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Designer reefs and coral probiotics: great concepts but are they good practice?

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Abstract

An opinion piece examining opportunities and potential risks of using new technologies in the conservation of coral reef ecosystems. To cite this article: Michael Sweet, Andrew Ramsey & Mark Bulling (2017): Designer reefs and coral probiotics: great concepts but are they good practice?, Biodiversity, DOI: 10.1080/14888386.2017.1307786 To link to this article: http://dx.doi.org/10.1080/14888386.2017.1307786

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... The manipulation of microbiomes associated with corals (Beneficial Microorganisms for Corals, BMC) [29] was recently proposed as a promising (albeit yet-to-be-explored) tool to improve coral health, potentially promoting resistance and resilience in coral populations and ultimately aiding recovery of impacted reefs [29][30][31][32]. BMCs can enhance coral fitness through their symbiotic relationships with the host, including the cycling of nutrients within the holobiont [33][34][35] or antagonism/exclusion of potential pathogens (biological control) [36][37][38]. ...
... Understanding the influence of the pBMC community at the cellular level is an important next step to elucidate this and other questions. It is currently not known if the pBMCs colonize the host and help to establish a healthy microbiome, thereby preventing a random assembly of the community that could be shifted easily by opportunistic and potentially pathogenic members, i.e., the pathobiome [31]. An alternative explanation would consist of pBMCs providing an additional source of nutrition through heterotrophy and stimulated microbial loops that sustain the corals and prevent bleaching, although Cobetia sp. ...
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Although the early coral reef-bleaching warning system (NOAA/USA) is established, there is no feasible treatment that can minimize temperature bleaching and/or disease impacts on corals in the field. Here, we present the first attempts to extrapolate the widespread and well-established use of bacterial consortia to protect or improve health in other organisms (e.g., humans and plants) to corals. Manipulation of the coral-associated microbiome was facilitated through addition of a consortium of native (isolated from Pocillopora damicornis and surrounding seawater) putatively beneficial microorganisms for corals (pBMCs), including five Pseudoalteromonas sp., a Halomonas taeanensis and a Cobetia marina-related species strains. The results from a controlled aquarium experiment in two temperature regimes (26 °C and 30 °C) and four treatments (pBMC; pBMC with pathogen challenge – Vibrio coralliilyticus, VC; pathogen challenge, VC; and control) revealed the ability of the pBMC consortium to partially mitigate coral bleaching. Significantly reduced coral-bleaching metrics were observed in pBMC-inoculated corals, in contrast to controls without pBMC addition, especially challenged corals, which displayed strong bleaching signs as indicated by significantly lower photopigment contents and Fv/Fm ratios. The structure of the coral microbiome community also differed between treatments and specific bioindicators were correlated with corals inoculated with pBMC (e.g., Cobetia sp.) or VC (e.g., Ruegeria sp.). Our results indicate that the microbiome in corals can be manipulated to lessen the effect of bleaching, thus helping to alleviate pathogen and temperature stresses, with the addition of BMCs representing a promising novel approach for minimizing coral mortality in the face of increasing environmental impacts.
... For example, while Cyanobacteria are also highly prevalent in corals [14], very few studies have reported cultured coral-associated Cyanobacteria, and most reported Cyanobacteria are associated with black band disease [87,88]. Cyanobacteria may lend themselves to carbon fixation enhancement through high light stressors, and specific efforts should be made to culture them, using appropriate light and specific culturing media such as BG-11, and ensure that they are not pathogens that would negatively impact coral reefs [89,90]. Overall, the lack of genomic data is hampering culturing efforts, and more culture-independent approaches, such as metagenomics, are needed to assess the specific metabolic needs of coralassociated bacteria. ...
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Coral reefs are rapidly declining because of widespread mass coral bleaching causing extensive coral mortality. Elevated seawater temperatures are the main drivers of coral bleaching, and climate change is increasing the frequency and severity of destructive marine heatwaves. Efforts to enhance coral thermal bleaching tolerance can be targeted at the coral host or at coral-associated microorganisms (e.g., dinoflagellate endosymbionts and bacteria). The literature on experimental evolution of bacteria suggests that it has value as a tool to increase coral climate resilience. We provide a workflow on how to experimentally evolve coral-associated bacteria to confer thermal tolerance to coral hosts and emphasize the value of implementing this approach in coral reef conservation and restoration efforts.
