Science China Earth Sciences

, Volume 63, Issue 1, pp 157–166 | Cite as

Antagonism between coral pathogen Vibrio coralliilyticus and other bacteria in the gastric cavity of scleractinian coral Galaxea fascicularis

  • Kaihao Tang
  • Waner Zhan
  • Yiqing Zhou
  • Tao Xu
  • Xiaoqing Chen
  • Weiquan Wang
  • Zhenshun Zeng
  • Yan WangEmail author
  • Xiaoxue WangEmail author
Research Paper


Scleractinian corals host numerous microbial symbionts with different types of interactions. The gastric cavity of scleractinian coral, as a semiclosed subenvironment with distinct chemical characteristics (e.g., dissolved O2, pH, alkalinity, and nutrients), harbors a distinct microbial community and a diverse array of bacteria that can be pathogenic or beneficial. Galaxea fascicularis is one of the dominant massive scleractinian coral species on inshore fringing reefs in the northern South China Sea. Although the abundance of coral-associated bacteria has been investigated in G. fascicularis, less is known about the microorganisms in the gastric cavity. In this study, we specially isolated cultivable bacterial strains from the gastric cavity of G. fascicularis collected from Hainan Island using a noninvasive sampling approach. Among the 101 representative bacterial strains, one Vibrio coralliilyticus strain, SCSIO 43001, was found to be a temperature-dependent opportunistic pathogen of G. fascicularis. The antagonistic activity between the 100 strains and V. coralliilyticus SCSIO 43001 was tested using a modified Burkholder diffusion assay. Our results showed that V. coralliilyticus SCSIO 43001 inhibits the growth of Erythrobacterflavus and Sphingomonas yabuuchiae. Additionally, we found that three Pseudoalteromonas strains showed moderate to high anti-bacterial activity against V. coralliilyticus SCSIO 43001 and several other coral-associated Gram-negative bacterial strains. These results suggest that competition between the coral pathogen and other bacteria also occurs in the gastric cavity of coral, and Pseudoalteromonas strains in the gastric cavity of G. fascicularis may provide a protective role in the defense against co-inhabiting coral pathogens at elevated temperature.


Coral pathogen Galaxea fascicularis Scleractinian coral Vibrio coralliilyticus 



This work was supported by the National Key R&D Program of China (Grant Nos. 2018YFC1406500 & 2017YFC0506303), the National Natural Science Foundation of China (Grant Nos. 41706172, 31625001 & 41376174) and the Hainan Provincial Key R&D (Grant No. ZDYF2018108).

