New directions in coral reef microbial ecology

Environmental Microbiology

Volumn 14, Issue 4, 2012, Pages 833-844

  Garren, Melissa ^a   Azam, Farooq ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANTHOZOA; CLIMATE CHANGE; CORAL REEF; ECOLOGY; ENVIRONMENTAL PROTECTION; MICROBIOLOGY; PHYSIOLOGY; SEA; SEDIMENT; SHORT SURVEY;

ANIMALS; ANTHOZOA; CLIMATE CHANGE; CONSERVATION OF NATURAL RESOURCES; CORAL REEFS; ECOLOGY; GEOLOGIC SEDIMENTS; OCEANS AND SEAS; WATER MICROBIOLOGY;

ANTHOZOA;

EID: 84859308135     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02597.x     Document Type: Short Survey

References (109)

1. Ahmed, T., Shimizu, T.S., and Stocker, R. (2010) Microfluidics for bacterial chemotaxis. Integr Biol 2: 604-629.
2. Ainsworth, T.D., Thurber, R.V., and Gates, R.D. (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25: 233-240.
3. Allers, E., Niesner, C., Wild, C., and Pernthaler, J. (2008) Microbes enriched in seawater after addition of coral mucus. Appl Environ Microbiol 74: 3274-3278.
4. Apprill, A., and Rappe, M.S. (2011) Response of the microbial community to coral spawning in lagoon and reef flat environments of Hawaii, USA. Aquat Microb Ecol 62: 251-266.
5. Azam, F. (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280: 694-696.
6. Azam, F., and Malfatti, F. (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782-791.
7. Baghdasarian, G., and Muscatine, L. (2000) Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol Bull 199: 278-286.
8. Barott, K.L., Rodriguez-Brito, B., Janouskovec, J., Marhaver, K.L., Smith, J.E., Keeling, P., etal. (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13: 1192-1204.
9. Beman, J.M., Roberts, K.J., Wegley, L., Rohwer, F., and Francis, C.A. (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73: 5642-5647.
10. Bourne, D.G., Garren, M., Work, T.M., Rosenberg, E., Smith, G.W., and Harvell, C.D. (2009) Microbial disease and the coral holobiont. Trends Microbiol 17: 554-562.
11. Bourne, D.G., Muirhead, A., and Sato, Y. (2011) Changes in sulfate-reducing bacterial populations during the onset of black band disease. ISME J 5: 559-564.
12. Brown, B.E., and Bythell, J.C. (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296: 291-309.
13. Casareto, B.E., Charpy, L., Langlade, M.J., Suzuki, T., Ohba, H., Niraula, M., etal. (2008) Nitrogen fixation in coral reef environments. Proceedings of the 11th International Coral Reef Symposum, Ft. Lauderdale, Florida, pp. 890-894.
14. Charpy, L., Palinska, K.A., Casareto, B., Langlade, M.J., Suzuki, Y., Abed, R.M.M., etal. (2010) Dinitrogen-fixing cyanobacteria in microbial mats of two shallow coral reef ecosystems. Microb Ecol 59: 174-186.
15. Chen, C.P., Tseng, C.H., Chen, C.A., and Tang, S.L. (2011) The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5: 728-740.
16. Coffroth, M.A. (1990) Mucous sheet formation on poritid corals - an evaluation of coral mucus as a nutrient source on reefs. Mar Biol 105: 39-49.
17. Dinsdale, E.A., Pantos, O., Smriga, S., Edwards, R.A., Angly, F., Wegley, L., etal. (2008) Microbial ecology of four coral atolls in the northern line islands. PLoS ONE 3: e1584.
18. van Duyl, F.C., and Gast, G.J. (2001) Linkage of small-scale spatial variations in DOC, inorganic nutrients and bacterioplankton growth with different coral reef water types. Aquat Microb Ecol 24: 17-26.
19. van Duyl, F.C., Gast, G.J., Steinhoff, W., Kloff, S., Veldhuis, M.J.W., and Bak, R.P.M. (2002) Factors influencing the short-term variation in phytoplankton composition and biomass in coral reef waters. Coral Reefs 21: 293-306.