... In summary, the application of beneficial microorganisms in coral is promising, and additional mid-and long-term realistic laboratory and well-controlled field pilot experiments are essential to unveil the modulated symbiotic mechanisms, microbiome dynamics, connectivity with other organisms and ecological improvements and outcomes, to indicate and define risk assessment boundaries and provide a safe framework to be applied in light of specific coral reef conditions and urgency for protection and rehabilitaion [80,81]. ...
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Background The coral microbiome plays a key role in host health by being involved in energy metabolism, nutrient cycling, and immune system formation. Inoculating coral with beneficial bacterial consortia may enhance the ability of this host to cope with complex and changing marine environments. In this study, the coral Pocillopora damicornis was inoculated with a beneficial microorganisms for corals (BMC) consortium to investigate how the coral host and its associated microbial community would respond. Results High-throughput 16S rRNA gene sequencing revealed no significant differences in bacterial community α-diversity. However, the bacterial community structure differed significantly between the BMC and placebo groups at the end of the experiment. Addition of the BMC consortium significantly increased the relative abundance of potentially beneficial bacteria, including the genera Mameliella and Endozoicomonas. Energy reserves and calcification rates of the coral host were also improved by the addition of the BMC consortium. Co-occurrence network analysis indicated that inoculation of coral with the exogenous BMC consortium improved the physiological status of the host by shifting the coral-associated microbial community structure. Conclusions Manipulating the coral-associated microbial community may enhance the physiology of coral in normal aquarium conditions (no stress applied), which may hypothetically contribute to resilience and resistance in this host.
... Also, slow release of cells from a solid support can reduce the need for constant reinoculation. Additionally, immobilized cells will disperse less widely compared with free-living cells, thereby effectively reducing potential issues concerning escaped microorganisms affecting or interacting with nontarget organisms (139). ...
Article
The use of Beneficial Microorganisms for Corals (BMCs) has been proposed recently as a tool for the improvement of coral health, with knowledge in this research topic advancing rapidly. BMCs are defined as consortia of microorganisms that contribute to coral health through mechanisms that include ( a) promoting coral nutrition and growth, ( b) mitigating stress and impacts of toxic compounds, ( c) deterring pathogens, and ( d) benefiting early life-stage development. Here, we review the current proposed BMC approach and outline the studies that have proven its potential to increase coral resilience to stress. We revisit and expand the list of putative beneficial microorganisms associated with corals and their proposed mechanisms that facilitate improved host performance. Further, we discuss the caveats and bottlenecks affecting the efficacy of BMCs and close by focusing on the next steps to facilitate application at larger scales that can improve outcomes for corals and reefs globally. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 9 is February 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... Manipulation of the coral microbiome was recently proposed as a promising means to improve coral health by strengthening coral resistance and resilience to environmental stress (Damjanovic et al., 2017;Sweet et al., 2017), and Endozoicomonas has been proposed as an environmental probiotic for this purpose (Peixoto et al., 2017). According to the site-specific distribution of Endozoicomonas, the microbial manipulation in coral would be more effective if we factor in local environmental parameters and host species. ...
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The Kuroshio Current (KC) is one of the fastest water currents in the world, running through the western boundary of the North Pacific Ocean. The KC strongly influences the regional hydroclimate by creating temperature, salinity, and pH gradients from tropical to subtropical and temperate zones, including regions with rich coral reef habitats. Microbial community composition of corals is influenced by various environmental factors, including salinity, pH, and geographical location. However, to date, it is unclear how coral-associated microbial communities would respond to the same water current running through different locations with a time lag. Therefore, we hypothesized that the locations subjected to the KC at higher latitudes experience similar but sequential lag in environmental variability compared to those at lower latitudes, and thus the coral communities of both will respond similarly, but at different times. In this year-long study, we compared the bacterial communities of Acropora muricata at Taiwan, Okinawa, and Kochi subjected to the KC. We found that site-specific conditions and site latitude may have stronger effects on bacterial composition and dynamics than a water current. Consequently, we suggest that latitude largely determines the temperature tolerance range of coral microbiota. Additionally, among the dominant coral associated bacteria, Endozoicomonas from A. muricata and Stylophora pistillata forms distinct phylogroups, while Acinetobacter is more likely a host generalist.
