Advertisement

33 Diversity of Bacteria Associated with the Cold Water Corals Lophelia pertusa and Madrepora oculata

  • Markus G. WeinbauerEmail author
  • Davide Oregioni
  • Anne Großkurth
  • Marie-Emanuelle Kerros
  • Tilmann Harder
  • Michael DuBow
  • Jean-Pierre Gattuso
  • Cornelia Maier
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 9)

Abstract

Recent research suggests that corals including cold-water corals harbor a diverse community of bacteria that are not only pathogens but also potential mutualists. Here we review data on bacterial community composition and diversity on the main cold-water corals framework builder species: Lophelia pertusa and Madrepora oculata. Sampling strategies such as box core, video grabs and remotely operated vehicle did not reveal strong differences between bacterial community composition as long as samples were used that looked ‘not contaminated’. However, there were strong differences of bacterial diversity between the two coral species. An analysis of bacterial community composition by pyrosequencing of L. pertusa and M. oculata revealed for the Mediterranean Sea the presence of the potential mutualists already found in the Atlantic indicating a species-specific core microbiome. The data also suggest some biogeographical differences between the Mediterranean Sea and the North Atlantic for both coral species, however, this depends on the phylogenetic levels applied. In addition, there was also indication for a shared microbiome between the Mediterranean Sea and the Atlantic. Therefore species-specific bacterial associations seem to exist, whereas the biogeographical variability can be seen as adaptation to specific environmental conditions.

Keywords

Fingerprints Pyrosequencing Biogeography Microenvironments Core microbiome 

Notes

Acknowledgements

We thank the captain and the crew of the RVs Pelagia and Thethys I’ for their support, as well as the supporting departments at NIOZ for coordination, data management and technical support. This research has been financed by the Dutch NWO/ALW project BIOSYS (no. 835.30.024 and 814.01.005) and the project COMP of the Foundation Prince Albert II (Monaco). This work is also a contribution to the ‘European Project on Ocean Acidification’ (EPOCA) which received funding from the European Community’s Seventh Framework Specific Programme (PP7/2007-2013) under grant agreement no. 211384.