20. Efrony, R., Loya, Y., Bacharach, E., and Rosenberg, E. (2007) Phage therapy of coral disease. Coral Reefs 26: 7-13.
21. Efrony, R., Atad, I., and Rosenberg, E. (2009) Phage therapy of coral white plague disease: properties of phage BA3. Curr Microbiol 58: 139-145.
22. Ferrier-Pages, C., Gattuso, J.P., Cauwet, G., Jaubert, J., and Allemand, D. (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172: 265-274.
23. Gaidos, E., Rusch, A., and Ilardo, M. (2011) Ribosomal tag pyrosequencing of DNA and RNA from benthic coral reef microbiota: community spatial structure, rare members and nitrogen-cycling guilds. Environ Microbiol 13: 1462-2920.
24. Garren, M., and Azam, F. (2010) New method for counting bacteria associated with coral mucus. Appl Environ Microbiol 76: 6128-6133.
25. Garren, M., Smriga, S., and Azam, F. (2008) Gradients of coastal fish farm effluents and their effect on coral reef microbes. Environ Microbiol 10: 2299-2312.
26. Garren, M., Raymundo, L., Guest, J., Harvell, C.D., and Azam, F. (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS ONE 4: e7319.
27. Gast, G.J., Wiegman, S., Wieringa, E., van Duyl, F.C., and Bak, R.P.M. (1998) Bacteria in coral reef water types: removal of cells, stimulation of growth and mineralization. Mar Ecol Prog Ser 167: 37-45.
28. Gast, G.J., Jonkers, P.J., van Duyl, F.C., and Bak, R.P.M. (1999) Bacteria, flagellates and nutrients in island fringing coral reef waters: influence of the ocean, the reef and eutrophication. Bull Mar Sci 65: 523-538.
29. Genin, A., Monismith, S.G., Reidenbach, M.A., Yahel, G., and Koseff, J.R. (2009) Intense benthic grazing of phytoplankton in a coral reef. Limnol Oceanogr 54: 938-951.
30. Gilbert, J.A., and Dupont, C.L. (2011) Microbial metagenomics: beyond the genome. Annu Rev Mar Sci 3: 347-371.
31. de Goeij, J.M., and van Duyl, F.C. (2007) Coral cavities are sinks of dissolved organic carbon (DOC). Limnol Oceanogr 52: 2608-2617.
32. Haagensen, J.A.J., Regenberg, B., and Sternberg, C. (2011) Advanced microscopy of microbial cells. High Resolution Microbial Single Cell Analytics 124: 21-54.
33. Hama, T., Hama, J., and Handa, N.(1993) 13C tracer methodology in microbial ecology with special reference to primary production processes in aquatic environments. In Advances in Microbial Ecology. Jones, J.G. (ed.). New York, USA: Plenum Press, pp. 39-83.
34. Herndl, G.J. (1991) Microbial biomass dynamics along a trophic gradient at the atlantic barrier-reef off belize (Central-America). P S Z N I: Mar Ecol 12: 41-51.
35. Hewson, I., and Fuhrman, J.A. (2006) Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities. Mar Ecol Prog Ser 306: 79-86.
36. Hoch, M.P., Dillon, K.S., Coffin, R.B., and Cifuentes, L.A. (2008) Sensitivity of bacterioplankton nitrogen metabolism to eutrophication in sub-tropical coastal waters of Key West, Florida. Mar Pollut Bull 56: 913-926.
37. Holmer, M., Duarte, C.M., Heilskov, A., Olesen, B., and Terrados, J. (2003) Biogeochemical conditions in sediments enriched by organic matter from net-pen fish farms in the Bolinao area, Philippines. Mar Pollut Bull 46: 1470-1479.
38. Huettel, M., Wild, C., and Gonelli, S. (2006) Mucus trap in coral reefs: formation and temporal evolution of particle aggregates caused by coral mucus. Mar Ecol Prog Ser 307: 69-84.
39. Hughes, T.P., Graham, N.A.J., Jackson, J.B.C., Mumby, P.J., and Steneck, R.S. (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25: 633-642.
40. Jatkar, A.A., Brown, B.E., Bythell, J.C., Guppy, R., Morris, N.J., and Pearson, J.P. (2010) Coral mucus: the properties of its constituent mucins. Biomacromolecules 11: 883-888.
41. Johannes, R.E., McCloske, L., Marsh, J.A., Marshall, N., Maragos, J., Alberts, J., etal. (1972) Metabolism of some coral reef communities - team study of nutrient and energy flux at eniwetok. Bioscience 22: 541-543.
