Integrated approach to understanding the onset and pathogenesis of black band disease in corals

Environmental Microbiology

Volumn 18, Issue 3, 2016, Pages 752-765

  Sato, Yui ^a   Civiello, Michael ^b   Bell, Sara C ^a   Willis, Bette L ^b   Bourne, David G ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANTHOZOA; CORAL REEF; CYANOBACTERIUM; ECOSYSTEM; MICROBIAL CONSORTIUM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTHOZOA; CORAL REEFS; CYANOBACTERIA; ECOSYSTEM; MICROBIAL CONSORTIA;

EID: 84961166669     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13122     Document Type: Short Survey

References (112)

1. Abed, R.M.M., Golubic, S., Garcia-Pichel, F., Camoin, G.F., and Sprachta, S. (2003) Characterization of microbialite-forming cyanobacteria in a tropical lagoon: Tikehau Atoll, Tuamotu, French Polynesia. J Phycol 39: 862-873.
2. Aeby, G.S., and Santavy, D.L. (2006) Factors affecting susceptibility of the coral Montastraea faveolata to black-band disease. Mar Ecol Prog Ser 318: 103-110.
3. Al-Moghrabi, S.M. (2001) Unusual black band disease (BBD) outbreak in the northern tip of the Gulf of Aqaba (Jordan). Coral Reefs 19: 330-331.
4. Anderson, R.M., and May, R.M. (1991) Infectious Diseases of Humans: Dynamics and Control. Oxford, UK: Oxford University Press.
5. Antonius, A. (1976) New observations on coral destruction in reefs. Proceeding of the 10th Meeting of the Association of Island Marine Laboratories of the Caribbean, University of Puerto Rico, Mayagüez, September 4-7 1973 10: 17.
6. Antonius, A. (1981) The 'band' diseases in coral reefs. Proc 4th Int Coral Reef Symp 2: 7-14.
7. Antonius, A. (1985) Black band disease infection experiments on hexacorals and octocorals. Proc fifth Int Coral Reef Cong 6: 155-160.
8. Antonius, A., and Riegl, B. (1998) Coral diseases and Drupella cornus invasion in the Red Sea. Coral Reefs 17: 48.
9. Bakaletz, L.O. (2004) Developing animal models for polymicrobial diseases. Nat Rev Microbiol 2: 552-568.
10. Belda-Ferre, P., Alcaraz, L.D., Cabrera-Rubio, R., Romero, H., Simon-Soro, A., Pignatelli, M., and Mira, A. (2012) The oral metagenome in health and disease. ISME J 6: 46-56.
11. Borger, J.L. (2005) Scleractinian coral diseases in south Florida: incidence, species susceptibility, and mortality. Dis Aquat Org 67: 249-258.
12. 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.
13. 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.
14. Bourne, D.G., van der Zee, M.J.J., Botté, E.S., and Sato, Y. (2013) Sulfur-oxidizing bacterial populations within cyanobacterial dominated coral disease lesions. Environ Microbiol Rep 5: 518-524.
15. Boyett, H.V., Bourne, D.G., and Willis, B.L. (2007) Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef. Mar Biol 151: 1711-1720.
16. Brodsky, I.E., and Medzhitov, R. (2009) Targeting of immune signalling networks by bacterial pathogens. Nat Cell Biol 11: 521-526.
17. Brogden, K.A., Guthmiller, J.M., and Taylor, C.E. (2005) Human polymicrobial infections. Lancet 365: 253-255.
18. Brownell, A.C., and Richardson, L.L. (2014) Sulfate reducing bacteria as secondary and necessary pathogens in black band disease of corals. Rev Biol Trop 62: 1-9.
19. Bruckner, A.W., and Bruckner, R.J. (1997) The persistence of black-band disease in Jamaica: impact on community structure. Proc 8th Int Coral Reef Symp 1: 601-606.
20. Bruckner, A.W., Bruckner, R.J., and Williams, E.H. (1997) Spread of a black-band disease epizootic through the coral reef system in St Ann's Bay, Jamaica. Bull Mar Sci 61: 919-928.
