Abstract
The community structure of coral associated microorganisms will change greatly in coral bleaching. However, the relationship between specific bacteria groups and Symbiodinium, which is easy to be found in the bleaching process, has been ignored for a long time. In this study, the changes of coral microbial community during a natural bleaching event in the South China Sea were studied by 16S rRNA gene high-throughput sequencing. The microbial community composition of bleached corals was significantly different from that of normal corals (P < 0.001). OTUs belong to Bacillus, Exiguobacterium, Oceanobacillus, Saccharibacteria and Ostreobiaceae was significantly increased in the bleaching corals. The relative abundance of 30.9% OTUS changed significantly during coral bleaching. The relative abundance of potential coral pathogenic groups was not significantly different between normal and bleaching corals. Symbiodinium positively correlated bacterial groups accounted for 6.9% and 4.3% in the normal corals and bleached corals, respectively. The dominated groups of potential Symbiodinium-partner bacteria are Lactococcus and Bacillus. The potential Symbiodinium-partner bacterial groups in bleached corals were significantly lower than that in the normal corals, which further showed their coexistence with Symbiodinium. This study provides insight into the role of potential Symbiodinium-partner bacterial groups in the coral bleaching process and supports the theory of beneficial microorganisms for corals.
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The 16S rRNA gene sequencing data has been deposited into NCBI SRA data bank under accession number SRP133762.
References
Ainsworth TD, Gates RD (2016) Corals’ microbial sentinels. Science 352:1518–1519. https://doi.org/10.1126/science.aad9957
Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evolut 25:233–240. https://doi.org/10.1016/j.tree.2009.11.001
Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55. https://doi.org/10.1007/s00227-002-0797-6
Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242. https://doi.org/10.1128/aem.69.7.4236-4242.2003
Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363. https://doi.org/10.1038/ismej.2007.112
Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562. https://doi.org/10.1016/j.tim.2009.09.004
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138. https://doi.org/10.1007/s003380050249
Caporaso JG et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carlton RG, Richardson LL (1995) Oxygen and sulfide dynamics in a horizontally migrating cyanobacterial mat: Black band disease of corals. FEMS Microbiol Ecol 18:155–162. https://doi.org/10.1016/0168-6496(95)00052-C
Gajigan AP, Diaz LA, Conaco C (2017) Resilience of the prokaryotic microbial community of Acropora digitifera to elevated temperature. Microbiol Open 6. https://doi.org/10.1002/mbo3.478
Gignoux-Wolfsohn SA, Vollmer SV (2015) Identification of candidate coral pathogens on white band disease-infected Staghorn coral. PloS One 10:e0134416. https://doi.org/10.1371/journal.pone.0134416
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17. https://doi.org/10.1007/bf00303779
Hadaidi G et al. (2017) Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas. Sci Rep 7:45362. https://doi.org/10.1038/srep45362
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162. https://doi.org/10.1126/science.1063699
Herlemann DPR, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Higuchi T et al. (2013) Bacterial enhancement of bleaching and physiological impacts on the coral Montipora digitata. J Exp Mar Biol Ecol 440:54–60. https://doi.org/10.1016/j.jembe.2012.11.011
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866. https://doi.org/10.1071/mf99078
Hughes TP et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933. https://doi.org/10.1126/science.1085046
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher-plants, algae and natural phytoplankton. Biochem Physiol Der Pflanzen 167:191–194
Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419-5425. https://doi.org/10.1073/pnas.091092998
Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62. https://doi.org/10.1086/378684
Koren O, Rosenberg E (2008) Bacteria associated with the bleached and cave coral Oculina patagonica. Microb Ecol 55:523–529. https://doi.org/10.1007/s00248-007-9297-z
Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc Biol Sci 280:20122328. https://doi.org/10.1098/rspb.2012.2328
Lee ST, Davy SK, Tang SL, Fan TY, Kench PS (2015) Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress. FEMS Microbiol Ecol 91. https://doi.org/10.1093/femsec/fiv142
