Figure 3 - uploaded by Esther R Angert
Content may be subject to copyright.
Source publication
Thiamin (vitamin B1) is a cofactor required for essential biochemical reactions in all living organisms, yet free thiamin is scarce in the environment. The diversity of biochemical pathways involved in the acquisition, degradation, and synthesis of thiamin indicates that organisms have evolved numerous ecological strategies for meeting this nutriti...
Context in source publication
Context 1
... the online edition for a color version of this figure. to biological degradation, as was first recog- nized in bacteria producing two distinct thi- amin-degrading enzymes (thiaminase I and II) that replace the thiazole moiety of intact thiamin with different nucleophiles (Kimura 1965; Murata 1965; Figure 3). ...
Citations
... For example, the potential number of trophic levels in a system is thought to depend on the input of macronutrients, but the actual food web structure is governed by a combination of productivity, ecological stoichiometry and trophic interactions [1][2][3][4][5]. While the dynamics and competition for macronutrients (e.g., nitrogen and phosphorus) are relatively well characterized (e.g., [6][7][8]), there is little knowledge on the flow and competition for micronutrients such as vitamins, from microbial producers such as bacteria and phytoplankton to consumers such as zooplankton and then to top consumers such as planktivorous and piscivorous fish [9,10]. The current paradigm is that macronutrients, i.e., nitrogen and phosphorous (sometimes silica), and the relative proportions of these macronutrients (stoichiometry) control organismal growth in most aquatic food webs [5,7,11]. ...
... Some micronutrients, including iron, are limiting or colimiting in a few systems [11,12]. It is increasingly thought that vitamins, in some cases, are limiting and potentially structuring various food web interactions [9,10,[13][14][15][16]. ...
... It is an essential substance in all organisms and is involved in several central cellular processes. Its active form, called thiamin diphosphate, is required for the activity of several enzymes, including pyruvate dehydrogenase, which contributes to the production of acetyl-CoA (for review, see [9]). Thiamin is also a co-factor for transketolase, which is a central metabolic enzyme in both the pentose phosphate pathway and the Calvin cycle [9]. ...
Micronutrients such as vitamins are transferred from lower to higher trophic levels, but no general ecological concept describes the factors regulating this process. Here, we investigated thiamin (thiamine, vitamin B1), which is an example of a metabolically important water-soluble micronutrient. Thiamin is produced by organisms such as bacteria and phytoplankton, and all consumers, such as zooplankton and fish, rely on a continuous intake of thiamin through their diet and possibly from de novo-synthesized thiamin by gut microbiota. A deficiency in thiamin negatively affects reproduction in fish and bird populations worldwide. The aim of this study was to quantify thiamin transfer in a planktonic food web in response to thiamin and/or nutrient addition, using an outdoor mesocosm system (an approximately 1.9 m³ bag submerged in sea water). These estimates were then compared with literature data on thiamin concentrations at different trophic levels. The results showed that thiamin was rapidly taken up by phytoplankton in both the ambient and nutrient-amended treatments. However, large differences in thiamin concentrations in phytoplankton did not lead to any significant changes in community composition or abundance. Nitrogen addition led to changes in the abundance and community composition of picoplankton and phytoplankton but there were no additional major effects of thiamin addition. Differences in thiamin concentrations in phytoplankton were not detected at the next trophic level in zooplankton. Although the concentrations did not change, a greater abundance of some zooplankton taxa were developed in the thiamin treatments. Comparing the mesocosm results with literature data demonstrated a gradual reduction in thiamin concentrations along the food chain, with six percent of the concentration in producers occurring in top consumers (i.e., piscivorous fish). Overall, these observations illustrate the concept of trophic dilution of micronutrients where concentrations decrease along the food web from phytoplankton via zooplankton and planktivorous fish to piscivorous fish.