Supplementary material


  1. Agostini S, Suzuki Y, Higuchi T, Casareto B E, Yoshinaga K, Nakano Y, Fujimura H. 2012. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs, 31: 147–156Google Scholar
  2. Basler M, Ho B T, Mekalanos J J. 2013. Tit-for-tat: Type VI secretion system counterattack during bacterial cell-cell interactions. Cell, 152: 884–894Google Scholar
  3. Bosch T C G. 2013. Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu Rev Microbiol, 67: 499–518Google Scholar
  4. Bosch T C G, McFall-Ngai M J. 2011. Metaorganisms as the new frontier. Zoology, 114: 185–190Google Scholar
  5. Bowman J P. 2007. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs, 5: 220–241Google Scholar
  6. Burkholder P R, Pfister R M, Leitz F H. 1966. Production of a pyrrole antibiotic by a marine bacterium. Appl Microbiol, 14: 649–653Google Scholar
  7. Cai L, Tian R M, Zhou G, Tong H, Wong Y H, Zhang W, Chui A P Y, Xie J Y, Qiu J W, Ang P O, Liu S, Huang H, Qian P Y. 2018. Exploring coral microbiome assemblages in the South China Sea. Sci Rep, 8: 2428Google Scholar
  8. Chao L, Levin B R. 1981. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA, 78: 6324–6328Google Scholar
  9. Chen D D, Wang D R, Zhu J T, Li Y C, Wu X X, Wang Y. 2013. Identification and characterization of microsatellite markers for scleractinian coral Galaxea fascicularis and its symbiotic zooxanthellae. Conservation Genet Resour, 5: 741–743Google Scholar
  10. Chimetto Tonon L A, Thompson J R, Moreira A P B, Garcia G D, Penn K, Lim R, Berlinck R G S, Thompson C C, Thompson F L. 2017. Quantitative detection of active vibrios associated with white plague disease in Mussismilia braziliensis corals. Front Microbiol, 8: 2272Google Scholar
  11. Cornforth D M, Foster K R. 2015. Antibiotics and the art of bacterial war. Proc Natl Acad Sci USA, 112: 10827–10828Google Scholar
  12. Feher D, Barlow R, McAtee J, Hemscheidt T K. 2010. Highly brominated antimicrobial metabolites from a marine Pseudoalteromonas sp.. J Nat Prod, 73: 1963–1966Google Scholar
  13. García-Bayona L, Comstock L E. 2018. Bacterial antagonism in host-associated microbial communities. Science, 361: eaat2456Google Scholar
  14. Garren M, Son K, Tout J, Seymour J R, Stocker R. 2016. Temperature-induced behavioral switches in a bacterial coral pathogen. ISME J, 10: 1363–1372Google Scholar
  15. Gavish A R, Shapiro O H, Kramarsky-Winter E, Vardi A. 2018. Microscale tracking of coral disease reveals timeline of infection and heterogeneity of polyp fate. bioRxiv, 302778Google Scholar
  16. Gong S Q, Chai G J, Xiao Y L, Xu L J, Yu K F, Li J L, Liu F, Cheng H, Zhang F L, Liao B L, Li Z Y. 2018. Flexible symbiotic associations of Symbiodinium with five typical coral species in tropical and subtropical reef regions of the northern South China Sea. Front Microbiol, 9: 2485Google Scholar
  17. Herndl G J, Velimirov B. 1985. Bacteria in the coelenteron of Anthozoa: Control of coelenteric bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol, 93: 115–130Google Scholar
  18. Hibbing M E, Fuqua C, Parsek M R, Peterson S B. 2010. Bacterial competition: Surviving and thriving in the microbial jungle. Nat Rev Microbiol, 8: 15–25Google Scholar
  19. Jones C G, Lawton J H, Shachak M. 1994. Organisms as ecosystem engineers. Oikos, 69: 373–386Google Scholar
  20. Kalinovskaya N I, Ivanova E P, Alexeeva Y V, Gorshkova N M, Kuznetsova T A, Dmitrenok A S, Nicolau D V. 2004. Low-molecular-weight, biologically active compounds from marine Pseudoalteromonas species. Curr Microbiol, 48: 441–446Google Scholar
  21. Kim B R. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser, 322: 1–14Google Scholar
  22. Kim O S, Cho Y J, Lee K, Yoon S H, Kim M, Na H, Park S C, Jeon Y S, Lee J H, Yi H, Won S, Chun J. 2012. Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evolary Microbiol, 62: 716–721Google Scholar
