Coral Reefs

, Volume 30, Issue 1, pp 39–52

Bacterial assemblages differ between compartments within the coral holobiont

Report

Abstract

It is widely accepted that corals are associated with a diverse and host species-specific microbiota, but how they are organized within their hosts remains poorly understood. Previous sampling techniques (blasted coral tissues, coral swabs and milked mucus) may preferentially sample from different compartments such as mucus, tissue and skeleton, or amalgamate them, making comparisons and generalizations between studies difficult. This study characterized bacterial communities of corals with minimal mechanical disruption and contamination from water, air and sediments from three compartments: surface mucus layer (SML), coral tissue and coral skeleton. A novel apparatus (the ‘snot sucker’) was used to separate the SML from tissues and skeleton, and these three compartments were compared to swab samples and milked mucus along with adjacent environmental samples (water column and sediments). Bacterial 16S rRNA gene diversity was significantly different between the various coral compartments and environmental samples (PERMANOVA, F = 6.9, df = 8, P = 0.001), the only exceptions being the complete crushed coral samples and the coral skeleton, which were similar, because the skeleton represents a proportionally large volume and supports a relatively rich microflora. Milked mucus differed significantly from the SML collected with the ‘snot sucker’ and was contaminated with zooxanthellae, suggesting that it may originate at least partially from the gastrovascular cavity rather than the tissue surface. A common method of sampling the SML, surface swabs, produced a bacterial community profile distinct from the SML sampled using our novel apparatus and also showed contamination from coral tissues. Our results indicate that microbial communities are spatially structured within the coral holobiont, and methods used to describe these need to be standardized to allow comparisons between studies.