... Complex regulation and specificity of HMP uptake that we describe could in part be due to cytotoxic properties of HMP at high concentrations, which have been described previously, and may drive the evolution of mechanisms that control intracellular concentrations (Garavito et al., 2015;Haughton & King, 1958;Rogers, 1970). Additionally, it is known that toxic HMP derivatives are produced by microbes, which could form the basis of allelopathic cellular interactions that favour highly specific uptake mechanisms in HMP auxotrophs (Cooper et al., 2014;Kraft & Angert, 2017;Reddick et al., 2001;Zilles et al., 2000). ...
Vitamin B1 is a universally required coenzyme in carbon metabolism. However, most marine microorganisms lack the complete biosynthetic pathway for this compound and must acquire thiamin, or precursor molecules, from the dissolved pool. The most common version of Vitamin B1 auxotrophy is for thiamin's pyrimidine precursor moiety, 4‐amino‐5‐hydroxymethyl‐2‐methylpyrimidine (HMP). Frequent HMP auxotrophy in plankton and vanishingly low dissolved concentrations (approximately 0.1–50 pM) suggest that high‐affinity HMP uptake systems are responsible for maintaining low ambient HMP concentrations. We used tritium‐labelled HMP to investigate HMP uptake mechanisms and kinetics in cell cultures of Candidatus Pelagibacter st. HTCC7211, a representative of the globally distributed and highly abundant SAR11 clade. A single protein, the sodium solute symporter ThiV, which is conserved across SAR11 genomes, is the likely candidate for HMP transport. Experimental evidence indicated transport specificity for HMP and mechanistically complex, high‐affinity HMP uptake kinetics. Km values ranged from 9.5 pM to 1.2 nM and were dramatically lower when cells were supplied with a carbon source. These results suggest that HMP uptake in HTCC7211 is subject to complex regulation and point to a strategy for high‐affinity uptake of this essential growth factor that can explain natural HMP levels in seawater.
... Thiamine (vitamin B 1 ) is required by all living organisms as an essential coenzyme in both anabolic and catabolic carbon metabolism (Whitfield et al. 2018). Yet despite being necessary for life, very few multicellular organisms can synthesize thiamine de novo, and most species must obtain it through diet or absorption from exogenous sources or partial synthesis from thiamine-related precursors (Kraft and Angert 2017;Tylicki et al. 2018;Whitfield et al. 2018). Thiamine deficiency in animals causes debilitating morbidities and neurological disorders and has even been linked to early life-stage mortality in taxa as diverse as foxes (Lee 1948), mink (Ender and Helgebostad 1939;Swale 1941), marine mammals (Aulerich et al. 1995), sheep (Evans et al. 1975), humans (Whitfield et al. 2018), reptiles (Marshall 1993;Honeyfield et al. 2008), and fishes (reviewed in Harder et al. 2018). ...
Thiamine deficiency complex (TDC) has been identified in an ever-expanding list of species and populations. In many documented occurrences of TDC in fishes, juvenile mortality can be high—up to 90% at the population level. Such sweeping demographic losses and concomitant decreases in genetic diversity due to TDC can be prevented by treating pre-spawn females or fertilized eggs with supplemental thiamine. However, some fisheries managers are hesitant to widely apply thiamine treatments due to the potential for unforeseen evolutionary consequences. With these concerns in mind, we first review the existing data regarding genetic adaptation to low-thiamine conditions and provide perspectives on evolution-informed treatment strategies with specific population examples. We also provide practical treatment information, consider the potential logistical constraints of thiamine supplementation, and explore the consequences of deciding against supplementation. Until new evidence bolsters or refutes the genetic adaptation hypothesis, we suggest that TDC mitigation strategies should be designed to support maximum population genetic diversity through thiamine supplementation.
... Article appropriate for thiamin and its precursors (≤1 μM); 10,38 concentrations higher than this are most unlikely to occur in natural environments. 43 ...