References

  1. Ainsworth TD, Fine M, Blackall LL, et al (2006) Fluorescence in situ hybridization and spectral imaging of coral-associated bacterial communities. Appl Environ Microbiol 72:3016–3020PubMedPubMedCentralCrossRefGoogle Scholar
  2. An S, Couteau C, Luo F, et al (2013) Bacterial diversity of surface sand samples from the Gobi and Taklamaken deserts. Microb Ecol 66:850–860PubMedCrossRefGoogle Scholar
  3. Arnaud-Haond S, Van den Beld IMJ, Becheler R, et al (2015) Two “pillars” of cold-water coral reefs along Atlantic European margins: prevalent association of Madrepora oculata with Lophelia pertusa, from reef to colony scale. Deep-Sea Res Part 2 Top Stud Oceanogr 145:110–119CrossRefGoogle Scholar
  4. 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
  5. Bourne DG, Iida Y, Uthicke S, et al (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363PubMedCrossRefGoogle Scholar
  6. Brooke S, Jarnegren J (2013) Reproductive periodicity of the scleractinian coral Lophelia pertusa from the Trondheim Fjord. Nor Mar Biol 160:139–153CrossRefGoogle Scholar
  7. Carlier A, Le Guilloux E, Olu K, et al (2009) Trophic relationships in a deep Mediterranean cold-water coral bank (Santa Maria di Leuca, Ionian Sea). Mar Ecol Progr Ser 397:125–137CrossRefGoogle Scholar
  8. Davies AJ, Duineveld GCA, Lavaleye MSS, et al (2009) Downwelling and deep-water bottom currents as food supply mechanisms to the cold-water coral Lophelia pertusa (Scleractinia) at the Mingulay Reef complex. Limnol Oceanogr 54:620–629CrossRefGoogle Scholar
  9. Dodds LA, Roberts JM, Taylor AC, et al (2007) Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. J Exp Mar Biol Ecol 349:205–214CrossRefGoogle Scholar
  10. Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725CrossRefGoogle Scholar
  11. Duineveld GCA, Lavaleye MSS, Berghuis EM (2004) Particle flux and food supply to a seamount coldwater coral community (Galicia Bank, NW Spain). Mar Ecol Progr Ser 277:12–23CrossRefGoogle Scholar
  12. Findlay HS, Artioli Y, Navas JM, et al (2013) Tidal downwelling and implications for the carbon biogeochemistry of cold-water corals in relation to future ocean acidification and warming. Glob Chang Biol 19:2708–2719PubMedCrossRefGoogle Scholar
  13. Gori A, Grover R, Orejas C, et al (2014) Uptake of dissolved free amino acids by four cold-water coral species from the Mediterranean Sea. Deep-Sea Res Part 2 Top Stud Oceanogr:42–50CrossRefGoogle Scholar
  14. Großkurth A (2007) Analysis of bacterial community composition on the cold-water coral Lophelia pertusa and antibacterial effects of coral extracts. Diploma thesis, Carl von Ossietzky Universität, Oldenburg, Germany, 93 ppGoogle Scholar
  15. Hansson L, Agis M, Maier C, et al (2009) Community composition of bacteria associated with cold-water coral Madrepora oculata: within and between colony variability. Mar Ecol Progr Ser 397:89–102CrossRefGoogle Scholar
  16. Harder T, Lau SCK, Dobretsov S, et al (2003) A distinctive epibiotic bacterial community on the soft coral Dendronephthya sp. and antibacterial activity of coral tissue extracts suggest a chemical mechanism against bacterial epibiosis. FEMS Microbiol Ecol 43:337–347PubMedCrossRefGoogle Scholar
  17. Heissenberger A, Leppard GG, Herndl GJ (1996) Relationship between the intracellular integrity and the morphology of the capsular envelope in attached and free-living marine bacteria. Appl Environ Microbiol 62:4521–4528PubMedPubMedCentralGoogle Scholar
  18. Henry LA, Roberts JM (2007) Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep-Sea Res Part 1 Oceanogr Res Pap 54:654–672CrossRefGoogle Scholar
  19. Henry LA, Roberts JM (2017) Global biodiversity in cold-water coral reef ecosystems. In: Rossi S, Bramanti L, Gori A, et al (eds) Marine animal forests: the ecology of benthic biodiversity hotspots. Springer, Cham, pp 235–256Google Scholar
  20. Hernandez-Agreda A, Leggat W, Bongaerts P, et al (2016) The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio 7:1–10CrossRefGoogle Scholar
  21. Hernandez-Agreda A, Gates RD, Ainsworth TC (2017) Defining the core microbiome in corals’ soup. Trends Microbiol 25:125–140PubMedCrossRefGoogle Scholar
  22. Jensen S, Neufeld JD, Birkeland NK, et al (2008a) Insight into the microbial community structure of a Norwegian deep-water coral reef environment. Deep-Sea Res Part 1 Oceanogr Res Pap 55:1554–1563CrossRefGoogle Scholar
  23. Jensen S, Neufeld JD, Birkeland NK, et al (2008b) Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway. FEMS Microbiol Ecol 66:320–330PubMedCrossRefGoogle Scholar