21. Campbell, B.J., Engel, A.S., Porter, M.L., and Takai, K. (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468.
22. Canfield, D.E., and Des Marais, D.J. (1993) Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim Cosmochim Acta 57: 3971-3984.
23. Carlton, R.G., and Richardson, L.L. (1995) Oxygen and sulfide dynamics in a horizontally migrating cyanobacterial mat - black band disease of corals. FEMS Microbiol Ecol 18: 155-162.
24. Carpenter, K.E., Abrar, M., Aeby, G., Aronson, R.B., Banks, S., Bruckner, A., etal. (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321: 560-563.
25. Cavicchioli, R., Curmi, P.M.G., Saunders, N., and Thomas, T. (2003) Pathogenic archaea: do they exist? Bioessays 25: 1119-1128.
26. Charpy, L., Alliod, R., Rodier, M., and Golubic, S. (2007) Benthic nitrogen fixation in the SW New Caledonia lagoon. Aquat Microb Ecol 47: 73-81.
27. Chong-Seng, K.M., Cole, A.J., Pratchett, M.S., and Willis, B.L. (2011) Selective feeding by coral reef fishes on coral lesions associated with brown band and black band disease. Coral Reefs 30: 473-481.
28. Croquer, A., and Weil, E. (2009) Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. II. Genera-level analysis. Dis Aquat Org 83: 209-222.
29. De'ath, G., Fabricius, K.E., Sweatman, H., and Puotinen, M. (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109: 17995-17999.
30. Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S., and Visscher, P.T. (2009) Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev 96: 141-162.
31. Edmunds, P.J. (1991) Extent and effect of black band disease on a Caribbean reef. Coral Reefs 10: 161-165.
32. Fraser, C., Riley, S., Anderson, R.M., and Ferguson, N.M. (2004) Factors that make an infectious disease outbreak controllable. Proc Natl Acad Sci USA 101: 6146-6151.
33. Frias-Lopez, J., Klaus, J.S., Bonheyo, G.T., and Fouke, B.W. (2004) Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70: 5955-5962.
34. Garren, M., and Azam, F. (2012) Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment. ISME J 6: 1159-1165.
35. 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.
36. Garrett, P., and Ducklow, H. (1975) Coral diseases in Bermuda. Nature 253: 349-350.
37. Glas, M.S., Motti, C.A., Negri, A., Sato, Y., Froscio, S., Humpage, A.R., etal. (2010) Cyanotoxins are not implicated in the etiology of coral black band disease outbreaks on Pelorus Island, Great Barrier Reef. FEMS Microbiol Ecol 73: 43-54.
38. Glas, M.S., Sato, Y., Ulstrup, K.E., and Bourne, D.G. (2012) Biogeochemical conditions determine virulence of black band disease in corals. ISME J 6: 1526-1534.
39. Goreau, T.J., Cervino, J., Goreau, M., Hayes, R., Hayes, M., Richardson, L., etal. (1998) Rapid spread of diseases in Caribbean coral reefs. Rev Biol Trop 46: 157-171.
40. Green, E.P., and Bruckner, A.W. (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96: 347-361.
41. Greene, A.C., Patel, B.K.C., and Sheehy, A.J. (1997) Deferribacter thermophilus gen nov, sp nov, a novel thermophilic manganese- and iron-reducing bacterium isolated from a petroleum reservoir. Int J Syst Bacteriol 47: 505-509.
42. Haapkylä, J., Unsworth, R.K.F., Flavell, M., Bourne, D.G., Schaffelke, B., and Willis, B.L. (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS ONE 6: e16893.
43. Hansen, J., Sato, M., Ruedy, R., Lo, K., Lea, D.W., and Medina-Elizade, M. (2006) Global temperature change. Proc Natl Acad Sci USA 103: 14288-14293.
44. Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., etal. (1999) Review: marine ecology - emerging marine diseases - climate links and anthropogenic factors. Science 285: 1505-1510.
45. Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S., and Samuel, M.D. (2002) Ecology - climate warming and disease risks for terrestrial and marine biota. Science 296: 2158-2162.
46. Harvell, D., Altizer, S., Cattadori, I.M., Harrington, L., and Weil, E. (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90: 912-920.
47. Hoegh-Guldberg, O. (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50: 839-866.
48. Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., etal. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
49. Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., etal. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933.
50. IPCC (2014) Climate change 2013: the physical science basis. In The Fifth Assessment Report: Intergovernmental Panel of Climate Change.
51. Jessen, C., Villa Lizcano, J.F., Bayer, T., Roder, C., Aranda, M., Wild, C., and Voolstra, C.R. (2013) In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS ONE 8: e62091.
52. Jonkers, H.M., Ludwig, R., De Wit, R., Pringault, O., Muyzer, G., Niemann, H., etal. (2003) Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: 'La Salada de Chiprana' (NE Spain). FEMS Microbiol Ecol 44: 175-189.
53. Jorgensen, B.B., and Revsbech, N.P. (1983) Colorless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in O2 and H2S microgradients. Appl Environ Microbiol 45: 1261-1270.
54. Kaczmarsky, L.T. (2006) Coral disease dynamics in the central Philippines. Dis Aquat Org 69: 9-21.
55. Kaczmarsky, L.T., Draud, M., and Williams, E.H. (2005) Is there a relationship between proximity to sewage effluent and the prevalence of coral disease? Caribb J Sci 41: 124-137.
56. Katz, S.M., Pollock, F.J., Bourne, D.G., and Willis, B.L. (2014) Crown-of-thorns starfish predation and physical injuries promote brown band disease on corals. Coral Reefs 33: 705-716.
57. Kerr, J.R. (1999) Cell adhesion molecules in the pathogenesis of and host defence against microbial infection. J Clin Pathol 52: 220-230.
58. Knodler, L.A., Celli, J., and Brett Finlay, B. (2001) Pathogenic trickery: deception of host cell processes. Nat Rev Mol Cell Biol 2: 578-588.
59. Kriwy, P., and Uthicke, S. (2011) Microbial diversity in marine biofilms along a water quality gradient on the Great Barrier Reef. Syst Appl Microbiol 34: 116-126.
60. Kuta, K.G., and Richardson, L.L. (1996) Abundance and distribution of black band disease on coral reefs in the northern Florida Keys. Coral Reefs 15: 219-223.
61. Kuta, K.G., and Richardson, L.L. (1997) Black band disease and the fate of diseased coral colonies in the Florida Keys. Proc 8th Int Coral Reef Symp 1: 575-578.
62. Kuta, K.G., and Richardson, L.L. (2002) Ecological aspects of black band disease of corals: relationships between disease incidence and environmental factors. Coral Reefs 21: 393-398.
63. Lafferty, K.D., Porter, J.W., and Ford, S.E. (2004) Are diseases increasing in the ocean? In Annual Review of Ecology, Evolution, and Systematics, pp. 31-54.
64. Miller, A.W., and Richardson, L.L. (2011) A meta-analysis of 16S rRNA gene clone libraries from the polymicrobial black band disease of corals. FEMS Microbiol Ecol 75: 231-241.
65. Miller, A.W., Blackwelder, P., Al-Sayegh, H., and Richardson, L.L. (2011) Fine-structural analysis of black band disease infected coral reveals boring cyanobacteria and novel bacteria. Dis Aquat Org 93: 179-190.
66. Miller, A.W., Blackwelder, P., Al-Sayegh, H., and Richardson, L.L. (2012) Insights into migration and development of coral black band disease based on fine structure analysis. Rev Biol Trop 60: 21-27.
67. Montano, S., Strona, G., Seveso, D., and Galli, P. (2012) First report of coral diseases in the Republic of Maldives. Dis Aquat Org 101: 159-165.
