Abstract
Rising concentrations of atmospheric carbon dioxide are acidifying the world's oceans. Surface seawater pH is 0.1 units lower than pre-industrial values and is predicted to decrease by up to 0.4 units by the end of the century. This change in pH may result in changes in the physiology of ocean organisms, in particular, organisms that build their skeletons/shells from calcium carbonate, such as corals. This physiological change may also affect other members of the coral holobiont, for example, the microbial communities associated with the coral, which in turn may affect the coral physiology and health. In the present study, we examined changes in bacterial communities in the coral mucus, tissue and skeleton following exposure of the coral Acropora eurystoma to two different pH conditions: 7.3 and 8.2 (ambient seawater). The microbial community was different at the two pH values, as determined by denaturing gradient gel electrophoresis and 16S rRNA gene sequence analysis. Further analysis of the community in the corals maintained at the lower pH revealed an increase in bacteria associated with diseased and stressed corals, such as Vibrionaceae and Alteromonadaceae. In addition, an increase in the number of potential antibacterial activity was recorded among the bacteria isolated from the coral maintained at pH 7.3. Taken together, our findings highlight the impact that changes in the pH may have on the coral-associated bacterial community and their potential contribution to the coral host.
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References
Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O . (2008). Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105: 17442–17446.
Arboleda M, Reichardt W . (2009). Epizoic communities of prokaryotes on healthy and diseased scleractinian corals in Lingayen Gulf, Philippines. Microb Ecol 57: 117–128.
Barneah O, Ben-Dov E, Kramarsky-Winter E, Kushmaro A . (2007). Characterization of black band disease in Red Sea stony corals. Environ Microbiol 9: 1995–2006.
Ben-Haim Y, Thompson FL, Thompson CC, Cnockaert MC, Hoste B, Swings J et al. (2003). Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Microbiol 53: 309–315.
Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J . (2007). Ocean acidification disrupts induced defenses in the intertidal gastropod Littorina littorea. Biol Lett 3: 699–701.
Bourne D, Iida Y, Uthicke S, Smith-Keune C . (2007). Changes in coral-associated microbial communities during a bleaching event. ISME J 2: 350–363.
Bourne DG, Munn CB . (2005). Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Appl Environ Micro 7: 1162–1174.
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD et al. (2007). Thermal stress and coral cover as drivers of coral disease outbreaks. Plos Biology 5: 1220–1227.
Caldeira K . (2007). What corals are dying to tell us about CO2 and ocean acidification. Oceangraphy 20: 188–195.
Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A et al. (2008). One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321: 560–563.
Connell H . (1978). Diversity in tropical rain forests and coral reefs. Science 199: 1302–13100.
Cooney RP, Pantos O, Le Tissier MD, Barer MR, O’Donnell AG, Bythell JC . (2002). Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 4: 401–413.
Farber SC, Costanza R, Wilson MA . (2002). Economic and ecological concepts for valuing ecosystem services. Ecol Econ 41: 375–392.
Fine M, Tchernov D . (2007). Scleractinian coral species survive and recover from decalcification. Science 315: 1811.
Frias-Lopez J, Klaus JS, Bonheyo GT, Fouke BW . (2004). Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70: 5955–5962.
Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW . (2002). Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68: 2214–2228.
Garren M, Raymundo L, Guest J, Harvell CD, Azam F . (2009). Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4: e7319.
Gattuso JP, Frankignoulle M, Bourge I, Romaine S, Buddemeier RW . (1998). Effect of calcium carbonate saturation of seawater on coral calcification. Global and Planetary Change 18: 37–46.
Guppy R, Bythell JC . (2006). Environmental effects on bacterial diversity in surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328: 133–142.
Harvell CD, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith GW et al. (2007). Coral disease, environmental drivers, and the balance between coaral and microbial associated. Oceangraphy 20: 172–195.
Hoegh-Guldberg O . (1999). Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50: 839–866.
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Green P, Gomez E et al. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318: 1737–1742.
The International Panel on Climate Change (2007) (Report). http://www.ipcc.ch.
Ishimatsu A, Hayashi M, Lee KS, Kikkawa T, Kita J . (2005). Physiological effects on fishes in a high-CO2 world. Journal of Geophysical Research-Oceans 110: C09S09.
Kellogg CA . (2004). Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273: 81–88.
Kelman D, Kashman Y, Rosenberg E, Kushmaro A, Loya Y . (2006). Antimicrobial activity of Red Sea corals. Mar Biol 149: 357–363.