  24. Kellogg CA (2004) Tropical archaea: diversity associated with the surface microlayer of corals. Mar Ecol Progr Ser 273:81–88CrossRefGoogle Scholar
  25. Kellogg CA, Lisle JT, Galkiewicz JP (2009) Culture- independent characterization of bacterial communities associated with the cold-water coral Lophelia pertusa in the northeastern Gulf of Mexico. Appl Environ Microbiol 73:5642–5647Google Scholar
  26. Kellogg C, Goldsmith D, Gray M (2017) Biogeographic comparison of Lophelia-associated bacterial communities in the western Atlantic reveals conserved core microbiome. Front Microbiol 8:1–15CrossRefGoogle Scholar
  27. Kiriakoulakis K, Fisher E, Wolff GA, et al (2005) Lipids and nitrogen isotopes of two deep-water corals from the North-East Atlantic: initial results and implications for their nutrition. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer, Berlin, Heidelberg, pp 715–729CrossRefGoogle Scholar
  28. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62PubMedCrossRefGoogle Scholar
  29. Kuhl M, Cohen Y, Dalsgaard T, et al (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Progr Ser 117:159–172CrossRefGoogle Scholar
  30. Larsson AI, Jarnegren J, Stromberg SM, et al (2014) Embryogenesis and larval biology of the cold-water coral Lophelia pertusa. PLoS One 9:e102222PubMedPubMedCentralCrossRefGoogle Scholar
  31. Lartaud F, Pareige S, de Rafelis M, et al (2013) A new approach for assessing cold-water coral growth using fluorescent calcein staining. Aquat Living Resour 26:187–196CrossRefGoogle Scholar
  32. Lartaud F, Pareige S, de Rafelis M, et al (2014) Temporal changes in the growth of two Mediterranean cold-water coral species, in situ and in aquaria. Deep-Sea Res Part 2 Top Stud Oceanogr 99:64–70CrossRefGoogle Scholar
  33. Lartaud F, Meistertzheim AL, Peru E, et al (2017) In situ growth experiments of reef-building cold-water corals: the good, the bad and the ugly. Deep-Sea Res Part 1 Oceanogr Res Pap 121:70–78CrossRefGoogle Scholar
  34. Le Goff-Vitry MC, Pybus OG, Rogers D (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 13:537–549PubMedCrossRefGoogle Scholar
  35. Leibold MA, Holyoak M, Mouquet N, et al (2004) The metacommunity concept: a framework for multi-scale communitgy ecology. Ecol Lett 7:601–613CrossRefGoogle Scholar
  36. Littman RA, Willis BL, Pfeffer C, et al (2009) Diversity of coral-associated bacteria differs with location but not species for three acroporids on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–163PubMedCrossRefGoogle Scholar
  37. Maier C, Hegeman J, Weinbauer MG, et al (2009) Calcification of the cold-water coral Lophelia pertusa under ambient and reduced pH. Biogeosciences 6:1671–1680CrossRefGoogle Scholar
  38. Maier C, De Kluijver A, Agis M, et al (2011) Dynamics of nutrients, total organic carbon, prokaryotes and viruses in onboard incubations of cold-water corals. Biogeosciences 8:1–34CrossRefGoogle Scholar
  39. Meistertzheim AL, Lartaud F, Arnaud-Haond S, et al (2016) Patterns of bacteria-host associations suggest different ecological strategies between two reef building cold-water coral species. Deep-Sea Res Part 1 Oceanogr Res Pap 114:12–22CrossRefGoogle Scholar
  40. Mueller CE, Larsson AL, Veuger B, et al (2014) Opportunistic feeding on various organic food sources by the cold-water coral Lophelia pertusa. Biogeosciences 11:123–133CrossRefGoogle Scholar
  41. Naumann MS, Orejas C, Ferrier-Pagès C (2014) Species-specific physiological response by the cold-water corals Lophelia pertusa and Madrepora oculata to variations within their natural temperature range. Deep-Sea Res Part 2 Top Stud Oceanogr 99:36–41CrossRefGoogle Scholar
  42. Neave M, Mitchell C, Apprill A, et al (2017) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci Rep 7:40579PubMedPubMedCentralCrossRefGoogle Scholar
  43. Neulinger SC, Jarnegren J, Ludvigsen M, et al (2008) Phenotype specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral’s nutrition, health, and distribution. Appl Environ Microbiol 74:7272–7285PubMedPubMedCentralCrossRefGoogle Scholar
  44. Neulinger SC, Gärtner A, Järnegren J, et al (2009) Tissue-associated “Candidatus Mycoplasma corallicola” and filamentous bacteria on the cold-water coral Lophelia pertusa (Scleractinia). Appl Environ Microbiol 75:1437–1444PubMedCrossRefGoogle Scholar
  45. Orejas C, Ferrier-Pagès C, Reynaud S, et al (2011) Long-term growth rates of four Mediterranean cold-water coral species maintained in aquaria. Mar Ecol Progr Ser 429:57–65CrossRefGoogle Scholar
  46. Orr JC, Fabry VJ, Aumont O, et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686PubMedCrossRefGoogle Scholar
