Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis

Rising seawater temperature associated with global climate change is a significant threat to coral health and is linked to increasing coral disease and pathogen-related bleaching events. We performed heat stress experiments with the coral Pocillopora damicornis, where temperature was increased to 31°C, consistent with the 2–3°C predicted increase in summer sea surface maxima. 16S rRNA amplicon sequencing revealed a large shift in the composition of the bacterial community at 31°C, with a notable increase in Vibrio, including known coral pathogens. To investigate the dynamics of the naturally occurring Vibrio community, we performed quantitative PCR targeting (i) the whole Vibrio community and (ii) the coral pathogen Vibrio coralliilyticus. At 31°C, Vibrio abundance increased by 2–3 orders of magnitude and V. coralliilyticus abundance increased by four orders of magnitude. Using a Vibrio-specific amplicon sequencing assay, we further demonstrated that the community composition shifted dramatically as a consequence of heat stress, with significant increases in the relative abundance of known coral pathogens. Our findings provide quantitative evidence that the abundance of potential coral pathogens increases within natural communities of coral-associated microbes as a consequence of rising seawater temperature and highlight the potential negative impacts of anthropogenic climate change on coral reef ecosystems.

[1]  Jan Holmgren,et al.  Cholera , 2017, The Lancet.

[2]  K. Ritchie,et al.  Type II White-Band Disease , 2017 .

[3]  C. Häse,et al.  Mortalities of Eastern and Pacific Oyster Larvae Caused by the Pathogens Vibrio coralliilyticus and Vibrio tubiashii , 2014, Applied and Environmental Microbiology.

[4]  Jesse R. Zaneveld,et al.  Natural volcanic CO2 seeps reveal future trajectories for host–microbial associations in corals and sponges , 2014, The ISME Journal.

[5]  Craig T. Michell,et al.  Whole-Genome Sequences of Three Symbiotic Endozoicomonas Bacteria , 2014, Genome Announcements.

[6]  J. Bythell,et al.  Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis , 2014, Proceedings of the Royal Society B: Biological Sciences.

[7]  C. Castro,et al.  Climate change affects key nitrogen-fixing bacterial populations on coral reefs , 2014, The ISME Journal.

[8]  J. Antón,et al.  New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities , 2014, The ISME Journal.

[9]  G. Aeby,et al.  Vibrio coralliilyticus Strain OCN008 Is an Etiological Agent of Acute Montipora White Syndrome , 2014, Applied and Environmental Microbiology.

[10]  K. Arrigo,et al.  Climate change influences on marine infectious diseases: implications for management and society. , 2014, Annual review of marine science.

[11]  R. Stocker,et al.  A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals , 2013, The ISME Journal.

[12]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

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

[14]  Carla Huete-Stauffer,et al.  16SrDNA Pyrosequencing of the Mediterranean Gorgonian Paramuricea clavata Reveals a Link among Alterations in Bacterial Holobiont Members, Anthropogenic Influence and Disease Outbreaks , 2013, PloS one.

[15]  J. Triñanes,et al.  Emerging Vibrio risk at high latitudes in response to ocean warming , 2013 .

[16]  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.

[17]  G. Aeby,et al.  Vibrio owensii Induces the Tissue Loss Disease Montipora White Syndrome in the Hawaiian Reef Coral Montipora capitata , 2012, PloS one.

[18]  G. De’ath,et al.  The 27–year decline of coral cover on the Great Barrier Reef and its causes , 2012, Proceedings of the National Academy of Sciences.

[19]  B. Willis,et al.  Global coral disease prevalence associated with sea temperature anomalies and local factors. , 2012, Diseases of aquatic organisms.

[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]  Wesley R. Johnson,et al.  Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus , 2011, The ISME Journal.

[22]  Eric P. Nawrocki,et al.  An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea , 2011, The ISME Journal.

[23]  L. Owens,et al.  Multilocus sequence analysis provides basis for fast and reliable identification of Vibrio harveyi-related species and reveals previous misidentification of important marine pathogens. , 2011, Systematic and applied microbiology.

[24]  Rob Knight,et al.  Using QIIME to Analyze 16S rRNA Gene Sequences from Microbial Communities , 2011, Current protocols in bioinformatics.

[25]  R. Colwell,et al.  Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios , 2011, The ISME Journal.

[26]  A. Meistertzheim,et al.  Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus , 2011, Journal of Experimental Biology.

[27]  F. Thompson,et al.  Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire , 2011, The ISME Journal.

[28]  B. Haas,et al.  Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. , 2011, Genome research.

[29]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010, Bioinform..

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

[31]  J. Triñanes,et al.  Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses , 2010 .

[32]  Carlo Cerrano,et al.  Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. , 2010, Environmental microbiology.

[33]  O. Hoegh-Guldberg,et al.  Increasing the accuracy of surface area estimation using single wax dipping of coral fragments , 2010, Coral Reefs.

[34]  B. Willis,et al.  Detection and Quantification of the Coral Pathogen Vibrio coralliilyticus by Real-Time PCR with TaqMan Fluorescent Probes , 2010, Applied and Environmental Microbiology.

[35]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[36]  L. Mydlarz,et al.  What are the physiological and immunological responses of coral to climate warming and disease? , 2010, Journal of Experimental Biology.

[37]  E. Dinsdale,et al.  Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? , 2010, Trends in microbiology.

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

[39]  L. Mydlarz,et al.  Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. , 2009, Diseases of aquatic organisms.

[40]  B. Willis,et al.  Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia) , 2009, Proceedings of the Royal Society B: Biological Sciences.

