Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress.

The coral mucus may harbor commensal bacteria that inhibit growth of pathogens. Therefore, there is a need to understand the dynamics of bacterial communities between the coral mucus and tissues. Nubbins of Acropora muricata were subjected to increasing water temperatures of 26°C-33°C, to simultaneously explore the bacterial diversity in coral mucus and tissues by 16S rRNA gene amplicon sequencing. Photochemical efficiency of symbiotic dinoflagellates within the corals declined above 31°C. Both the mucus and tissues of healthy A. muricata were dominated by γ-Proteobacteria, but under thermal stress there was a shift towards bacteria from the Verrucomicrobiaceae and α-Proteobacteria. Members of Cyanobacteria, Flavobacteria and Sphingobacteria also become more prominent at higher temperatures. The relative abundance of Vibrio spp. in the coral mucus increased at 29°C, but at 31°C, there was a drop in the relative abundance of Vibrio spp. in the mucus, with a reciprocal increase in the tissues. On the other hand, during bleaching, the relative abundance of Endozoicomonas spp. decreased in the tissues with a reciprocal increase in the mucus. This is the first systematic experiment that shows the potential for a bacterial community shift between the coral surface mucus and tissues in a thermally stressed coral.

[1]  R. Steneck,et al.  Coral Reefs Under Rapid Climate Change and Ocean Acidification , 2007, Science.

[2]  E. Weil,et al.  Bacterial communities associated with the mucopolysaccharide layers of three coral species affected and unaffected with dark spots disease. , 2007, Canadian journal of microbiology.

[3]  Chaolun Allen Chen,et al.  Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan , 2005, Coral Reefs.

[4]  E. N. Buckley,et al.  Response of marine bacterioplankton to differential filtration and confinement , 1984, Applied and environmental microbiology.

[5]  Y. Loya,et al.  Bacterial infection and coral bleaching , 1996, Nature.

[6]  J. Bythell,et al.  Measuring mucus thickness in reef corals using a technique devised for vertebrate applications , 2010 .

[7]  B. R. Kim,et al.  Carbon-source utilization patterns of coral-associated marine heterotrophs , 1995 .

[8]  S. K. Pandian,et al.  Phylogenetic characterization of culturable bacterial diversity associated with the mucus and tissue of the coral Acropora digitifera from the Gulf of Mannar. , 2009, FEMS microbiology ecology.

[9]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[10]  K. Hughen,et al.  The Microbiome of the Red Sea Coral Stylophora pistillata Is Dominated by Tissue-Associated Endozoicomonas Bacteria , 2013, Applied and Environmental Microbiology.

[11]  Esther G. L. Koh Do Scleractinian Corals Engage in Chemical Warfare Against Microbes? , 1997, Journal of Chemical Ecology.

[12]  Florent E. Angly,et al.  Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa , 2008, Proceedings of the National Academy of Sciences.

[13]  C. Kellogg Tropical archaea: diversity associated with the surface microlayer of corals , 2004 .

[14]  J. Gershenzon,et al.  Diversity and distribution of floral scent , 2006, The Botanical Review.

[15]  A. Barberán,et al.  Ecological Inferences from a deep screening of the Complex Bacterial Consortia associated with the coral, Porites astreoides , 2013, Molecular ecology.

[16]  Jizhong Zhou,et al.  Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. , 2010, Environmental microbiology.

[17]  N. Knowlton,et al.  Diversity and distribution of coral-associated bacteria , 2002 .

[18]  N. Shashar,et al.  Hydromechanical boundary layers over a coral reef , 1996 .

[19]  R. Stocker,et al.  Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis , 2015, Front. Microbiol..

[20]  M. Liles,et al.  Bacterial Associates of Two Caribbean Coral Species Reveal Species-Specific Distribution and Geographic Variability , 2012, Applied and Environmental Microbiology.

[21]  D. Bourne,et al.  Changes in coral-associated microbial communities during a bleaching event , 2008, The ISME Journal.

[22]  B. Brown,et al.  Coral bleaching: causes and consequences , 1997, Coral Reefs.

[23]  J. Heikoop,et al.  Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation , 2005, Coral Reefs.

[24]  Peter W. Glynn,et al.  Corals' adaptive response to climate change: Shifting to new algal symbionts may safeguard devastated reefs from extinction , 2004 .

[25]  Shinichi Sunagawa,et al.  Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata , 2009, The ISME Journal.

[26]  Porites white patch syndrome: associated viruses and disease physiology , 2015, Coral Reefs.

[27]  M. Breitbart,et al.  Coral-associated Archaea , 2004 .

[28]  R. Gates,et al.  The future of coral reefs: a microbial perspective. , 2010, Trends in ecology & evolution.

[29]  J. Bythell,et al.  Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata , 2006 .

[30]  Chaolun Allen Chen,et al.  Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input , 2014, PeerJ.

[31]  O. Pantos,et al.  Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. , 2002, Environmental microbiology.

[32]  O. Pantos,et al.  The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. , 2003, Environmental microbiology.

[33]  F. Azam,et al.  Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent , 2009, PloS one.