... Additionally, genetic engineering targeting the thermotolerance of key symbionts can also enhance the resilience of corals to climate change [99]. Probiotics and genetic engineering may provide a rapid and urgently needed response to coral decline, but it must be noted that the field is in its infancy and substantially more research is needed to understand its efficacy and risks [100]. The potential of using beneficial endolithic microorganisms as probiotics, or the long-term effects of manipulating members of the coral microbiome on the endolithic community, is yet to be studied in detail. ...
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Coral microbial ecology is a burgeoning field, driven by the urgency of understanding coral health and slowing reef loss due to climate change. Coral resilience depends on its microbiota, and both the tissue and the underlying skeleton are home to a rich biodiversity of eukaryotic, bacterial and archaeal species that form an integral part of the coral holobiont. New techniques now enable detailed studies of the endolithic habitat, and our knowledge of the skeletal microbial community and its eco-physiology is increasing rapidly, with multiple lines of evidence for the importance of the skeletal microbiota in coral health and functioning. Here, we review the roles these organisms play in the holobiont, including nutritional exchanges with the coral host and decalcification of the host skeleton. Microbial metabolism causes steep physico-chemical gradients in the skeleton,
... New techniques have recently been developed that enable large scale production of sexually produced coral spat for just such scenarios 17 . This could then be linked into current more elaborate attempts around reef restoration including practices such as assisted gene flow 18,19 , hybridisation 20 and the use of coral probiotics 21,22 . When coupled with the advancements in settlement substrates 23 -upscaling seems to be within reach. ...
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Reef restoration efforts, utilising sexual coral propagation need up-scaling to have ecologically meaningful impact. Post-settlement survival bottlenecks, in part due to competitive benthic algae interactions should be addressed, to improve productivity for these initiatives. Sea urchins are keystone grazers in reef ecosystems, yet feeding behaviour of adults causes physical damage and mortality to developing coral spat. To investigate if microherbivory can be utilised for co-culture, we quantitatively assessed how varying densities of juvenile sea urchins Mespilia globulus (Linnaeus, 1758), reared alongside the coral Acropora millepora (Ehrenberg, 1834) effected survival and growth of coral recruits. Spawning of both species were induced ex situ. A comparison of A. millepora spat reared in three M. globulus densities (low 16.67 m−2, medium 37.50 m−2, high 75.00 m−2) and a non-grazed control indicated coral survival is significantly influenced by grazing activity (p < 0.001) and was highest in the highest density treatment (39.65 ± 10.88%, mean ± s.d). Urchin grazing also significantly (p < 0.001) influenced coral size (compared to non-grazing control), with colonies in the medium and high-densities growing the largest (21.13 ± 1.02 mm & 20.80 ± 0.82, mean ± s.e.m). Increased urchin density did however have a negative influence on urchin growth, a result of limited food availability.
... Additionally, genetic engineering targeting the thermotolerance of key symbionts can also enhance the resilience of corals to climate change [99]. Probiotics and genetic engineering may provide a rapid and urgently needed response to coral decline, but it must be noted that the field is in its infancy and substantially more research is needed to understand its efficacy and risks [100]. The potential of using beneficial endolithic microorganisms as probiotics, or the long-term effects of manipulating members of the coral microbiome on the endolithic community, is yet to be studied in detail. ...
Preprint
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Coral microbial ecology is a burgeoning field, driven by the urgency of understanding coral health and slowing reef loss due to climate change. Coral resilience depends on its microbiota, and both the tissue and the underlying skeleton are home to a rich biodiversity of eukaryotic, bacterial and archaeal species that form an integral part of the coral holobiont. New techniques now enable detailed studies of the endolithic habitat, and our knowledge of the skeletal microbial community and its eco-physiology is increasing rapidly, with multiple lines of evidence for the importance of the skeletal microbiota in coral health and functioning. Here, we review the roles these organisms play in the holobiont, including nutritional exchanges with the coral host and decalcification of the host skeleton. Microbial metabolism causes steep physico-chemical gradients in the skeleton, creating micro-niches that, along with dispersal limitation and priority affects, define the fine-scale microbial community assembly. Coral bleaching causes drastic changes in the skeletal microbiome, which can mitigate bleaching effects and promote coral survival during stress periods, but may also have detrimental effects. Finally, we discuss the idea that the skeleton may function as a microbial reservoir that can promote recolonization of the tissue microbiome following dysbiosis and help the coral holobiont return to homeostasis.