Kooperman N, Ben-Dov E, Kramarsky-Winter E, Barak Z, Kushmaro A . (2007). Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol Lett 276: 106–113.
Koren O, Rosenberg E . (2006). Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72: 5254–5259.
Kuffner BI, Andersson JA, Jokiel LP, Rodgers SK, Mackenize TF . (2007). Decreases abundance of crustose coralline algae due to ocean acidification. Nature 1: 114–117.
Lampert Y, Kalman D, Nitzan Y, Dubinsky Z, Behar A, Hill RT . (2008). Phylogenetic diversity of bacteria associated with the mucus of Red Sea corals. FEMS Microbiol Ecol 64: 187–198.
Lane DJ . (1991). 16S/23S rRNA Sequencing. John Wiley & Sons: Chichester, United Kingdom.
Loya Y, Sakai K, Nakano Y, Sambali H, Van Woesik R . (2001). Coral bleaching: the winners and the losers. Ecol Lett 4: 122–131.
Lozupone C, Hamady M, Knight R . (2006). UniFrac—An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7: 371.
Lozupone C, Knight R . (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228–8235.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Research 32: 1363–1371.
Muyzer M, Smalla K . (1998). Application of denaturing gradient gel electophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127–141.
Nithyanand P, Pandian SK . (2009). Phylogenetic characterization of culturable bacterial diversity associated with the mucus and tissue of the coral Acropora digitifera from the Gulf of Mannar. FEMS Microbiol Ecol 69: 384–394.
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.
Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC . (2003). The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Appl Environ Microbiol 5: 370–382.
Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola JM, Basile I et al. (1999). Climate and atmospheric history of the past 420 000 years from the Vostok ice core, Antarctica. Nature 399: 429–436.
Rahmstorf S, Cazenave A, Church JC, Keeling RF, Parker DE, Somerville CJ . (2007). Recent climate observations compared to projections. Science 316: 709.
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E . (2006). The coral probiotic hypothesis. Appl Environ Microbiol 8: 2067–2073.
Richardson LL, Kuta KG, Schnell S, Carlton RG . (1997). Ecology of the black band disease microbial consortium. In: Lessios HA, Macintyre IG (eds). Proceedings of the Eighth International Coral Reef Symposium vol 1 Smithsonian Tropical Research Institute: Balboa, Panama, pp 597–600.
Ritchie KB . (2006). Regulation of microbial population by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1–14.
Ritchie KB, Smith GW . (2004). Coral Health and Disease. Springer Press: New York/Berlin.
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N . (2001). Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20: 85–91.
Rohwer F, Kelly S . (2004). Coral Health and Disease. Springer Press: New York/Berlin.
Rohwer F, Seguritan V, Azam F, Knowlton N . (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1–10.
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I . (2007). The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology 5: 355–362.
Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L . (2009). The role of microorganisms in coral bleaching. ISME J 3: 139–146.
Rypien KL, Ward JR, Azam F . (2009). Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12: 28–39.
Schloss PD, Handelsman J . (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501–1506.
Schnell S, Assmus S, Richardson LLR . (1996). Role of sulfate reducing bacteria in the black band disease of corals. Abstr Annu Meet VAAM (Ver Allg Angew Mikrobiol) GBCH (Ges Biol Chem) Elsevier, Cologne, Germany, 116.
Sebens K . (1994). Biodiversity of coral reefs: what are we losing and why? Amer Zool 34: 115–133.
Sekar R, Kaczmarsky L, Richardson LL . (2008). Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser 362: 38–98.
Sekar R, Mills DK, Remily ER, Voss JD, Richardson LL . (2006). Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl Environ Microbiol 72: 5963–5973.
Shnit-Orland M, Kushmaro A . (2009). Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67: 371–380.
Siboni N, Ben-Dov E, Sivan A, Kushmaro A . (2008). Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10: 2979–2990.
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al. (2009). Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3: 512–521.
Vega-Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F et al. (2009). Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148–2163.
Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F . (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707–2719.
Acknowledgements
This work was partially supported by a grant (no. 2006318) from the United States-Israel Binational Science Foundation to EB.
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Meron, D., Atias, E., Iasur Kruh, L. et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5, 51–60 (2011). https://doi.org/10.1038/ismej.2010.102
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DOI: https://doi.org/10.1038/ismej.2010.102
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