42. Jones, R.J. (2007) Chemical contamination of a coral reef by the grounding of a cruise ship in Bermuda. Mar Pollut Bull 54: 905-911.
43. Jones, R.J., and Yellowlees, D. (1997) Regulation and control of intracellular algae (equals zooxanthellae) in hard corals. Philos Trans R Soc Lond B Biol Sci 352: 457-468.
44. Kiorboe, T., and Jackson, G.A. (2001) Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol Oceanogr 46: 1309-1318.
45. Knowlton, N., and Rohwer, F. (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162: S51-S62.
46. Koren, O., and Rosenberg, E. (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72: 5254-5259.
47. Larkum, A.W.D., Kennedy, I.R., and Muller, W.J. (1988) Nitrogen-fixation on a coral-reef. Mar Biol 98: 143-155.
48. Leichter, J.J., Stewart, H.L., and Miller, S.L. (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48: 1394-1407.
49. Linley, E.A.S., and Koop, K. (1986) Significance of pelagic bacteria as a trophic resource in a coral-reef lagoon, one tree island, great-barrier-reef. Mar Biol 92: 457-464.
50. Long, R.A., and Azam, F. (2001) Microscale patchiness of bacterioplankton assemblage richness in seawater. Aquat Microb Ecol 26: 103-113.
51. Looney, E.E., Sutherland, K.P., and Lipp, E.K. (2010) Effects of temperature, nutrients, organic matter and coral mucus on the survival of the coral pathogen, Serratia marcescens PDL100. Environ Microbiol 12: 2479-2485.
52. Mao-Jones, J., Ritchie, K.B., Jones, L.E., and Ellner, S.P. (2010) how microbial community composition regulates coral disease development. PLoS Biol 8: e1000345.
53. Mayer, F.W., and Wild, C. (2010) Coral mucus release and following particle trapping contribute to rapid nutrient recycling in a Northern Red Sea fringing reef. Mar Freshw Res 61: 1006-1014.
54. Miyajima, T., Suzumura, M., Umezawa, Y., and Koike, I. (2001) Microbiological nitrogen transformation in carbonate sediments of a coral-reef lagoon and associated seagrass beds. Mar Ecol Prog Ser 217: 273-286.
55. Mouchka, M.E., Hewson, I., and Harvell, C.D. (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662-674.
56. Mueller, R.S., McDougald, D., Cusumano, D., Sodhi, N., Kjelleberg, S., Azam, F., etal. (2007) Vibrio cholerae strains possess multiple strategies for abiotic and biotic surface colonization. J Bacteriol 189: 5348-5360.
57. Naumann, M.S., Richter, C., el-Zibdah, M., and 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: 65-76.
58. Naumann, M.S., Haas, A., Struck, U., Mayr, C., El-Zibdah, M., and Wild, C. (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29: 649-659.
59. Negri, A.P., Smith, L.D., Webster, N.S., and Heyward, A.J. (2002) Understanding ship-grounding impacts on a coral reef: potential effects of anti-foulant paint contamination on coral recruitment. Mar Pollut Bull 44: 111-117.
60. Nelson, C.E., Alldredge, A.L., McCliment, E.A., Amaral-Zettler, L.A., and Carlson, C.A. (2011) Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem. ISME J 5: 1-14.
61. Nogales, B., Lanfranconi, M.P., Pina-Villalonga, J.M., and Bosch, R. (2011) Anthropogenic perturbations in marine microbial communities. FEMS Microbiol Rev 35: 275-298.
62. de O Santos, E., Alves, J.N., Dias, G.M., Mazotto, A.M., Vermelho, A., Vora, G.J., etal. (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J 5: 1-13.
63. Olson, N.D., Ainsworth, T.D., Gates, R.D., and Takabayashi, M. (2009) Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J Exp Mar Bio Ecol 371: 140-146.
64. Patten, N.L., Seymour, J.R., and Mitchell, J.G. (2006) Flow cytometric analysis of virus-like particles and heterotrophic bacteria within coral-associated reef water. J Mar Biolog Assoc UK 86: 563-566.