Keywords

Bacterial communities Corals Compartments Mucus Tissue Skeleton 

References

  1. Ainsworth TD, Hoegh-Guldberg O (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4:289–296CrossRefGoogle Scholar
  2. Ainsworth TD, Fine M, Blackall LL, Hoegh-Guldberg O (2006) Flouresence in situ hybridization and spectral imaging of coral-associated bacterial communities. Appl Environ Microbiol 72:3016–3020PubMedCrossRefGoogle Scholar
  3. Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240PubMedCrossRefGoogle Scholar
  4. Allers E, Niesner C, Wild C, Pernthaler J (2008) Microbes enriched in seawater after addition of coral mucus. Appl Environ Microbiol 74:3274–3278PubMedCrossRefGoogle Scholar
  5. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46CrossRefGoogle Scholar
  6. Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174PubMedCrossRefGoogle Scholar
  7. Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562PubMedCrossRefGoogle Scholar
  8. Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309CrossRefGoogle Scholar
  9. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLOS Biol 5:1220–1227CrossRefGoogle Scholar
  10. Bythell JC, Barer MR, Cooney RP, Guest JR, O’Donnell AG, Pantos O, Le Tissier MDA (2002) Histopathological methods for the investigation of microbial communities associated with disease lesions in reef corals. Lett Appl Microbiol 34:359–364PubMedCrossRefGoogle Scholar
  11. Clarke KR, Warwick RM (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol Prog Ser 216:265–278CrossRefGoogle Scholar
  12. Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Ogata H, Abergel C (2009) Mimivirus and mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol 101:172–180PubMedCrossRefGoogle Scholar
  13. Coffroth MA (1990) Mucous sheet formation on poritid corals—an evaluation of coral mucus as a nutrient source on reefs. Mar Biol 105:39–49CrossRefGoogle Scholar
  14. Cooney RP, Pantos O, Le Tissier MDA, 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 4:401–413PubMedCrossRefGoogle Scholar
  15. Croquer A, Bastidas C, Lipscomb D (2006) Folliculinid ciliates: a new threat to Caribbean corals? Dis Aquat Org 69:75–78PubMedCrossRefGoogle Scholar
  16. Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the Staghorn Coral Acropora acuminata. Mar Biol 60:81–90CrossRefGoogle Scholar
  17. Crossland CJ, Hatcher BG, Atkinson MJ, Smith SV (1984) Dissolved nutrients of a high-latitude coral-reef, Houtman Abrolhos Islands, Western-Australia. Mar Ecol Prog Ser 14:159–163CrossRefGoogle Scholar
  18. Daumas R, Galois R, Thomassin BA (1981) Biochemical composition of soft and hard coral mucus on a New Caledonian lagoonal reef. Proc 4th Int Coral Reef Symp:59–67Google Scholar
  19. Davy SK, Burchett SG, Dale AL, Davies P, Davy JE, Muncke C, Hoegh-Guldberg O, Wilson WH (2006) Viruses: agents of coral disease? Dis Aquat Org 69:101–110PubMedCrossRefGoogle Scholar
  20. Dong ZJ, Huang H, Huang LM, Li YC (2009) Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the Xisha Islands in the South China Sea. J Syst Evol 47:321–326CrossRefGoogle Scholar
  21. Ducklow HW, Mitchell R (1979a) Composition of mucus released by coral reef coelenterates. Oceanography 24:706–714Google Scholar
  22. Ducklow HW, Mitchell R (1979b) Bacterial-populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725CrossRefGoogle Scholar
  23. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc of Lond B Biol Sci 269:1205–1210CrossRefGoogle Scholar
  24. Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Freshw Res 55:115–121CrossRefGoogle Scholar
  25. Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208:75–81PubMedCrossRefGoogle Scholar
  26. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68:2214–2228PubMedCrossRefGoogle Scholar
  27. Gil-Agudelo DL, Fonseca DP, Weil E, Garzon-Ferreira J, Smith GW (2007) Bacterial communities associated with the mucopolysaccharide layers of three coral species affected and unaffected with dark spots disease. Can J Microbiol 53:465–471PubMedCrossRefGoogle Scholar
  28. Golubic S, Radtke G, Le Campion-Alsumard T (2005) Endolithic fungi in marine ecosystems. Trends Microbiol 13:229–235PubMedCrossRefGoogle Scholar
  29. Guppy R, Bythell JC (2006) Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328:133–142CrossRefGoogle Scholar
  30. Herndl GJ, Velimirov B (1985) Bacteria in the coelenteron of Anthozoa—control of coelenteric bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93:115–130CrossRefGoogle Scholar
  31. Herndl GJ, Velimirov B, Krauss RE (1985) Heterotrophic nutrition and control of bacterial density in the coelenteron of the Giant Sea-Anemone Stoichactis giganteum. Mar Ecol Prog Ser 22:101–105CrossRefGoogle Scholar
  32. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  33. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  34. Jatkar AA, Brown BE, Bythell JC, Guppy R, Morris NJ, Pearson JP (2010) Measuring mucus thickness in reef corals using a technique devised for vertebrate applications. Mar Biol 157:261–267CrossRefGoogle Scholar
  35. Johnston IS, Rohwer F (2007) Microbial landscapes on the outer tissue surfaces of the reef-building coral Porites compressa. Coral Reefs 26:375–383CrossRefGoogle Scholar
  36. Kellogg CA (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88CrossRefGoogle Scholar
  37. Kimes NE, Van Nostrand JD, Weil E, Zhou JZ, Morris PJ (2010) Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol 12:541–556PubMedCrossRefGoogle Scholar
  38. Kirkwood M, Todd JD, Rypien KL, Johnston AWB (2010) The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate. ISME J 4:147–150PubMedCrossRefGoogle Scholar
  39. Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2005) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24:129–137CrossRefGoogle Scholar
  40. 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 276:106–113PubMedCrossRefGoogle Scholar
  41. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in the summer and winter. Appl Environ Microbiol 72:5254–5259PubMedCrossRefGoogle Scholar
  42. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS One 5:e10401PubMedCrossRefGoogle Scholar
  43. Lampert Y, Kelman 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 64:187–198PubMedCrossRefGoogle Scholar
