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Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

ABSTRACT: Coral reefs host hundreds of thousands of animal species that are increasingly threatened by anthropogenic disturbances. These animals host microbial communities at their surface, playing crucial roles for their fitness. However, the diversity of such microbiomes is mostly described in a few coral species and still poorly defined in other invertebrates and vertebrates. Given the diversity of animal microbiomes, and the diversity of host species inhabiting coral reefs, the contribution of such microbiomes to the total microbial diversity of coral reefs could be important, yet potentially vulnerable to the loss of animal species. Analysis of the surface microbiome from 74 taxa, including teleost fishes, hard and soft corals, crustaceans, echinoderms, bivalves and sponges, revealed that more than 90% of their prokaryotic phylogenetic richness was specific and not recovered in surrounding plankton. Estimate of the total richness associated with coral reef animal surface microbiomes reached up to 2.5% of current estimates of Earth prokaryotic diversity. Therefore, coral reef animal surfaces should be recognized as a hotspot of marine microbial diversity. Loss of the most vulnerable reef animals expected under present-day scenarios of reef degradation would induce an erosion of 28% of the prokaryotic richness, with unknown consequences on coral reef ecosystem functioning.

SUBMITTER: Chiarello M

PROVIDER: S-EPMC7287350 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

Chiarello Marlène M Auguet Jean-Christophe JC Graham Nicholas A J NAJ Claverie Thomas T Sucré Elliott E Bouvier Corinne C Rieuvilleneuve Fabien F Restrepo-Ortiz Claudia Ximena CX Bettarel Yvan Y Villéger Sébastien S Bouvier Thierry T

Proceedings. Biological sciences 20200513 1927

Coral reefs host hundreds of thousands of animal species that are increasingly threatened by anthropogenic disturbances. These animals host microbial communities at their surface, playing crucial roles for their fitness. However, the diversity of such microbiomes is mostly described in a few coral species and still poorly defined in other invertebrates and vertebrates. Given the diversity of animal microbiomes, and the diversity of host species inhabiting coral reefs, the contribution of such mi ...[more]

PMID: 32396801

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Project description:BackgroundCoral reefs are facing unprecedented pressure on local and global scales. Sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. Although the fundamental contribution of microbes to the stability and functioning of coral reefs is widely recognised, it remains unclear how different reef microbiomes respond to environmental perturbations and whether microbiomes are sensitive enough to predict environmental anomalies that can lead to ecosystem stress. However, the lack of coral reef microbial baselines hinders our ability to study the link between shifts in microbiomes and ecosystem stress. In this study, we established a comprehensive microbial reference database for selected Great Barrier Reef sites to assess the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems.ResultsA comprehensive microbial reference database, originating from multiple coral reef microbiomes (i.e. seawater, sediment, corals, sponges and macroalgae), was generated by 16S rRNA gene sequencing for 381 samples collected over the course of 16 months. By coupling this database to environmental parameters, we showed that the seawater microbiome has the greatest diagnostic value to infer shifts in the surrounding reef environment. In fact, 56% of the observed compositional variation in the microbiome was explained by environmental parameters, and temporal successions in the seawater microbiome were characterised by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less responsive to the environment and their community assembly patterns were generally less uniform. By applying a suite of indicator value and machine learning approaches, we further showed that seawater microbial community data provide an accurate prediction of temperature and eutrophication state (i.e. chlorophyll concentration and turbidity).ConclusionOur results reveal that free-living microbial communities have a high potential to infer environmental parameters due to their environmental sensitivity and predictability. This highlights the diagnostic value of microorganisms and illustrates how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.

Project description:The diverse prokaryotic communities associated with reef-building corals may provide important ecological advantages to their threatened hosts. The consistency of relationships between corals and specific prokaryotes, however, is debated, and the locations where microbially mediated processes occur in the host are not resolved. Here, we examined how the prokaryotic associates of five common Caribbean corals with different evolutionary and ecological traits differ across mucus and tissue habitats. We used physical and chemical separation of coral mucus and tissue and sequencing of partial small-subunit rRNA genes of bacteria and archaea from these samples to demonstrate that coral tissue and mucus harbor unique reservoirs of prokaryotes, with 23 to 49% and 31 to 56% of sequences exclusive to the tissue and mucus habitats, respectively. Across all coral species, we found that 46 tissue- and 22 mucus-specific microbial members consistently associated with the different habitats. Sequences classifying as "Candidatus Amoebophilus," Bacteroidetes-affiliated intracellular symbionts of amoebae, emerged as previously unrecognized tissue associates of three coral species. This study demonstrates how coral habitat differentiation enables highly resolved examination of ecological interactions between corals and their associated microorganisms and identifies previously unrecognized tissue and mucus associates of Caribbean corals for future targeted study. IMPORTANCE This study demonstrates that coral tissue or mucus habitats structure the microbiome of corals and that separation of these habitats facilitates identification of consistent microbial associates. Using this approach, we demonstrated that sequences related to "Candidatus Amoebophilus," recognized intracellular symbionts of amoebae, were highly associated with the tissues of Caribbean corals and possibly endosymbionts of a protistan host within corals, adding a further degree of intricacy to coral holobiont symbioses. Examining specific habitats within complex hosts such as corals is useful for targeting important microbial associations that may otherwise be masked by the sheer microbial diversity associated with all host habitats.

Dataset Information

Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

Publications

Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

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