65. Patten, N.L., Mitchell, J.G., Middelboe, M., Eyre, B.D., Seuront, L., Harrison, P.L., etal. (2008) Bacterial and viral dynamics during a mass coral spawning period on the Great Barrier Reef. Aquat Microb Ecol 50: 209-220.
66. Paul, J.H., Deflaun, M.F., and Jeffrey, W.H. (1986) Elevated levels of microbial activity in the coral surface microlayer. Mar Ecol Prog Ser 33: 29-40.
67. Petry, R., Schmitt, M., and Popp, J. (2003) Raman spectroscopy - a prospective tool in the life sciences. Chemphyschem 4: 14-30.
68. Pringault, O., Duran, R., Jacquet, S., and Torreton, J.P. (2008) Temporal variations of microbial activity and diversity in marine tropical sediments (New Caledonia lagoon). Microb Ecol 55: 247-258.
69. Rasheed, M., Wild, C., Franke, U., and Huettel, M. (2004) Benthic photosynthesis and oxygen consumption in permeable carbonate sediments at Heron Island, Great Barrier Reef, Australia. Estuar Coast Shelf Sci 59: 139-150.
70. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I., and Rosenberg, E. (2006) The coral probiotic hypothesis. Environ Microbiol 8: 2068-2073.
71. Ritchie, K.B. (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14.
72. Rochelle-Newall, E.J., Torreton, J.P., Mari, X., and Pringault, O. (2008) Phytoplankton-bacterioplankton coupling in a subtropical South Pacific coral reef lagoon. Aquat Microb Ecol 50: 221-229.
73. Rohwer, F., Breitbart, M., Jara, J., Azam, F., and Knowlton, N. (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20: 85-91.
74. Rosenberg, E., Koren, O., Reshef, L., Efrony, R., and Zilber-Rosenberg, I. (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5: 355-362.
75. Rusch, A., Hannides, A.K., and Gaidos, E. (2009) Diverse communities of active Bacteria and Archaea along oxygen gradients in coral reef sediments. Coral Reefs 28: 15-26.
76. Rypien, K.L., Ward, J.R., and Azam, F. (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12: 28-39.
77. Seymour, J.R., Mitchell, J.G., Pearson, L., and Waters, R.L. (2000) Heterogeneity in bacterioplankton abundance from 4.5 millimetre resolution sampling. Aquat Microb Ecol 22: 143-153.
78. Seymour, J.R., Patten, N., Bourne, D.G., and Mitchell, J.G. (2005) Spatial dynamics of virus-like particles and heterotrophic bacteria within a shallow coral reef system. Mar Ecol Prog Ser 288: 1-8.
79. Sharp, K.H., Ritchie, K.B., Schupp, P.J., Ritson-Williams, R., and Paul, V.J. (2010) Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS ONE 5: e10898.
80. Shashar, N., Cohen, Y., Loya, Y., and Sar, N. (1994) Nitrogen-fixation (acetylene-reduction) in stony corals - evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111: 259-264.
81. Siboni, N., Ben-Dov, E., Sivan, A., and 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.
82. Smith, L.D., Negri, A.P., Philipp, E., Webster, N.S., and Heyward, A.J. (2003) The effects of antifoulant-paint-contaminated sediments on coral recruits and branchlets. Marine Biology 143: 651-657.
83. Smriga, S. (2010) Ecological significance of bacteria associated with coral reef fish feces. PhD thesis. San Diego, USA: University of California.
84. Smriga, S., Sandin, S.A., and Azam, F. (2010) Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol Ecol 73: 31-42.
85. Sorokin, Y.I. (1973a) Trophical role of bacteria in ecosystem of coral reef. Nature 242: 415-417.
86. Sorokin, Y.I. (1973b) On the feeding of some scleractinian corals with bacteria and dissolved organic matter. Limnol Oceanogr 18: 380-385.
87. Sorokin, Y.I. (1978) Microbial-production in coral-reef community. Archiv Fur Hydrobiologie 83: 281-323.
88. Stanic, D., Oehrle, S., Gantar, M., and Richardson, L.L. (2011) Microcystin production and ecological physiology of Caribbean black band disease cyanobacteria. Environ Microbiol 13: 900-910.
89. Tanaka, Y., Ogawa, H., and Miyajima, T. (2011) Bacterial decomposition of coral mucus as evaluated by long-term and quantitative observation. Coral Reefs 30: 443-449.