Salvage pathways for thiamin and its thiazole and pyrimidine moieties are poorly characterized compared to synthesis pathways. A candidate salvage gene is oarX, which encodes a short-chain dehydrogenase/reductase. In diverse bacteria, oarX clusters on the chromosome with genes of thiamin synthesis, salvage, or transport and is preceded by a thiamin pyrophosphate riboswitch. Thiamin and its moieties can undergo oxidations that convert a side-chain hydroxymethyl group to a carboxyl group, or the thiazole ring to a thiazolone, causing a loss of biological activity. To test if OarX participates in salvage of the carboxyl or thiazolone products, we used a genetic approach in Corynebacterium glutamicum ATCC 14067, which is auxotrophic for thiamin’s pyrimidine moiety. This strain could not utilize the pyrimidine carboxyl derivative. This excluded a role in salvaging this product and narrowed the function search to metabolism of the carboxyl or thiazolone derivatives of thiamin or its thiazole moiety. However, a ΔthiG (thiazole auxotroph) strain was not rescued by any of these derivatives. Nor did deleting oarX affect rescue by the physiological pyrimidine and thiazole precursors of thiamin. These findings reinforce the genomic evidence that OarX has a function in thiamin metabolism and rule out five logical possibilities for what this function is.
... Vitamin B1 (Thiamine) functions as a vital coenzyme in facilitating the energy production process within the human body, regulates body temperature, is involved in fat formation, and is required for the proper operation of the nervous and immunological systems (Kraft and Angert 2017). Thiamine deficiency exerts a notable influence on the immune system through various pathogenic mechanisms, including heightened inflammatory response and augmented oxidative stress and other factors. ...
Vitamins and minerals are receiving a lot of attention for their potential to boost the immune system, particularly in relation to the COVID-19 pandemic. Although these nutrients do not act as a cure or preventative measure for the virus, their role in boosting the immune system is essential for fighting infections such as respiratory illnesses, including COVID-19. Vitamin C is recognized for its ability to act as an antioxidant, stimulating the development of white blood cells and antibodies, which strengthens the body's ability to defend itself. Likewise, vitamin D is crucial for the functioning of the immune system, and a lack of it has been associated with a higher risk of getting sick. Vitamin A helps maintain the health of skin and mucous membrane cells, acting as a protective shield against harmful pathogens. Zinc and selenium are necessary for the proper operation of immune cells, while vitamin E serves as an antioxidant, shielding cells from harm. Although it is ideal to have a well-rounded diet that is high in these nutrients, it is important to recognize that excessive supplementing may not provide any extra advantages and may even be harmful. The focus should be on getting a variety of nutrients from a wide range of foods such as fruits, vegetables, nuts, seeds, and lean meats. Amid the COVID-19 pandemic, it is crucial to prioritize compliance with public health precautions including vaccination, hygiene protocols, and maintaining physical distance. It is recommended to seek guidance from medical professionals before making any dietary changes or starting on any supplements, especially for those with pre-existing health issues. Recognizing the importance of vitamins and minerals in supporting the immune system contributes to a comprehensive approach to staying healthy during difficult times.
... Thiamin uptake is essential for aerobic metabolism given its role, for example, in the citric acid cycle (Krebs cycle) as a cofactor of enzymes (Manzetti et al., 2014;Sañudo-Wilhelmy et al., 2014;Kraft & Angert, 2017) and its role in other metabolic processes due to its antioxidant properties (Lukienko et al., 2000). In aquatic ecosystems, thiamin is produced by certain species of prokaryotes, phytoplankton, and fungi (Croft et al., 2006;Paerl et al., 2018). ...
Thiamin is an essential water‐soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids.
... Thiamine (vitamin B 1 ) is an essential cofactor in multiple enzyme complexes required for metabolism of carbohydrates and amino acids 1 . Yet despite being necessary for all life, animals cannot synthesize thiamine de novo, and so the majority must obtain it through diet or direct uptake in the case of fry [2][3][4][5] . Biological thiamine synthesis is energetically expensive and complicated 6,7 . ...