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001
Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152. https://doi.org/10.3354/meps07008
Lins-de-Barros MM et al. (2013) Microbial community compositional shifts in bleached colonies of the Brazilian reef-building coral Siderastrea stellata. Microb Ecol 65:205–213. https://doi.org/10.1007/s00248-012-0095-x
Littman R, Willis BL, Bourne DG (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Rep 3:651–660. https://doi.org/10.1111/j.1758-2229.2010.00234.x
Littman RA, Bourne DG, Willis BL (2010) Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol Ecol 19:1978–1990. https://doi.org/10.1111/j.1365-294X.2010.04620.x
Liu Z, Chen C, Gao L, Zhang Y, Pei J, Ren C, Hu C (2016) Differences in microbial communities between healthy and bleached coral Acropora solitaryensis from Xisha Islands, South China Sea. Mar Biol Res 12:1101–1108. https://doi.org/10.1080/17451000.2016.1236201
Moreira AP et al. (2014) Culturable heterotrophic bacteria associated with healthy and bleached scleractinian Madracis decactis and the fireworm Hermodice carunculata from the remote St. Peter and St. Paul Archipelago, Brazil. Curr Microbiol 68:38–46. https://doi.org/10.1007/s00284-013-0435-1
Ng JC, Chan Y, Tun HM, Leung FC, Shin PK, Chiu JM (2015) Pyrosequencing of the bacteria associated with Platygyra carnosus corals with skeletal growth anomalies reveals differences in bacterial community composition in apparently healthy and diseased tissues. Front Microbiol 6:1142. https://doi.org/10.3389/fmicb.2015.01142
Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215. https://doi.org/10.1111/j.1574-6968.2009.01490.x
Peixoto RS, Rosado PM, Leite DC, Rosado AS, Bourne DG (2017) Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol 8:341. https://doi.org/10.3389/fmicb.2017.00341
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073. https://doi.org/10.1111/j.1462-2920.2006.01148.x
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Progress Ser 243:1–10. https://doi.org/10.3354/meps243001
Rosenberg E, Falkovitz L (2004) The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu Rev Microbiol 58:143–159. https://doi.org/10.1146/annurev.micro.58.030603.123610
Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146. https://doi.org/10.1038/ismej.2008.104
Thinesh T, Jose PA, Patterson EJK (2013) Predominant bacterial candidates associated with diseased corals from Gulf of Mannar, India. J Pure Appl Microbiol 7:2397–2403
Thinesh T, Mathews G, Patterson Edward JK (2011) Coral disease prevalence in the Palk Bay, Southeastern India - with special emphasis to black band. Indian J Mar Sci 40:813–820
Tracy AM, Koren O, Douglas N, Weil E, Harvell CD (2015) Persistent shifts in Caribbean coral microbiota are linked to the 2010 warm thermal anomaly. Environ Microbiol Rep 7:471–479. https://doi.org/10.1111/1758-2229.12274
Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pages C (2012) Autotrophic carbon budget in coral tissue: a new C-13-based model of photosynthate translocation. J Exp Biol 215:1384–1393. https://doi.org/10.1242/jeb.065201
van Oppen MJ, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA 112:2307–2313. https://doi.org/10.1073/pnas.1422301112
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Zhang Y, Yang Q, Ling J, Van Nostrand JD, Shi Z, Zhou J, Dong J (2017) Diversity and structure of diazotrophic communities in mangrove rhizosphere, revealed by high-throughput sequencing. Front Microbiol 8:2032. https://doi.org/10.3389/fmicb.2017.02032
Acknowledgements
The research was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA13020300), National Key Research and Development Program of China (2017YFC0506301, 2016YFC1403003, 2018FY100105), National Natural Science Foundation of China (41676107 and 41976147), Study on Engineering Technology of Planning, Construction and Management for Marine Ranching in Guangdong Province (GML2019ZD0402), Pearl River S&T Nova Program of Guangzhou (201806010017), Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences (ISEE2018ZD02) and Science and Technology Planning Project of Guangdong Province, China (2020B1212060058).
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Yang, Q., Zhang, Y., Ahmad, M. et al. Microbial community structure shifts and potential Symbiodinium partner bacterial groups of bleaching coral Pocillopora verrucosa in South China Sea. Ecotoxicology 30, 966–974 (2021). https://doi.org/10.1007/s10646-021-02380-y
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DOI: https://doi.org/10.1007/s10646-021-02380-y