Microbes are well-recognized members of the coral holobiont. However, little is known about the short-term dynamics of mucus-associated microbial communities under natural conditions and after disturbances, and how these dynamics relate to the host's health. Here we examined the natural variability of prokaryotic communities (based on 16S ribosomal RNA gene amplicon sequencing) associating with the surface mucus layer (SML) of Porites astreoides, a species exhibiting cyclical mucus aging and shedding. Shifts in the prokaryotic community composition during mucus aging led to the prevalence of opportunistic and potentially pathogenic bacteria (Verrucomicrobiaceae and Vibrionaceae) in aged mucus and to a twofold increase in prokaryotic abundance. After the release of aged mucus sheets, the community reverted to its original state, dominated by Endozoicimonaceae and Oxalobacteraceae. Furthermore, we followed the fate of the coral holobiont upon depletion of its natural mucus microbiome through antibiotics treatment. After re-introduction to the reef, healthy-looking microbe-depleted corals started exhibiting clear signs of bleaching and necrosis. Recovery versus mortality of the P. astreoides holobiont was related to the degree of change in abundance distribution of the mucus microbiome. We conclude that the natural prokaryotic community inhabiting the coral SML contributes to coral health and that cyclical mucus shedding has a key role in coral microbiome dynamics.

Background Coral 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. Results A 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). Conclusion Our 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. Electronic supplementary material The online version of this article (10.1186/s40168-019-0705-7) contains supplementary material, which is available to authorized users.

The study of complex microbial communities poses unique conceptual and analytical challenges, with microbial species potentially numbering in the thousands. With transient or allochthonous microorganisms often adding to this complexity, a 'core' microbiota approach, focusing only on the stable and permanent members of the community, is becoming increasingly popular. Given the various ways of defining a core microbiota, it is prudent to examine whether the definition of the core impacts upon the results obtained. Here we used complex marine sponge microbiotas and undertook a systematic evaluation of the degree to which different factors used to define the core influenced the conclusions. Significant differences in alpha- and beta-diversity were detected using some but not all core definitions. However, findings related to host specificity and environmental quality were largely insensitive to major changes in the core microbiota definition. Furthermore, none of the applied definitions altered our perception of the ecological networks summarising interactions among bacteria within the sponges. These results suggest that, while care should still be taken in interpretation, the core microbiota approach is surprisingly robust, at least for comparing microbiotas of closely related samples.

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Sponges underpin the productivity of coral reefs, yet few of their microbial symbionts have been functionally characterised. Here we present an analysis of ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 microbial phyla. Compared to MAGs derived from reef seawater, sponge-associated MAGs were enriched in glycosyl hydrolases targeting components of sponge tissue, coral mucus and macroalgae, revealing a critical role for sponge symbionts in cycling reef organic matter. Further, visualisation of the distribution of these genes amongst symbiont taxa uncovered functional guilds for reef organic matter degradation. Genes for the utilisation of sialic acids and glycosaminoglycans present in sponge tissue were found in specific microbial lineages that also encoded genes for attachment to sponge-derived fibronectins and cadherins, suggesting these lineages can utilise specific structural elements of sponge tissue. Further, genes encoding CRISPR and restriction-modification systems used in defence against mobile genetic elements were enriched in sponge symbionts, along with eukaryote-like gene motifs thought to be involved in maintaining host association. Finally, we provide evidence that many of these sponge-enriched genes are laterally transferred between microbial taxa, suggesting they confer a selective advantage within the sponge niche and therefore play a critical role in host ecology and evolution.

Genotype-specific contributions to the environmental tolerance and disease susceptibility of corals are widely accepted. Yet our understanding of how host genotype influences the composition and stability of the coral microbiome subjected to environmental fluctuations is limited. To gain insight into the community dynamics and environmental stability of microbiomes associated with distinct coral genotypes, we assessed the microbial community associated with Acropora tenuis under single and cumulative pressure experiments. Experimental treatments comprised either a single pulse of reduced salinity (minimum of 28 psu) or exposure to the cumulative pressures of reduced salinity (minimum of 28 psu), elevated seawater temperature (+2 °C), elevated pCO2 (900 ppm), and the presence of macroalgae. Analysis of 16S rRNA gene amplicon sequence data revealed that A. tenuis microbiomes were highly host-genotype specific and maintained high compositional stability irrespective of experimental treatment. On average, 48% of the A. tenuis microbiome was dominated by Endozoicomonas. Amplicon sequence variants (ASVs) belonging to this genus were significantly different between host individuals. Although no signs of stress were evident in the coral holobiont and the vast majority of ASVs remained stable across treatments, a microbial indicator approach identified 26 ASVs belonging to Vibrionaceae, Rhodobacteraceae, Hahellaceae, Planctomycetes, Phylobacteriaceae, Flavobacteriaceae, and Cryomorphaceae that were significantly enriched in corals exposed to single and cumulative stressors. While several recent studies have highlighted the efficacy of microbial indicators as sensitive markers for environmental disturbance, the high host-genotype specificity of coral microbiomes may limit their utility and we therefore recommend meticulous control of host-genotype effects in coral microbiome research.

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Coral reef ecosystems are under increasing pressure by multiple stressors that degrade reef condition and function. Although improved management systems have yielded benefits in many regions, broad‐scale declines continue and additional practical and effective solutions for reef conservation and management are urgently needed. Ecological interventions to assist or enhance ecosystem recovery are standard practice in many terrestrial management regimes, and they are now increasingly being implemented in the marine environment. Intervention activities in coral reef systems include the control of coral predators (e.g. crown‐of‐thorns starfish), substrate modification, the creation of artificial habitats and the cultivation, transplantation, and assisted recruitment of corals. On many coastal reefs, corals face competition and overgrowth by fleshy macroalgae whose abundance may be elevated due to acute disturbance events, chronic nutrient enrichment, and reduced herbivory. Active macroalgae removal has been proposed and trialed as a management tool to reduce competition between algae and corals and provide space for coral recruitment, in the hope of restoring the spatial dominance of habitat‐forming corals. However, macroalgae removal has received little formal attention as a method of reef restoration. This review synthesizes available knowledge of the ecological role of macroalgae on coral reefs and the potential benefits and risks associated with their active removal.