Thiamine (vitamin B 1 ) is required by all living organisms in multiple metabolic pathways. It is scarce in natural systems, and deficiency can lead to reproductive failure, neurological issues, and death. One major cause of thiamine deficiency is an overreliance on diet items containing the enzyme thiaminase. Thiaminase activity has been noted in many prey fishes and linked to cohort failure in salmonid predators that eat prey fish with thiaminase activity, yet it is generally unknown whether evolutionary history, fish traits, and/or environmental conditions lead to production of thiaminase. We conducted literature and GenBank BLAST sequence searches to collect thiaminase activity data and sequence homology data in expressed protein sequences for 300 freshwater and marine fishes. We then tested whether presence or absence of thiaminase could be predicted by evolutionary relationships, trophic level, omega-3 fatty acid concentrations, habitat, climate, invasive potential, and body size. There was no evolutionary relationship with thiaminase activity. It first appears in Class Actinoptergyii (bony ray-finned fishes) and is present across the entire Actinoptergyii phylogeny in both primitive and derived fish orders. Instead, ecological factors explained the most variation in thiaminase: fishes were more likely to express thiaminase if they fed closer to the base of the food web, were high in polyunsaturated fatty acids, lived in freshwater, and were from tropical climates. These data provide a foundation for understanding sources of thiaminase leading to thiamine deficiency in fisheries and other organisms, including humans that eat uncooked fish.
... Homologs of THI4 (thiazole synthase), THI5 (HMP synthase), THI6 (hydroxyethylthiazole kinase), and THI20 (HMP kinase) 32 were not found in the genomes of Phytophthora species. By contrast, the THI80 gene, which encodes a thiamine pyrophosphatase that converts thiamine or TMP into its active form TPP, is present in both S. cerevisiae and Phytophthora, enabling thiamine utilization 33 . Particularly, THI6 absence leads to the inability to synthesize thiamine molecules from simpler precursors. ...
... Fully understanding the physiological and biochemical basis of these regulation processes requires deeper insights at the community level. Thiamine is widely detected in aquatic and terrestrial environments, where it is utilized by thiamine auxotrophs 33 . Considering its low concentration in the environment, the thiamine-associated regulation of gene expression by riboswitches and similar mechanisms 54 might be negligible in the thiamine producers in the natural community, instead, by possible public thiamine regulation. ...
Public metabolites such as vitamins play critical roles in maintaining the ecological functions of microbial community. However, the biochemical and physiological bases for fine-tuning of public metabolites in the microbiome remain poorly understood. Here, we examine the interactions between myxobacteria and Phytophthora sojae , an oomycete pathogen of soybean. We find that host plant and soil microbes complement P. sojae’ s auxotrophy for thiamine. Whereas, myxobacteria inhibits Phytophthora growth by a thiaminase I CcThi1 secreted into extracellular environment via outer membrane vesicles (OMVs). CcThi1 scavenges the required thiamine and thus arrests the thiamine sharing behavior of P. sojae from the supplier, which interferes with amino acid metabolism and expression of pathogenic effectors, probably leading to impairment of P. sojae growth and pathogenicity. Moreover, myxobacteria and CcThi1 are highly effective in regulating the thiamine levels in soil, which is correlated with the incidence of soybean Phytophthora root rot. Our findings unravel a novel ecological tactic employed by myxobacteria to maintain the interspecific equilibrium in soil microbial community.
... Black arrows represent enzymatic reactions that require TDP as a cofactor and the associated enzymes are highlighted in blue. Figure adapted with permission fromKraft and Angert (2017). ...
Thiamine deficiency from the consumption of invasive, high-thiaminase prey fishes is considered to be a major barrier for lake trout restoration in the Great Lakes. In fishes, an understudied aspect of thiamine deficiency is its effect on cardiac function. I examined the effects of dietary thiaminase on cardiac function and morphology in lake trout, specifically as they relate to thermal tolerance. Two hatchery strains of lake trout (Seneca and Slate) were raised on a control or thiaminase diet for nine months. The thiaminase diet was associated with significant ventricle enlargement, impaired cardiac function, and reduced thermal tolerance; these effects were more pronounced in Slate strain fish. Similar cardiac morphological changes were observed in wild-caught lake trout from the Sudbury Basin. These results suggest that dietary thiaminase impairs cardiac function and alters cardiac morphology in fishes, and that such changes may become increasingly important as water temperatures increase through climate change.