  23. Krediet C J, Ritchie K B, Alagely A, Teplitski M. 2013. Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J, 7: 980–990Google Scholar
  24. Krediet C J, Ritchie K B, Cohen M, Lipp E K, Sutherland K P, Teplitski M. 2009. Utilization of mucus from the coral Acropora palmata by the pathogen Serratia marcescens and by environmental and coral commensal bacteria. Appl Environ Microbiol, 75: 3851–3858Google Scholar
  25. Ley R E, Lozupone C A, Hamady M, Knight R, Gordon J I. 2008. Worlds within worlds: Evolution of the vertebrate gut microbiota. Nat Rev Microbiol, 6: 776–788Google Scholar
  26. Li J, Chen Q, Zhang S, Huang H, Yang J, Tian X P, Long L J, Schuch R. 2013. Highly heterogeneous bacterial communities associated with the South China Sea reef corals Porites lutea, Galaxea fascicularis and Acropora millepora. PLoS ONE, 8: e71301Google Scholar
  27. Liang J Y, Yu K F, Wang Y H, Huang X Y, Huang W, Qin Z J, Pan Z L, Yao Q C, Wang W J, Wu Z C. 2017. Distinct bacterial communities associated with massive and branching scleractinian corals and potential linkages to coral susceptibility to thermal or cold stress. Front Microbiol, 8: 979Google Scholar
  28. Littman R A, Bourne D G, Willis B L. 2010. Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol Ecol, 19: 1978–1990Google Scholar
  29. Liu G Y, Nizet V. 2009. Color me bad: Microbial pigments as virulence factors. Trends Microbiol, 17: 406–413Google Scholar
  30. McFall-Ngai M, Hadfield M G, Bosch T C G, Carey H V, Domazet-Lošo T, Douglas A E, Dubilier N, Eberl G, Fukami T, Gilbert S F, Hentschel U, King N, Kjelleberg S, Knoll A H, Kremer N, Mazmanian S K, Metcalf J L, Nealson K, Pierce N E, Rawls J F, Reid A, Ruby E G, Rumpho M, Sanders J G, Tautz D, Wernegreen J J. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA, 110: 3229–3236Google Scholar
  31. Mitova M, Tommonaro G, Hentschel U, Müller W E G, De Rosa S. 2004. Exocellular cyclic dipeptides from a Ruegeria strain associated with cell cultures of Suberites domuncula. Mar Biotech, 6: 95–103Google Scholar
  32. Miura N, Motone K, Takagi T, Aburaya S, Watanabe S, Aoki W, Ueda M. 2019. Ruegeria sp. strains isolated from the reef-building coral Galaxea fascicularis inhibit growth of the temperature-dependent pathogen Vibrio coralliilyticus. Mar Biotechnol, 21: 1–8Google Scholar
  33. Pantos O, Bongaerts P, Dennis P G, Tyson G W, Hoegh-Guldberg O. 2015. Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J, 9: 1916–1927Google Scholar
  34. Peixoto R S, Rosado P M, Leite DCA, Rosado A S, Bourne D G. 2017. Beneficial microorganisms for corals (BMC): Proposed mechanisms for coral health and resilience. Front Microbiol, 8: 341Google Scholar
  35. Rivers A R, Burns A S, Chan L K, Moran M A. 2016. Experimental identification of small non-coding RNAs in the model marine bacterium Ruegeria pomeroyi DSS-3. Front Microbiol, 7: 380Google Scholar
  36. Rosado P M, Leite D C A, Duarte G A S, Chaloub R M, Jospin G, Nunes da Rocha U P, Saraiva J, Dini-Andreote F, Eisen J A, Bourne D G, Peixoto R S. 2018. Marine probiotics: Increasing coral resistance to bleaching through microbiome manipulation. ISME J, 13: 921–936Google Scholar
  37. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. 2007. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol, 5: 355–362Google Scholar
  38. Rubio-Portillo E, Santos F, Martínez-García M, de Los Ríos A, Ascaso C, Souza-Egipsy V, Ramos-Esplá A A, Anton J. 2016. Structure and temporal dynamics of the bacterial communities associated to microhabitats of the coral Oculina patagonica. Environ Microbiol, 18: 4564–4578Google Scholar
  39. Rypien K L, Ward J R, Azam F. 2010. Antagonistic interactions among coral-associated bacteria. Environ Microbiol, 12: 28–39Google Scholar
  40. Sachs J L, Skophammer R G, Regus J U. 2011. Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci USA, 108: 10800–10807Google Scholar