68. Myers, J.L., and Richardson, L.L. (2009) Adaptation of cyanobacteria to the sulfide-rich microenvironment of black band disease of coral. FEMS Microbiol Ecol 67: 242-251.
69. Myhr, S., and Torsvik, T. (2000) Denitrovibrio acetiphilus, a novel genus and species of dissimilatory nitrate-reducing bacterium isolated from an oil reservoir model column. Int J Syst Evol Microbiol 50: 1611-1619.
70. Osborne, K., Dolman, A.M., Burgess, S.C., and Johns, K.A. (2011) Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995-2009). PLoS ONE 6: e17516.
71. Page, C., and Willis, B.L. (2006) Distribution, host range and large-scale spatial variability in black band disease prevalence on the Great Barrier Reef, Australia. Dis Aquat Org 69: 41-51.
72. Pandolfi, J.M., Bradbury, R.H., Sala, E., Hughes, T.P., Bjorndal, K.A., Cooke, R.G., etal. (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301: 955-958.
73. Pandolfi, J.M., Connolly, S.R., Marshall, D.J., and Cohen, A.L. (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422.
74. Peters, E.C. (1984) A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals. Helgol Mar Res 37: 113-137.
75. Pollock, F.J., Lamb, J.B., Field, S.N., Heron, S.F., Schaffelke, B., Shedrawi, G., etal. (2014) Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS ONE 9: e102498.
76. Pomeroy, L.R., and Wiebe, W.J. (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23: 187-204.
77. Pugh, C.E., Hossner, L.R., and Dixon, J.B. (1984) Oxidation rate of iron sulfides as affected by surface area, morphology, oxygen concentration, and autotrophic bacteria. Soil Sci 137: 309-314.
78. Ramos-Flores, T. (1983) Lower marine fungus associated with black line disease in star corals (Montastrea annularis, E. & S.). Biol Bull 165: 429-435.
79. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I., and Rosenberg, E. (2006) The coral probiotic hypothesis. Environ Microbiol 8: 2068-2073.
80. Richardson, L.L. (1996) Horizontal and vertical migration patterns of Phormidium corallyticum and Beggiatoa spp. associated with black-band disease of corals. Microb Ecol 32: 323-335.
81. Richardson, L.L. (1998) Coral diseases: what is really known? Trends Ecol Evol 13: 438-443.
82. Richardson, L.L. (2004) Black band disease. In Coral Health and Disease. Rosenberg, E., and Loya, Y. (eds). Heidelberg: Springer-Verlag, pp. 325-336.
83. Richardson, L.L., and Kuta, K.G. (2003) Ecological physiology of the black band disease cyanobacterium Phormidium corallyticum. FEMS Microbiol Ecol 43: 287-298.
84. Richardson, L.L., Kuta, K.G., Schnell, S., and Carlton, R.G. (1997) Ecology of the black band disease microbial consortium. Proc 8th Int Coral Reef Symp 1: 597-600.
85. Richardson, L.L., Smith, G.W., Ritchie, K.B., and Carlton, R.G. (2001) Integrating microbiological, microsensor, molecular, and physiologic techniques in the study of coral disease pathogenesis. Hydrobiologia 460: 71-89.
86. Richardson, L.L., Miller, A.W., Broderick, E., Kaczmarsky, L., Gantar, M., Stanic, D., and Sekar, R. (2009) Sulfide, microcystin, and the etiology of black band disease. Dis Aquat Org 87: 79-90.
87. Richardson, L.L., Stanić, D., May, A., Brownell, A., Gantar, M., and Campagna, S.R. (2014) Ecology and physiology of the pathogenic cyanobacterium Roseofilum reptotaenium. Life 4: 968-987.
88. Rodriguez, S., and Croquer, A. (2008) Dynamics of black band disease in a Diploria strigosa population subjected to annual upwelling on the northeastern coast of Venezuela. Coral Reefs 27: 381-388.
89. Rosenberg, E., and Ben-Haim, Y. (2002) Microbial diseases of corals and global warming. Environ Microbiol 4: 318-326.
90. 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.