  44. Le Campion-Alsumard T, Golubic S, Priess K (1995) Fungi in corals—symbiosis or disease—interaction between polyps and fungi causes pearl-like skeleton niomineralization. Mar Ecol Prog Ser 117:137–147CrossRefGoogle Scholar
  45. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000PubMedCrossRefGoogle Scholar
  46. Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007a) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44CrossRefGoogle Scholar
  47. Lesser MP, Falcon LI, Rodriguez-Roman A, Enriquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007b) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152CrossRefGoogle Scholar
  48. Marhaver KL, Edwards RA, Rohwer F (2008) Viral communities associated with healthy and bleaching corals. Environ Microbiol 10:2277–2286PubMedCrossRefGoogle Scholar
  49. Means JC, Sigleo AC (1986) Contribution of coral-reef mucus to the colloidal organic pool in the vicinity of Discovery Bay, Jamaica, WI. Bull Mar Sci 39:110–118Google Scholar
  50. Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937CrossRefGoogle Scholar
  51. Mouchka ME, Hewson J, Harvell CD (2010) Coral-associated bacterial assemblages: Current knowledge and the potential for climate-driven impacts. Integr Comp Biol. doi:10.1093/icb/icq061
  52. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing Gradient Gel-Electrophoresis Analysis of Polymerase Chain Reaction-Amplified Genes-Coding for 16 s Ribosomal-RNA. Appl Environ Microbiol 59:695–700PubMedGoogle Scholar
  53. Naumann MS, Richter C, el-Zibdah M, Wild C (2009) Coral mucus as an efficient trap for picoplanktonic cyanobacteria: implications for pelagic-benthic coupling in the reef ecosystem. Mar Ecol Prog Ser 385:65–76CrossRefGoogle Scholar
  54. 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. Environ Microbiol 5:370–382PubMedCrossRefGoogle Scholar
  55. Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin BA (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Mar Biol 136:19–27CrossRefGoogle Scholar
  56. Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501PubMedCrossRefGoogle Scholar
  57. Ravindran J, Raghukumar C, Raghukumar S (2001) Fungi in Porites lutea: association with healthy and diseased corals. Dis Aquat Org 47:219–228PubMedCrossRefGoogle Scholar
  58. Ritchie AE (2005) Bacterial composition of surface associated microbes found in three Hawaiian coral species: Porites compressa, Porites lobata, and Montipora capitata. J Young Investigators 12(4). http://www.jyi.org/research/re.php?id=140
  59. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  60. Ritchie KB, Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 259–264Google Scholar
  61. Rivest EB, Baker DM, Rypien KL, Harvell CD (2010) Nitrogen source preference of Aspergillus sydowii, an infective agent associated with aspergillosis of sea fan corals. Limnol Oceanogr 55:386–392CrossRefGoogle Scholar
  62. Rohwer F, Kelley S (2004) Culture-independent analyses of coral-associated microbes. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 265–277Google Scholar
  63. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  64. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  65. 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 5:355–362PubMedCrossRefGoogle Scholar
  66. Rypien KL, Baker DM (2009) Isotopic labeling and antifungal resistance as tracers of gut passage of the sea fan pathogen Aspergillus sydowii. Dis Aquat Org 86:1–7PubMedCrossRefGoogle Scholar
  67. Sanchez O, Gasol JM, Massana R, Mas J, Pedros-Alio C (2007) Comparison of different denaturing gradient gel electrophoresis primer sets for the study of marine bacterioplankton communities. Appl Environ Microbiol 73:5962–5967PubMedCrossRefGoogle Scholar
  68. Sebastian CR, Sink KJ, McClanahan TR, Cowan DA (2009) Bleaching response of corals and their Symbiodinium communities in southern Africa. Mar Biol 156:2049–2062CrossRefGoogle Scholar
  69. Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488PubMedCrossRefGoogle Scholar
  70. Shashar N, Banaszak AT, Lesser MP, Amrami D (1997) Coral endolithic algae: life in a protected environment. Pac Sci 51:167–173Google Scholar
  71. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defence. FEMS Microbiol Ecol 67:371–380PubMedCrossRefGoogle Scholar
  72. Siboni N, Lidor M, Kramarsky-Winter E, Kushmaro A (2007) Conditioning film and initial biofilm formation on ceramics tiles in the marine environment. FEMS Microbiol Lett 274:24–29PubMedCrossRefGoogle Scholar
  73. Smith CJ, Danilowicz BS, Meijer WG (2007) Characterization of the bacterial community associated with the surface and mucus layer of whiting (Merlangius merlangus). FEMS Microbiol Ecol 62:90–97PubMedCrossRefGoogle Scholar
  74. Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA (2009) Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713CrossRefGoogle Scholar
  75. Toller WW, Rowan R, Knowlton N (2002) Genetic evidence for a protozoan (phylum Apicomplexa) associated with corals of the Montastraea annularis species complex. Coral Reefs 21:143–146Google Scholar
  76. Webster NS, Bourne D (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94PubMedCrossRefGoogle Scholar
  77. Wegley L, Yu YN, Breitbart M, Casas V, Kline DI, Rohwer F (2004) Coral-associated archaea. Mar Ecol Prog Ser 273:89–96CrossRefGoogle Scholar
  78. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jergensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70PubMedCrossRefGoogle Scholar
  79. Wild C, Naumann MS, Haas A, Struck U, Mayer FW, Rasheed MY, Huettel M (2009) Coral sand O2 uptake and pelagic-benthic coupling in a subtropical fringing reef, Aqaba, Red Sea. Aquat Biol 6:133–142CrossRefGoogle Scholar
  80. Wilson WH, Francis I, Ryan K, Davy SK (2001) Temperature induction of viruses in symbiotic dinoflagellates. Aquat Microb Ecol 25:99–102CrossRefGoogle Scholar
  81. Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.School of Biology, Ridley BuildingUniversity of NewcastleNewcastle upon TyneUK
  2. 2.Departamento de estudios AmbientalesUniversidad Simon BolivarSartenejasVenezuela

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