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

[42]  Wesley R. Johnson,et al.  Role of Flagella in Virulence of the Coral Pathogen Vibrio coralliilyticus , 2009, Applied and Environmental Microbiology.

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

[44]  B. Willis,et al.  The Biogeochemical Cycling of Sulfur Coral-associated Bacteria and Their Role In , 2008 .

[45]  K. Hughen,et al.  The Vibrio core group induces yellow band disease in Caribbean and Indo‐Pacific reef‐building corals , 2008, Journal of applied microbiology.

[46]  G. Holmes,et al.  Estimating three-dimensional surface areas on coral reefs , 2008 .

[47]  F. Thompson,et al.  Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida. , 2008, Systematic and applied microbiology.

[48]  A. Edwards,et al.  One-Third of Reef-Building Corals Face Elevated Extinction Risk from Climate Change and Local Impacts , 2008, Science.

[49]  C. Häse,et al.  The Extracellular Metalloprotease of Vibrio tubiashii Is a Major Virulence Factor for Pacific Oyster (Crassostrea gigas) Larvae , 2008, Applied and Environmental Microbiology.

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

[51]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[52]  O. Hoegh‐Guldberg,et al.  Vulnerability of reef-building corals on the Great Barrier Reef to climate change , 2007 .

[53]  Hugh Sweatman,et al.  Thermal Stress and Coral Cover as Drivers of Coral Disease Outbreaks , 2007, PLoS biology.

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

[55]  E. Weil,et al.  The white band disease type II pathogen in Puerto Rico , 2006 .

[56]  O. Koren,et al.  Bacteria Associated with Mucus and Tissues of the Coral Oculina patagonica in Summer and Winter , 2006, Applied and Environmental Microbiology.

[57]  Wang Hualei,et al.  Design ofVibrio 16S rRNA gene specific primers and their application in the analysis of seawaterVibrio community , 2006 .

[58]  F. Azam,et al.  Antagonistic Interactions among Marine Bacteria Impede the Proliferation of Vibrio cholerae , 2005, Applied and Environmental Microbiology.

[59]  F. Thompson,et al.  Pathogenicity of vibrios to rainbow trout (Oncorhynchus mykiss, Walbaum) and Artemia nauplii. , 2005, Environmental microbiology.

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

[61]  J. Oliver Wound infections caused by Vibrio vulnificus and other marine bacteria , 2005, Epidemiology and Infection.

[62]  E. Brown,et al.  Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii , 2004 .

[63]  E. Rosenberg,et al.  The Vibrio shiloi/Oculina patagonica model system of coral bleaching. , 2004, Annual review of microbiology.

[64]  S. Ellner,et al.  The rising tide of ocean diseases: unsolved problems and research priorities , 2004 .

[65]  M. Polz,et al.  Diversity and Dynamics of a North Atlantic Coastal Vibrio Community , 2004, Applied and Environmental Microbiology.

[66]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[67]  William J. Skirving,et al.  A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions , 2004, Coral Reefs.

[68]  E. Rosenberg,et al.  Temperature-Regulated Bleaching and Lysis of the Coral Pocillopora damicornis by the Novel Pathogen Vibrio coralliilyticus , 2003, Applied and Environmental Microbiology.

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

[70]  E. Rosenberg,et al.  A novel Vibrio sp. pathogen of the coral Pocilloporadamicornis , 2002 .

[71]  R. Ostfeld,et al.  Climate Warming and Disease Risks for Terrestrial and Marine Biota , 2002, Science.

[72]  Shawn W. Polson,et al.  The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[73]  J. Frias-Lopez,et al.  Partitioning of Bacterial Communities between Seawater and Healthy, Black Band Diseased, and Dead Coral Surfaces , 2002, Applied and Environmental Microbiology.

[74]  R. Aronson,et al.  White-band disease and the changing face of Caribbean coral reefs , 2001, Hydrobiologia.

[75]  Y. Loya,et al.  Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. , 2001, FEMS microbiology letters.

[76]  Y. Loya,et al.  Effect of the Environment on the Bacterial Bleaching of Corals , 2000 .

[77]  J. Burkholder,et al.  Emerging marine diseases--climate links and anthropogenic factors. , 1999, Science.

[78]  Y. Loya,et al.  Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1 , 1998 .

[79]  S. Altekruse,et al.  The role of Gulf Coast oysters harvested in warmer months in Vibrio vulnificus infections in the United States, 1988-1996. Vibrio Working Group. , 1998, The Journal of infectious diseases.

[80]  Y. Loya,et al.  Effect of Temperature on Adhesion ofVibrio Strain AK-1 to Oculina patagonica and on Coral Bleaching , 1998, Applied and Environmental Microbiology.

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

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

[83]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[84]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[85]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[86]  V. Jeffries Three Vibrio strains pathogenic to larvae of Crassostrea gigas and Ostrea edulis , 1982 .

[87]  O. Hoegh‐Guldberg Coral reefs in a century of rapid environmental change , 2004 .

[88]  K. Ritchie,et al.  Microbial Communities of Coral Surface Mucopolysaccharide Layers , 2004 .

[89]  F. Thompson,et al.  Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. , 2003, International journal of systematic and evolutionary microbiology.

[90]  J Swings,et al.  Genomic diversity amongst Vibrio isolates from different sources determined by fluorescent amplified fragment length polymorphism. , 2001, Systematic and applied microbiology.

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

[92]  I. Furuta,et al.  Bacterial Infection , 2020, Definitions.

[93]  R. Colwell,et al.  Vibrio tubiashii sp. nov., a Pathogen of Bivalve Mollusks , 1984 .