  47. Raina JB, Tapiolas D, Willis BL, et al (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 11:3492–3501CrossRefGoogle Scholar
  48. Ray JL, Töpper B, An S, et al (2012) Effect of increased pCO2 on bacterial assemblage shifts in response to glucose addition in Fram Strait seawater mesocosms. FEMS Microbiol Ecol 82:713–723PubMedCrossRefGoogle Scholar
  49. Reitner J (2005) Calcifying extracellular mucus substances (EMS) of Madrepora oculata – a first geobiological approach. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer, Berlin, Heidelberg, pp 731–744CrossRefGoogle Scholar
  50. Reshef L, Koren O, Loya Y, et al (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073PubMedCrossRefGoogle Scholar
  51. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Progr Ser 322:1–14CrossRefGoogle Scholar
  52. Ritchie KB, Smith GW (1995) Preferential carbon utilization by surface bacterial communities from water mass, normal and white-band diseased Acropora cervicornis. Mol Mar Biol Biotechnol 4:345–335Google Scholar
  53. 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 259–263CrossRefGoogle Scholar
  54. Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547CrossRefGoogle Scholar
  55. Roberts JM, Davies AJ, Henry LA, et al (2009) Mingulay reef complex: an interdisciplinary study of cold-water coral habitat, hydrography and biodiversity. Mar Ecol Progr Ser 397:139–151CrossRefGoogle Scholar
  56. Rogers D (1999) The biology of Lophelia pertusa (Linnaeus 1758) and other deep-water reef- forming corals and impacts from human activities. Int Rev Hydrobiol 84:315–406CrossRefGoogle Scholar
  57. Rohwer F, Breitbart M, Jara J, et al (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–95CrossRefGoogle Scholar
  58. Rohwer F, Seguritan V, Farooq A, et al (2002) Diversity and distribution of coral- associated bacteria. Mar Ecol Progr Ser 243:1–10CrossRefGoogle Scholar
  59. Rosenberg E, Koren O, Reshef L, et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362PubMedCrossRefGoogle Scholar
  60. Santavy DL (1995) The diversity of microorganisms associated with marine invertebrates and their roles in the maintenance of ecosystems. In: Allsopp D, Colwell RR, Hawksworth DL (eds) Microbial diversity and ecosystem function. CAB International, Wallingford, pp 211–229Google Scholar
  61. Schöttner S, Hoffmann F, Wild C, et al (2009) Inter- and intra-habitat bacterial diversity associated with cold-water corals. ISME J 3:756–769PubMedCrossRefGoogle Scholar
  62. Schöttner S, Wild C, Hoffmann F, et al (2012) Spatial scales of bacterial diversity in cold-water coral reef ecosystems. PLoS One 7:e3209324CrossRefGoogle Scholar
  63. Silveira CB, Cavalcanti GS, Walter JM, et al (2017) Microbial processes driving coral reef organic carbon flow. FEMS Microbiol Rev 41:575–595PubMedCrossRefGoogle Scholar
  64. Taviani M, Freiwald A, Zibrowius H (2005) Deep coral growth in the Mediterranean Sea: an overview. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer, Berlin, Heidelberg, pp 137–156CrossRefGoogle Scholar
  65. Turley CM, Roberts JM, Guinotte JM (2007) Corals in deep-water: will the unseen hand of ocean acidification destroy cold-water ecosystems? Coral Reefs 26:445–448CrossRefGoogle Scholar
  66. van Bleijsweijk JDL, Whalen C, Duineveld GCA, et al (2015) Microbial assemblages on a cold-water coral mound at the SE Rockall Bank (NE Atlantic): interactions with hydrography and topography. Biogeochemistry 12:4483–4496Google Scholar
  67. Waller RG, Tyler PA (2005) The reproductive biology of two deep-water, reef-building scleractinians from the NE Atlantic Ocean. Coral Reefs 24:514–522CrossRefGoogle Scholar
  68. Weinbauer MG, Ogier J, Maier C (2012) Microbial abundance in the coelenteron and mucus of the cold-water coral Lophelia pertusa and in bottom water of the reef environment. Aquat Biol 16:209–216CrossRefGoogle Scholar
  69. Wild C, Huettel M, Klueter A (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70 59PubMedCrossRefGoogle Scholar
  70. Wild C, Mayr C, Wehrmann L, et al (2008) Organic matter release by cold water corals and its implication for fauna-microbe interactions. Mar Ecol Progr Ser 372:67–75CrossRefGoogle Scholar
  71. Wild C, Naumann M, Niggl W, et al (2010) Carbohydrate composition of mucus released by scleractinian warm- and cold-water reef corals. Aquat Biol 10:41–45CrossRefGoogle Scholar
  72. Yakimov MM, Cappello S, Crisafi E (2005) Phylogenetic survey of metabolically active microbial communities associated with the deep-sea coral Lophelia pertusa from the Apulian plateau, Central Mediterranean Sea. Deep-Sea Res Part 1 Oceanogr Res Pap 53:62–75CrossRefGoogle Scholar