  41. Sharon G, Rosenberg E. 2008. Bacterial growth on coral mucus. Curr Microbiol, 56: 481–488Google Scholar
  42. Shnit-Orland M, Kushmaro A. 2009. Coral mucus-associated bacteria: A possible first line of defense. FEMS Microbiol Ecol, 67: 371–380Google Scholar
  43. Shnit-Orland M, Sivan A, Kushmaro A. 2012. Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb Ecol, 64: 851–859Google Scholar
  44. Soliev A B, Hosokawa K, Enomoto K. 2011. Bioactive pigments from marine bacteria: Applications and physiological roles. Evid-based Compl Alt Med, 2011: 1–17Google Scholar
  45. Sonnenschein E C, Nielsen K F, D’Alvise P, Porsby C H, Melchiorsen J, Heilmann J, Kalatzis P G, López-Pérez M, Bunk B, Spröer C, Middelboe M, Gram L. 2017. Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis. ISME J, 11: 569–583Google Scholar
  46. Speare L, Cecere A G, Guckes K R, Smith S, Wollenberg M S, Mandel M J, Miyashiro T, Septer A N. 2018. Bacterial symbionts use a type VI secretion system to eliminate competitors in their natural host. Proc Natl Acad Sci USA, 115: E8528–E8537Google Scholar
  47. Stubbendieck R M, Straight P D. 2016. Multifaceted interfaces of bacterial competition. J Bacteriol, 198: 2145–2155Google Scholar
  48. Tang K H, Wang Y, Wang X X. 2019. Recent progress on signalling molecules of coral-associated microorganisms. Sci China Earth Sci, 62: 609–618Google Scholar
  49. Ushijima B, Smith A, Aeby G S, Callahan S M. 2012. Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS ONE, 7: e46717Google Scholar
  50. Ushijima B, Videau P, Burger A H, Shore-Maggio A, Runyon C M, Sudek M, Aeby G S, Callahan S M, Wommack K E. 2014. Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol, 80: 2102–2109Google Scholar
  51. Ushijima B, Videau P, Poscablo D, Stengel J W, Beurmann S, Burger A H, Aeby G S, Callahan S M. 2016. Mutation of the toxR or mshA genes from Vibrio coralliilyticus strain OCN014 reduces infection of the coral Acropora cytherea. Environ Microbiol, 18: 4055–4067Google Scholar
  52. van Oppen M J H, Oliver J K, Putnam H M, Gates R D. 2015. Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA, 112: 2307–2313Google Scholar
  53. Veron J E N. 2000. Paleobiology: Reef processes in the long view. Science, 287: 811–812Google Scholar
  54. Vynne N G, Månsson M, Nielsen K F, Gram L. 2011. Bioactivity, chemical profiling, and 16S rRNA-based phylogeny of Pseudoalteromonas strains collected on a global research cruise. Mar Biotechnol, 13: 1062–1073Google Scholar
  55. Weisburg W G, Barns S M, Pelletier D A, Lane D J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol, 173: 697–703Google Scholar
  56. Yang L H, Xiong H, Lee O O, Qi S H, Qian P Y. 2007. Effect of agitation on violacein production in Pseudoalteromonas luteoviolacea isolated from a marine sponge. Lett Appl Microbiol, 44: 625–630Google Scholar
  57. Yu K F. 2012. Coral reefs in the South China Sea: Their response to and records on past environmental changes. Sci China Earth Sci, 55: 1217–1229Google Scholar
  58. Yu M, Wang J F, Tang K H, Shi X C, Wang S S, Zhu W M, Zhang X H. 2012. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology, 158: 835–842Google Scholar
  59. Zhao W J, Caro F, Robins W, Mekalanos J J. 2018. Antagonism toward the intestinal microbiota and its effect on Vibrio cholerae virulence. Science, 359: 210–213Google Scholar
  60. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiol Rev, 32: 723–735Google Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Kaihao Tang
    • 1
  • Waner Zhan
    • 1
    • 2
  • Yiqing Zhou
    • 1
    • 2
  • Tao Xu
    • 3
  • Xiaoqing Chen
    • 3
  • Weiquan Wang
    • 1
    • 2
  • Zhenshun Zeng
    • 1
  • Yan Wang
    • 3
    Email author
  • Xiaoxue Wang
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, RNAM Center for Marine Microbiology, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Ocean CollegeHainan UniversityHaikouChina

Personalised recommendations