... Some authors have the purpose of identifying the pathogen, fulfilling the postulates of Köch (Puyana et al., 2015). For the identification of pathogens, the most commonly used techniques are microbiology and molecular biology like Polymerase Chain Reaction (PCR) because of their simplicity, low cost, and reliability of results (Sweet et al., 2017). The study of the different diseases that are presented in corals is of international concern. ...
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Large-scale rearing of coral larvae during mass spawning events and subsequent direct introduction of competent larvae onto denuded reefs ('larval seeding') has been proposed as a low-tech and affordable way of enhancing coral settlement and hence recovery of degraded reefs. While some studies have shown positive short-term effects on settlement, to date, none have examined the long-term effects of larval seeding for a broadcast-spawning coral. Here, we test whether larval seeding significantly increases coral recruitment rates both in the short (5 wk) and longer (∼6 mo to 1 yr) term. Larvae of Acropora digitifera were reared ex situ, and ∼1 million larvae were introduced to 7 artificial reefs (ARs) while 7 others were left unseeded. Settlement tiles deployed on both seeded and control ARs were retrieved for examination 5 and 30 wk after seeding. In addition, the presence of visible coral recruits on the AR surfaces was monitored before and for ∼13 mo post-seeding. Density of acroporid spat was significantly higher on seeded tiles than on controls 5 wk after seeding, but this effect had vanished by 30 wk. Comparison of the densities of new visible Acropora recruits between seeded and control ARs showed no significant difference ∼13 mo after seeding. Larval seeding therefore had no long-term effect due to high post-settlement mortality (which appeared to be density-related). Results suggest that reef-rehabilitation methods that aim to harness coral sexual reproduction might better focus on rearing juveniles through early post-settlement mortality bottlenecks.
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In most tropical countries, coral reef ecosystems provide many goods and services to coastal populations. A variety of anthropogenic practices threatens reef health and therefore jeopardizes the benefits flowing from these services and goods. These threats range from local pollution, sedimentation, destructive fishing practices and coral mining to global issues like coral bleaching. Economic valuation can help to shed light to the importance of the services and goods by 'getting some of the numbers on the table'. And creating markets for sustainable resource utilization can enhance the value captured by the local population from these goods and services. This paper gives some background to economic valuation (Total Economic Value, Cost Benefit Analysis) and market creation as well as three case studies. These case studies illustrate: (i) the economic valuation of marine protected areas; (ii) the economic valuation of a threat to coral reefs (coral mining); and (iii) the creation of a market for sustainably caught/reared reef fish as an alternative to cyanide fishing.
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Because of their ability to transform atmospheric N2 into ammonia that can be used by the plant, researchers were originally very optimistic about the potential of associative diazotrophic bacteria to promote the growth of many cereals and grasses. However, multiple inoculation experiments during recent decades failed to show a substantial contribution of Biological Nitrogen Fixation (BNF) to plant growth in most cases. It is now clear that associative diazotrophs exert their positive effects on plant growth directly or indirectly through (a combination of) different mechanisms. Apart from fixing N2, diazotrophs can affect plant growth directly by the synthesis of phytohormones and vitamins, inhibition of plant ethylene synthesis, improved nutrient uptake, enhanced stress resistance, solubilization of inorganic phosphate and mineralization of organic phosphate. Indirectly, diazotrophs are able to decrease or prevent the deleterious effects of pathogenic microorganisms, mostly through the synthesis of antibiotics and/or fungicidal compounds, through competition for nutrients (for instance, by siderophore production) or by the induction of systemic resistance to pathogens. In addition, they can affect the plant indirectly by interacting with other beneficial microorganisms, for example, Azospirillum increasing nodulation of legumes by rhizobia. The further elucidation of the different mechanisms involved will help to make associative diazotrophs a valuable partner in future agriculture.