... Its key functions make thiamine a vital compound for plants, many microbes, and animals. Thiamine synthesis is limited to plants, fungi and microbes, and among these taxa some can completely synthesise thiamine while others need precursor molecules (Kraft & Angert, 2017;Ejsmond et al., 2019). Thiamine deficiency in consumers can lead to impaired functioning of mitochondria, nervous system and the immune system (Kraft & Angert, 2017), ultimately resulting in reproductive failure, increased mortality and possibly also population decline in the case of systemic thiamine deficiency (Ejsmond et al., 2019). ...
... Thiamine synthesis is limited to plants, fungi and microbes, and among these taxa some can completely synthesise thiamine while others need precursor molecules (Kraft & Angert, 2017;Ejsmond et al., 2019). Thiamine deficiency in consumers can lead to impaired functioning of mitochondria, nervous system and the immune system (Kraft & Angert, 2017), ultimately resulting in reproductive failure, increased mortality and possibly also population decline in the case of systemic thiamine deficiency (Ejsmond et al., 2019). Thiamine deficiency can occur in aquatic ecosystems, caused by the production of thiaminases as antifeedants in planktonic algae (Kraft & Angert, 2017;Harder et al., 2018). ...
... Thiamine deficiency in consumers can lead to impaired functioning of mitochondria, nervous system and the immune system (Kraft & Angert, 2017), ultimately resulting in reproductive failure, increased mortality and possibly also population decline in the case of systemic thiamine deficiency (Ejsmond et al., 2019). Thiamine deficiency can occur in aquatic ecosystems, caused by the production of thiaminases as antifeedants in planktonic algae (Kraft & Angert, 2017;Harder et al., 2018). However, some fish species appear to accumulate thiaminases from their food without any detrimental fitness effects (Kraft & Angert, 2017) and use these accumulated enzymes as antifeedants against higher order carnivores themselves. ...
Nitrogen (N) deposition has increased substantially since the second half of the 20th century due to human activities. This increase of reactive N into the biosphere has major implications for ecosystem functioning, including primary production, soil and water chemistry and producer community structure and diversity. Increased N deposition is also linked to the decline of insects observed over recent decades. However, we currently lack a mechanistic understanding of the effects of high N deposition on individual fitness, species richness and community structure of both invertebrate and vertebrate consumers. Here, we review the effects of N deposition on producer-consumer interactions, focusing on five existing ecological frameworks: C:N:P ecological stoichiometry, trace element ecological stoichiometry, nutritional geometry, essential micronutrients and allelochemicals. We link reported N deposition-mediated changes in producer quality to life-history strategies and traits of consumers, to gain a mechanistic understanding of the direction of response in consumers. We conclude that high N deposition influences producer quality via eutrophication and acidification pathways. This makes oligotrophic poorly buffered ecosystems most vulnerable to significant changes in producer quality. Changes in producer quality between the reviewed frameworks are often interlinked, complicating predictions of the effects of high N deposition on producer quality. The degree and direction of fitness responses of consumers to changes in producer quality varies among species but can be explained by differences in life-history traits and strategies, particularly those affecting species nutrient intake regulation, mobility, relative growth rate, host-plant specialisation, ontogeny and physiology. To increase our understanding of the effects of N deposition on these complex mechanisms, the inclusion of life-history traits of consumer species in future study designs is pivotal. Based on the reviewed literature, we formulate five hypotheses on the mechanisms underlying the effects of high N deposition on consumers, by linking effects of nutritional ecological frameworks to life-history strategies. Importantly, we expect that N-deposition-mediated changes in producer quality will result in a net decrease in consumer community as well as functional diversity. Moreover, we anticipate an increased risk of outbreak events of a small subset of generalist species, with concomitant declines in a multitude of specialist species. Overall, linking ecological frameworks with consumer life-history strategies provides a mechanistic understanding of the impacts of high N deposition on producer-consumer interactions, which can inform management towards more effective mitigation strategies.