91. Sato, Y., Bourne, D.G., and Willis, B.L. (2009) Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia). Proc R Soc B Biol Sci 276: 2795-2803.
92. Sato, Y., Willis, B.L., and Bourne, D.G. (2010) Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J 4: 203-214.
93. Sato, Y., Bourne, D.G., and Willis, B.L. (2011) Effects of temperature and light on the progression of black band disease of the reef coral, Montipora hispida. Coral Reefs 30: 753-761.
94. Sato, Y., Willis, B.L., and Bourne, D.G. (2013) Pyrosequencing-based profiling of archaeal and bacterial 16S rRNA genes identifies a novel archaeon associated with black band disease in corals. Environ Microbiol 15: 2994-3007.
95. Sibley, C.D., Rabin, H., and Surette, M.G. (2006) Cystic fibrosis: a polymicrobial infectious disease. Future Microbiol 1: 53-61.
96. Sibley, C.D., Duan, K., Fischer, C., Parkins, M.D., Storey, D.G., Rabin, H.R., and Surette, M.G. (2008) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.
97. Sokolow, S. (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87: 5-18.
98. Sussman, M., Bourne, D.G., and Willis, B.L. (2006) A single cyanobacterial ribotype is associated with both red and black bands on diseased corals from Palau. Dis Aquat Org 69: 111-118.
99. Sutherland, K.P., Porter, J.W., and Torres, C. (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266: 273-302.
100. Viehman, S., Mills, D.K., Meichel, G.W., and Richardson, L.L. (2006) Culture and identification of Desulfovibrio spp. from corals infected by black band disease on Dominican and Florida Keys reefs. Dis Aquat Org 69: 119-127.
101. Viehman, T.S., and Richardson, L.L. (2002) Motility patterns of Beggiatoa and Phormidium corallyticum in black band disease. Proc 9th Int Coral Reef Symp 2: 1251-1255.
102. Voss, J.D., and Richardson, L.L. (2006a) Coral diseases near Lee Stocking Island, Bahamas: Patterns and potential drivers. Dis Aquat Org 69: 33-40.
103. Voss, J.D., and Richardson, L.L. (2006b) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25: 569-576.
104. Ward, J.R., and Lafferty, K.D. (2004) The elusive baseline of marine disease: Are diseases in ocean ecosystems increasing? PLoS Biol 2: 542-547.
105. Weber, M., De Beer, D., Lott, C., Polerecky, L., Kohls, K., Abed, R.M.M., etal. (2012) Mechanisms of damage to corals exposed to sedimentation. Proc Natl Acad Sci USA 109: E1558-E1567.
106. Weil, E., Smith, G., and Gil-Agudelo, D.L. (2006) Status and progress in coral reef disease research. Dis Aquat Org 69: 1-7.
107. Weil, E., Irikawa, A., Casareto, B., and Suzuki, Y. (2012) Extended geographic distribution of several Indo-Pacific coral reef diseases. Dis Aquat Org 98: 163-170.
108. Willis, B.L., Page, C.A., and Dinsdale, E.A. (2004) Coral disease on the Great Barrier Reef. In Coral Health and Disease. Rosenberg, E., and Loya, Y. (eds). Heidelberg: Springer-Verlag, pp. 69-104.
109. Witt, V., Wild, C., and Uthickea, S. (2012) Terrestrial runoff controls the bacterial community composition of biofilms along a water quality gradient in the Great Barrier Reef. Appl Environ Microbiol 78: 7786-7791.
110. Wobeser, G.A. (1994) Investigation and Management of Disease in Wild Animals. New York, NY, USA: Plenum Press, p. 265.
111. Wobeser, G.A. (2006) Essentials of Disease in Wild Animals. Ames, IA, USA: Blackwell Publishing, p. 243.
112. Zvuloni, A., Artzy-Randrup, Y., Stone, L., Kramarsky-Winter, E., Barkan, R., and Loya, Y. (2009) Spatio-temporal transmission patterns of black-band disease in a coral community. PLoS ONE 4: e4993.