90. Torreton, J.P., and Dufour, P. (1996a) Bacterioplankton production determined by DNA synthesis, protein synthesis, and frequency of dividing cells Tuamotu atoll lagoons and surrounding ocean. Microb Ecol 32: 185-202.
91. Torreton, J.P., and Dufour, P. (1996b) Temporal and spatial stability of bacterioplankton biomass and productivity in an atoll lagoon. Aquat Microb Ecol 11: 251-261.
92. Torreton, J.P., Talbot, V., and Garcia, N. (2000) Nutrient stimulation of bacterioplankton growth in Tuamotu atoll lagoons. Aquat Microb Ecol 21: 125-137.
93. Torreton, J.P., Pages, J., and Talbot, V. (2002) Relationships between bacterioplankton and phytoplankton biomass, production and turnover rate in Tuamotu atoll lagoons. Aquat Microb Ecol 28: 267-277.
94. Torreton, J.P., Rochelle-Newall, E., Pringault, O., Jacquet, S., Faure, V., and Briand, E. (2010) Variability of primary and bacterial production in a coral reef lagoon (New Caledonia). Mar Pollut Bull 61: 335-348.
95. Tremblay, P., Weinbauer, M.G., Rottier, C., Guerardel, Y., Nozais, C., and Ferrier-Pages, C. (2011) Mucus composition and bacterial communities associated with the tissue and skeleton of three scleractinian corals maintained under culture conditions. J Mar Biolog Assoc UK 91: 649-657.
96. Vacelet, E., and Thomassin, B.A. (1991) Microbial utilization of coral mucus in long-term insitu incubation over a coral-reef. Hydrobiologia 211: 19-32.
97. Wagner, M. (2009) Single-cell ecophysiology of microbes as revealed by raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 63: 411-429.
98. Werner, U., Bird, P., Wild, C., Ferdelman, T., Polerecky, L., Eickert, G., etal. (2006) Spatial patterns of aerobic and anaerobic mineralization rates and oxygen penetration dynamics in coral reef sediments. Mar Ecol Prog Ser 309: 93-105.
99. Wild, C., Huettel, M., Klueter, A., Kremb, S.G., Rasheed, M.Y.M., and Jorgensen, B.B. (2004a) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428: 66-70.
100. Wild, C., Rasheed, M., Werner, U., Franke, U., Johnstone, R., and Huettel, M. (2004b) Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267: 159-171.
101. Wild, C., Woyt, H., and Huettel, M. (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287: 87-98.
102. Wild, C., Laforsch, C., and Huettel, M. (2006) Detection and enumeration of microbial cells within highly porous calcareous reef sands. Mar Freshw Res 57: 415-420.
103. Wild, C., Jantzen, C., Struck, U., Hoegh-Guldberg, O., and Huettel, M. (2008) Biogeochemical responses following coral mass spawning on the Great Barrier Reef: pelagic-benthic coupling. Coral Reefs 27: 123-132.
104. Wild, C., Niggl, W., Naumann, M.S., and Haas, A.F. (2010) Organic matter release by Red Sea coral reef organisms-potential effects on microbial activity and in situ O-2 availability. Mar Ecol Prog Ser 411: 61-71.
105. Wild, C., Hoegh-Guldberg, O., Naumann, M.S., Colombo-Pallotta, M.F., Ateweberhan, M., Fitt, W.K., etal. (2011) Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res 62: 205-215.
106. Yahel, G., Post, A.F., Fabricius, K., Marie, D., Vaulot, D., and Genin, A. (1998) Phytoplankton distribution and grazing near coral reefs. Limnol Oceanogr 43: 551-563.
107. Yahel, G., Zalogin, T., Yahel, R., and Genin, A. (2006) Phytoplankton grazing by epi- and infauna inhabiting exposed rocks in coral reefs. Coral Reefs 25: 153-163.
108. Yahel, R., Yahel, G., and Genin, A. (2002) Daily cycles of suspended sand at coral reefs: a biological control. Limnol Oceanogr 47: 1071-1083.
109. Yoshinaga, I., Fukami, K., and Ishida, Y. (1991) Comparison of dna and protein-synthesis rates of bacterial assemblages between coral-reef waters and pelagic waters in tropical ocean. Mar Ecol Prog Ser 76: 167-174.