chromosomal islands. The accessory genome has a different nucleotide composition from the core despite a long history of coexistence.
Article
The B12 or cobalamin coenzymes are complex macrocycles whose reactivity is associated with a unique cobalt - carbon bond. The two biologically active forms are MeCbl and AdoCbl and their closely related cobamide forms. MeCbl participate s as the intermediate carrier of activated methyl groups. During the catalytic cycle the coenzyme shuttles between MeCbl and the highly nucleophilic cob(I)alamin form. Examples of MeCbl-dependent enzymes include methionine synthase and Me-H4-MPT:coenzyme M methyl transferase. AdoCbl functions as a source of carbon-based free radicals that are unmasked by homolysis of the coenzyme's cobalt - carbon bond. The free radicals are subsequently used to remove non-acid hydrogen atoms from substrates to facilitate a variety of reactions involving cleavage of carbon-carbon, carbon-oxygen and carbon-nitrogen bonds. Most reactions involve 1,2 migrations of hydroxy-, amino- and carbon-containing groups, but there is also one class of ribonucleotide reductases that uses AdoCbl. The structures of two cobalamin-dependent enzymes, methionine synthase and methylmalonyl-CoA mutase, have been solved. In both cases the cobalt is co-ordinated by a histidine ligand from the protein. The significance of this binding motif is presently unclear since in other cobalamin-dependent enzymes spectroscopic evidence suggests that the coenzyme's nucleotide 'tail' remains co-ordinated to cobalt when bound to the protein.
Article
Primary production in the Ross Sea, one of the most productive areas in the Southern Ocean, has previously been shown to be seasonally limited by iron. In two of three bottle incubation experiments conducted in the austral summer, significantly higher chlorophyll a (Chl a) concentrations were measured upon the addition of iron and B12, relative to iron additions alone. Initial bacterial abundances were significantly lower in the two experiments that showed phytoplankton stimulation upon addition of B12 and iron relative to the experiment that did not show this stimulation. This is consistent with the hypothesis that the bacteria and archaea in the upper water column are an important source of B12 to marine phytoplankton. The addition of iron alone increased the growth of Phaeocystis antarctica relative to diatoms, whereas in an experiment where iron and B12 stimulated total phytoplankton growth, the diatom Pseudonitzschia subcurvata went from comprising approximately 70% of the phytoplankton community to over 90%. Cobalt additions, with and without iron, did not alter Chl a biomass relative to controls and iron additions alone in the Ross Sea. Iron and vitamin B12 plus iron treatments caused reductions in the DMSP (dimethyl sulfoniopropionate) : Chl a ratio relative to the control and B12 treatments, consistent with the notion of an antioxidant function for DMSP. These results demonstrate the importance of a vitamin to phytoplankton growth and community composition in the marine environment.
Article
Without an adequate supply of dissolved vitamins, many species of phytoplankton do not grow. Additions of inorganic nutrients like phosphorus and nitrogen, and trace metals like iron, are not alone adequate to sustain life-a practical lesson learned quickly by experimental biologists when they try to keep eukaryotic phytoplankton cultures alive in their labs. The reason is that coenzymes such as B vitamins are also required for many metabolic pathways. For example, vitamin B1 serves as a cofactor for a large number of enzymatic systems, including the pyruvate dehydrogenase complex required for the metabolism of carbohydrates (glycolysis) and amino acid synthesis [Vandamme, 1989]. Vitamin B12 is used primarily to assist two enzymes: methionine synthase, which is involved in DNA synthesis, and methylmalonyl CoA mutase, which is required for inorganic carbon assimilation [Lindemans and Abels, 1985].
Article
Atlantic sea water with a low cobalt (Co) concentration (0.02 nM) was enriched with Co additions (0.2, 0.5, 1.0 and 3.0 nM), inoculated with a monoculture of Chrysochromulina polylepis Manton & Parke and incubated under laboratory conditions. Co additions (as a salt) increased the yield (number of cells) of C. polylepis. Biomass production was not markedly different if a chelator (EDTA) was added together with Co or if Co was added as vitamin B12 (cyanocobalamin). The maximal growth rate of C. polylepis was 0.8 d-1. Growth rate during the exponential phase was not influenced by Co concentrations, possibly due to Co contamination. The cell quota of Co for C. polylepis in the stationary growth phase was estimated at 0.55 to 0.69 fg Co cell-1 based on cell yield in relation to Co uptake and 0.55 to 0.70 fg Co cell-1 based on analysis of cells. In the 1988 C. polylepis bloom in the Kattegat and Skagerrak, cell concentrations reached levels of 100 x 10(6) cells 1(-1), requiring a Co supply of at least 1 nM. Concentrations of Co in the Kattegat are below 0.5 nM, implying possible Co control of C. polylepis biomass accumulation.
Article
Despite the biological necessity of vitamin B12 (cobalamin), its importance in phytoplankton ecology has been ignored for nearly three decades. Here we report strong and selective responses of phytoplankton communities to varying low levels (5-87 pM) of dissolved B12 in several coastal embayments. The ecological importance of this vitamin is inferred from observed declines in dissolved B12 levels as field populations of large (>5 μm) phytoplankton increased. In contrast, biomass of small (<5 μm) phytoplankton varied independently of B12 concentrations. These observations were corroborated by field-based nutrient amendment experiments, in which B12 additions stimulated growth of large phytoplankton taxa 6-fold over unamended controls. In contrast, small taxa (<5 μm) were largely unaffected. This study provides the first evidence of vitamin B12's influence on phytoplankton field population dynamics based on direct chemical measurements of cobalamin, and implicates B12 as an important organic regulator of photoautotrophic fertility in marine systems.