Cross References

  1. Boavida J, Becheler R, Addamo A, et al (this volume) Past, present and future connectivity of Mediterranean cold-water corals: patterns, drivers and fate in a technically and environmentally changing worldGoogle Scholar
  2. D’Onghia G (this volume) Cold-water coral as shelter, feeding and life-history critical habitats for fish species: ecological interactions and fishing impactGoogle Scholar
  3. Lartaud F, Mouchi V, Chapron L, et al (this volume) Growth patterns of Mediterranean calcifying cold-water coralsGoogle Scholar
  4. Maier C, Weinbauer MG, Gattuso J-P (this volume) Fate of Mediterranean scleractinian Cold-Water Corals as a Result of Global Climate Change. A SynthesisGoogle Scholar
  5. Movilla J (this volume) A case study: variability in the calcification response of Mediterranean cold-water corals to ocean acidificationGoogle Scholar
  6. Otero M, Marin P (this volume) Conservation of cold-water corals in the Mediterranean: current status and future prospects for improvementGoogle Scholar
  7. Reynaud S, Ferrier-Pagès C (this volume) Biology and ecophysiology of Mediterranean cold-water coralsGoogle Scholar
  8. Rueda JL, Urra J, Aguilar R, et al (this volume) Cold-water coral associated fauna in the Mediterranean Sea and adjacent areasGoogle Scholar
  9. Weinbauer MG, Oregoni D, Maier C (this volume) Lophelia pertusa and Madrepora oculata: an Archaea riddle?Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Markus G. Weinbauer
    • 1
    Email author
  • Davide Oregioni
    • 1
  • Anne Großkurth
    • 2
  • Marie-Emanuelle Kerros
    • 1
  • Tilmann Harder
    • 2
  • Michael DuBow
    • 3
  • Jean-Pierre Gattuso
    • 1
    • 4
  • Cornelia Maier
    • 1
  1. 1.Sorbonne Universités, CNRS, Laboratoire d’Océanographie de VillefrancheVillefranche-sur-MerFrance
  2. 2.Bremen Marine Ecology Centre for Research and EducationUniversity of Bremen and Section Ecological Chemistry, Alfred Wegener Institute for Polar and Marine ResearchBremenGermany
  3. 3.Institute for Integrative Biology of the Cell (I2BC)CEA, CNRS UMR 9198, Université Paris-Saclay, Université Paris-SudOrsayFrance
  4. 4.Institute for Sustainable Development and International Relations, Sciences PoParisFrance

Personalised recommendations