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Many reef coral diseases have been described affecting corals in the wild, several of which have been associated with causal agents based on experimental inoculation and testing of Koch’s postulates. In the aquarium industry, many coral diseases and pathologies are known from the grey literature but as yet these have not been systematically described and the relationship to known diseases in the wild is difficult to determine. There is therefore scope to aid the maintenance and husbandry of corals in aquaria by informing the field of the scientifically described wild diseases, if these can be reliably related. Conversely, since the main driver to identifying coral diseases in aquaria is to select an effective treatment, the lessons learnt by aquarists on which treatments work with particular syndromes provides invaluable evidence for determining the causal agents. Such treatments are not commonly sought by scientists working in the natural environment due the cost and potential environmental impacts of the treatments. Here we review both wild and aquarium diseases and attempt to relate the two. Many important aquarium diseases could not be reconciled to those in the wild. In one case, however, namely that of the ciliate Helicostoma sp. as a causal agent of brown jelly syndrome in aquarium corals, there may be similarities with pathogenic agents of the wild coral diseases, such as white syndrome and brown band syndrome. We propose that Helicostoma is actually a misnomer, but improved understanding of this pathogen and others could benefit both fields. Improved practices in aquarium maintenance and husbandry would also benefit natural environments by reducing the scale of wild harvest and improving the potential for coral culture, both for the aquarium industry and for rehabilitation programmes.
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Chytridiomycosis is an emerging infectious disease of amphibians caused by the chytrid Batrachochytrium dendrobatidis. The disease has been associated with global amphibian declines and species extinctions, however the principle drivers that underly the emergence of chytridiomycosis remain unclear. Current evidence suggests that the world trade in amphibians is implicated in the emergence of chytridiomycosis. Here, we review the evidence that the amphibian trade is driving the emergence of chytridiomycosis by (1) spreading infected animals worldwide, (2) introducing non-native infected animals into naïve populations and (3) amplifying infection of amphibians by co-housing, followed by untreated discharge of infectious zoospores into water supplies. We conclude that the evidence that the amphibian trade is contributing to the spread of Batrachochytrium dendrobatidis is strong, and that specific actions are necessary to prevent the introduction of the pathogen into thus-far uninfected areas. Specifically, we recommend the development of national risk-abatement plans, focused on firstly preventing introduction of Bd into disease free areas, and secondly, decreasing the impact of the disease on populations that are currently infected.
Article
Marine protected areas (MPAs) have been widely adopted as the leading tool for coral-reef conservation, but resource users seldom accept them , and many have failed to produce tangible conservation benefits [3]. Few studies have objectively and simultaneously examined the types of MPAs that are most effective in conserving reef resources and the socioeconomic factors responsible for effective conservation [4-6]. We simultaneously explored measures of reef and socioeconomic conservation success at four national parks, four comanaged reserves, and three traditionally managed areas in Indonesia and Papua New Guinea. Underwater visual censuses of key ecological indicators [7, 8] revealed that the average size and biomass of fishes were higher in all areas under traditional management and at one comanaged reserve when compared to nearby unmanaged areas. Socioeconomic assessments [6, 9, 10] revealed that this "effective conservation" was positively related to compliance, visibility of the reserve, and length of time the management had been in place but negatively related to market integration, wealth, and village population size. We suggest that in cases where the resources for enforcement are lacking, management regimes that are designed to meet community goals can achieve greater compliance and subsequent conservation success than regimes designed primarily for biodiversity conservation.
Contrasting Patterns of Coral Bleaching Susceptibility
  • J R Guest
  • A H Baird
  • J A Maynard
  • E Muttaqin
  • A J Edwards
  • S J Campbell
  • K Yewdall
  • Y A Affendi
  • L M Chou
Guest, J. R., A. H. Baird, J. A. Maynard, E. Muttaqin, A. J. Edwards, S. J. Campbell, K. Yewdall, Y. A. Affendi, and L. M. Chou. 2012. "Contrasting Patterns of Coral Bleaching Susceptibility in 2010 Suggest an Adaptive Response to Thermal Stress. " PLoS ONE 7: e33353.
https://coralreefwatch. noaa.gov/satellite/analyses_guidance/global_coral_ bleaching_2014-17_statusBuilding Coral Reef Resilience through Assisted Evolution
  • Noaa Coral
  • Reef Watch
  • J K Oliver
  • H M Putnam
  • R D Gates
NOAA Coral Reef Watch. 2017. https://coralreefwatch. noaa.gov/satellite/analyses_guidance/global_coral_ bleaching_2014-17_status.php van Oppen, M. J. H., J. K. Oliver, H. M. Putnam, and R. D. Gates. 2015. "Building Coral Reef Resilience through Assisted Evolution. " Proc Natl Acad Sci 112: 1-7.