Article
Vitamins play an integral role in the cellular biochemistry of algae, but the effect of these organic metabolites on the growth and diversity of phytoplankton communities has been poorly studied. We integrated newly developed techniques to directly measure vitamins B, and B12 with field-based amendment experiments to elucidate the role of B-vitamins in phytoplankton population dynamics in coastal marine environments. Two sites on Long Island, New York, USA, were monitored from spring through fall: the tidal Old Fort Pond (OFP) and the brackish Peconic River (PR) estuary. Vitamin B-12 levels were similar between sites (OFP: 1.6 to 21 pM; PR: 1.6 to 17 pM) and were significantly correlated with bacterial densities, dissolved organic nitrogen and dissolved organic phosphorus at OFP, suggesting that B-12 behaves like regenerated organic nutrients. Concentrations of vitamin B, were substantially higher in the freshwater dominated site (PR: 12 to 190 pM; OFP: 9 to 43 pM) and were inversely correlated with salinity, suggesting that rivers and groundwater may be an important source of vitamin B-1. During dinoflagellate blooms (>10(4) cells ml(-1)), occurring in late summer and early fall, vitamin B-12 and B-1 levels in PR decreased 90% relative to pre-bloom levels, while levels temporarily increased to seasonal maxima in OFP, likely reflecting vitamin synthesis and/or regeneration by microbial communities. Nutrient amendment experiments conducted at both sites during summer demonstrated that algal communities were primarily N-limited, while those conducted during early fall showed that vitamins B-1 and B-12 were each capable of significantly enhancing the biomass of larger phytoplankton (>5 mu m). The autumnal shift in phytoplankton communities from dinoflagellates to diatoms, as vitamin levels became depleted and algal communities were limited by vitamin B12, suggests that B-vitamins may influence the succession of coastal phytoplankton.
Article
The folates are made up of a pterdine ring attached to a p-aminobenzoate and a polyglutamyl chain. The active form is tetrahydrofolate which can have C1 units enzymically attached. These C1 units (as a formyl group) are passed on to enzymes in the purine pathway that insert the C−2 and C−8 into the purine ring. A methylene group (−CH2−) attached to tetrahydrofolate is used to convert the uracil-type pyrimidine base found in RNA into the thymine base found in DNA. A further folate cofactor, i.e. 5-methyltetrahydrofolate, is involved in the remethylation of the homocysteine produced in the methylation cycle back to methionine. After activation to S-adenosylmethionine this acts as a methyl donor for the dozens of different methyltransferases present in all cells. Folate deficiency results in reduction of purine and pyrimidine biosynthesis and consequently DNA biosynthesis and cell division. This process is most easily seen in a reduction of erythrocytes causing anaemia. Reduction in the methylation cycle has multiple effects less easy to identify. One such effect is certainly on the nerve cells, because interruption of the methylation cycle causing neuropathy can also happen in vitamin B12 deficiency due to reduced activity of the vitamin B12-dependent enzyme methionine synthase (EC 2.1.1.13). In vitamin B12 deficiency, blocking of the methylation cycle causes the folate cofactors in the cell to become trapped as 5-methyltetrahydrofolate. This process in turn produces a pseudo folate deficiency in such cells, preventing cell division and giving rise to an anaemia identical to that seen in folate deficiency.
Article
Vitamin-requiring marine algae, Cyclotella nana, Monochrysis lutheri, and Amphidinium carterae, were grown in batch culture with limiting concentrations of vitamin B12, thiamine, and biotin, respectively. Cell numbers, average cell volumes, biomasses, 11CO2 uptake rates, and chlorophyll a contents were determined daily. Maximum 14CO2 uptake rates in most vitamin concentrations were obtained at 2 days with C. nana and M. lutheri and at 4 days with A. carterae after starved cultures were exposed to the vitamin. Radiocarbon uptake rates approximately reflect biomass increases. Cell numbers were proportional to vitamin concentrations when cells were incubated for 2 to 3 more days. Cell sizes varied depending on time of incubation. Chlorophyll a content did not always reflect vitamin concentrations. Maximum carbon assimilation rates (Km) and saturation constants (Ks) determined from 14CO2, uptake rates in different vitamin concentrations during early incubation were higher than when determined from cell number in log phase growth. Dissolved vitamin B12, thiamine, and biotin in many samples of seawaters were in the ranges which influence the growth rate, cell size, and chlorophyll a content of C. nana, M. lutheri, and A. carterae, respectively, in laboratory studies. The effects of vitamins on these algae in situ may be similar.
Article
Among the sixteen investigated algal strains (Chlorococcales) ten of them synthesize ketocarotenoids and sporopollenins which are located in the trilaminar structure of the cell wall. In contrast to the colourless cell walls of algae which are unable to form the above substances, the cell walls of strains synthesizing them are pinkish coloured due to the carotenoids which are mainly ketocarotenoids. Constant cell wall pigments are (3S,3′S)-astaxanthin, its oxidation products semiastacene and astacene, canthaxanthin, echinenone (only in cell walls obtained from homogenates), (3S,3′R)-fritschiellaxanthin, 2,3-didehydro-(6′R,3′R)-fritschiellaxanthin, (3R,3′R,6′R)-lutein and two unidentified carotenoids. All these cell wall-carotenoids are present in the free, unesterified form. This is the first discovery of the occurrence of fritschiellaxanthin and 2,3-didehydro-fritschiellaxanthin in the free form in plants. It is postulated that cell wall carotenoids of the described algae may be involved in sporopollenin formation.