[34]  K. Ritchie Regulation of microbial populations by coral surface mucus and mucus-associated bacteria , 2006 .

[35]  E. Kramarsky-Winter,et al.  Coral mucus-associated bacterial communities from natural and aquarium environments. , 2007, FEMS microbiology letters.

[36]  S. Golubić,et al.  Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton , 2000 .

[37]  R. Edwards,et al.  Viral communities associated with healthy and bleaching corals , 2008, Environmental microbiology.

[38]  J. Bythell,et al.  Perspectives on mucus secretion in reef corals , 2005 .

[39]  David W. Russell,et al.  Recovery of DNA from agarose and polyacrylamide gels: electroelution into dialysis bags. , 2006, CSH protocols.

[40]  W. Meijer,et al.  Characterization of the bacterial community associated with the surface and mucus layer of whiting (Merlangius merlangus). , 2007, FEMS microbiology ecology.

[41]  Peter W. Glynn,et al.  Coral reefs: Corals' adaptive response to climate change , 2004, Nature.

[42]  J. Claverie,et al.  Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. , 2009, Journal of invertebrate pathology.

[43]  J. Todd,et al.  The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate , 2010, The ISME Journal.

[44]  C. Kuo,et al.  Temporal and Spatial Variations in Symbiont Communities of Catch Bowl Coral Isopora palifera (Scleractinia: Acroporidae) on Reefs in Kenting National Park, Taiwan , 2012 .

[45]  M. Riley,et al.  The ecological role of bacteriocins in bacterial competition. , 1999, Trends in microbiology.

[46]  M. Aranda,et al.  Bacterial profiling of White Plague Disease in a comparative coral species framework , 2013, The ISME Journal.

[47]  S. Golubić,et al.  Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia) , 1995 .

[48]  S. Sunagawa,et al.  Threatened Corals Provide Underexplored Microbial Habitats , 2010, PloS one.

[49]  S. Golubić,et al.  Endolithic fungi in marine ecosystems. , 2005, Trends in microbiology.

[50]  Anthony A. Fodor,et al.  Effects of Experimental Choices and Analysis Noise on Surveys of the “Rare Biosphere” , 2009, Applied and Environmental Microbiology.

[51]  I. Hewson,et al.  Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. , 2010, Integrative and comparative biology.

[52]  R. Sanford,et al.  Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. , 2007, Environmental microbiology.

[53]  Florent E. Angly,et al.  Metagenomic analysis of stressed coral holobionts. , 2009, Environmental microbiology.

[54]  Markus Huettel,et al.  Coral mucus functions as an energy carrier and particle trap in the reef ecosystem , 2004, Nature.

[55]  A. James 2010 , 2011, Philo of Alexandria: an Annotated Bibliography 2007-2016.

[56]  Chaolun Allen Chen,et al.  Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas , 2012, Molecular ecology.

[57]  V. Paul,et al.  Community Shifts in the Surface Microbiomes of the Coral Porites astreoides with Unusual Lesions , 2014, PloS one.

[58]  S. Wooldridge A new conceptual model for the enhanced release of mucus in symbiotic reef corals during ‘bleaching’ conditions , 2009 .

[59]  C. Munn,et al.  Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. , 2005, Environmental microbiology.

[60]  L. Richardson,et al.  Microbial Communities in the Surface Mucopolysaccharide Layer and the Black Band Microbial Mat of Black Band-Diseased Siderastrea siderea , 2006, Applied and Environmental Microbiology.

[61]  O. Hoegh‐Guldberg,et al.  Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress , 2009 .

[62]  Ming-Hui Chen,et al.  Pseudoteredinibacter isoporae gen. nov., sp. nov., a marine bacterium isolated from the reef-building coral Isopora palifera. , 2011, International journal of systematic and evolutionary microbiology.

[63]  C. D. Harvell,et al.  Microbial Disease and the Coral Holobiont , 2022 .

[64]  F. Rohwer,et al.  Culture-Independent Analyses of Coral-Associated Microbes , 2004 .

[65]  V. Paul,et al.  Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides , 2011, The ISME Journal.

[66]  Midori Kurahashi,et al.  Endozoicomonas elysicola gen. nov., sp. nov., a gamma-proteobacterium isolated from the sea slug Elysia ornata. , 2007, Systematic and applied microbiology.

[67]  M. Arboleda,et al.  Epizoic Communities of Prokaryotes on Healthy and Diseased Scleractinian Corals in Lingayen Gulf, Philippines , 2008, Microbial Ecology.

[68]  Eugene Rosenberg,et al.  Bleaching of the coral Oculina patagonica by Vibrio AK-1 , 1997 .

[69]  C. Callieri,et al.  Microbial Communities , 2021, Springer Berlin Heidelberg.

[70]  H. Elifantz,et al.  The impact of reduced pH on the microbial community of the coral Acropora eurystoma , 2011, The ISME Journal.

[71]  Eugene Rosenberg,et al.  The role of microorganisms in coral health, disease and evolution , 2007, Nature Reviews Microbiology.

[72]  O. Hoegh‐Guldberg Climate change, coral bleaching and the future of the world's coral reefs , 1999 .