Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems

Annual Review of Microbiology

Volumn 70, Issue , 2016, Pages 317-340

  Bourne, David G ^a,b   Morrow, Kathleen M ^b,c   Webster, Nicole S ^b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

Coral holobiont; Coral hologenome; Coral microbiome; Cumulative stressors; Holobiont resilience

Indexed keywords

CARBON; GLYCOSAMINOGLYCAN; NITROGEN; PHOSPHORUS; SULFUR;

ACIDIFICATION; ARCHAEON; ARTICLE; CARBON CYCLING; CILIATE; CORAL REEF; ECOSYSTEM RESILIENCE; ENVIRONMENTAL HEALTH; FUNGUS; MARINE ENVIRONMENT; MICROBIAL COMMUNITY; MICROBIOME; MICROHABITAT; NITROGEN CYCLING; NONHUMAN; NUTRIENT CYCLING; PRIORITY JOURNAL; SEDIMENTATION; SPECIES DIFFERENCE; SYMBIODINIUM; SYMBIOSIS; TEMPERATURE STRESS; VIRUS LIKE AGENT; ANIMAL; ANTHOZOA; BACTERIUM; CLASSIFICATION; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

ANIMALS; ANTHOZOA; BACTERIA; CORAL REEFS; ECOSYSTEM; FUNGI; MICROBIOTA;

EID: 84986626338     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-102215-095440     Document Type: Article

References (157)

1. Agostini S, Suzuki Y, Higuchi T, Casareto B, Yoshinaga K, et al. 2012. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31:147-56
2. AinsworthTD, Krause L, Bridge T, TordaG,Raina J-B, et al. 2015. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9:2261-74. doi:10.1038/ismej.2015.39
3. Ainsworth TD, Thurber RV, Gates RD. 2010. The future of coral reefs: a microbial perspective. Trends Ecol. Evol. 25:233-40
4. Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, et al. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98-101
5. Apprill A, Marlow HQ, Martindale MQ, Rappe MS. 2009. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 3:685-99
6. Baird AH, Bhagooli R, Ralph PJ, Takahashi S. 2009. Coral bleaching: the role of the host. Trends Ecol. Evol. 24:16-20
7. Barott KL, Rodriguez-Mueller B, Youle M, Marhaver KL, Vermeij MJA, et al. 2012. Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc. R. Soc. B 279:1655-64
8. Barott KL, Rohwer FL. 2012. Unseen players shape benthic competition on coral reefs. TrendsMicrobiol. 20:621-28
9. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, et al. 2013. Bacteriophage adhering tomucus provide a non-host-derived immunity. PNAS 110:10771-76
10. Bayer T, Arif C, Ferrier-Pages C, Zoccola D, Aranda M, Voolstra CR. 2013. Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar. Ecol. Prog. Ser. 479:75-84
11. Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK, et al. 2013. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79:4759-62
12. Beinart RA, Nyholm SV, Dubilier N, Girguis PR. 2014. Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-proteobacterial symbionts. Environ. Microbiol. Rep. 6:656-64
13. Bell JJ, Davy SK, Jones T, Taylor MW,Webster NS. 2013. Could some coral reefs become sponge reefs as our climate changes? Glob. Change Biol. 19:2613-24
14. Bentis CJ, Kaufman L, Golubic S. 2000. Endolithic fungi in reef-building corals (order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol. Bull. 198:254-60
15. Blackall LL, Wilson B, Oppen MJH. 2015. Coral\-The world's most diverse symbiotic ecosystem. Mol. Ecol. 24:5330-47
16. Bordenstein SR, Theis KR. 2015. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLOS Biol. 13:e1002226
17. Bourne D, Iida Y, Uthicke S, Smith-Keune C. 2008. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2:350-63
18. Brown BE. 1997. Coral bleaching: causes and consequences. Coral Reefs 16:129-38
19. Brown BE, Bythell JC. 2005. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 296:291-309
20. Brune A, Dietrich C. 2015. The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu. Rev. Microbiol. 69:145-66
21. Bythell JC, Wild C. 2011. Biology and ecology of coral mucus release. J. Exp. Mar. Biol. Ecol. 408:88-93
22. Cardini U, Bednarz VN, Naumann MS, van Hoytema N, Rix L, et al. 2015. Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc. R. Soc. Lond. Ser. B 282:20152257
23. Ceh J, KilburnMR, Cliff JB, Raina J-B, KeulenM, Bourne DG. 2013. Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol. Evol. 3:2393-400
24. Correa AMS,Welsh RM, Thurber RLV. 2013. Unique nucleocytoplasmic dsDNA and +ssRNA viruses are associated with the dinoflagellate endosymbionts of corals. ISME J. 7:13-27
25. Cumbo VR, Baird AH, Moore RB, Negri AP, Neilan BA, et al. 2013. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist 164:237-44
26. Davy SK, Allemand D, Weiss VM. 2012. Cell-biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:229-61
27. Day T, Bonduriansky R. 2011. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178:E18-36
28. De'ath G, Fabricius KE, Sweatman H, Puotinen M. 2012. The 27-year decline of coral cover on the Great Barrier Reef and its causes. PNAS 109:17995-99
29. Decelle J. 2013. New perspectives on the functioning and evolution of photosymbiosis in plankton: mutualism or parasitism? Commun. Integr. Biol. 6:e24560
30. Deschaseaux ESM, Jones GB,Deseo MA, Shepherd KM, Kiene RP, et al. 2014. Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol. Oceanogr. 59:758-68
31. Dias BG, Ressler KJ. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17:89-96
32. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, et al. 2008. Functional metagenomic profiling of nine biomes. Nature 452:629-32
33. Dinsdale EA, Rohwer F. 2011. Fish or germs? Microbial dynamics associated with changing trophic structures on coral reefs. In Coral Reefs: An Ecosystem in Transition, ed. Z Dubinsky,NStambler, pp. 231-40. Dordrecht, Neth.: Springer
34. Durham BP, Sharma S, Luo H, Smith CB, Amin SA, et al. 2015. Cryptic carbon and sulfur cycling between surface ocean plankton. PNAS 112:453-57
35. Dyhrman ST, Benitez-Nelson CR, Orchard ED, Haley ST, Pellechia PJ. 2009. A microbial source of phosphonates in oligotrophic marine systems. Nat. Geosci. 2:696-99
36. Fabricius KE. 2011. Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. In Coral Reefs: An Ecosystem in Transition, ed. Z Dubinsky, N Stambler, pp. 493-505. Dordrecht, Neth.: Springer
37. Falkowski PG, Dubinsky Z, Muscatine L,McCloskey LR. 1993. Population control in symbiotic corals. Bioscience 43:453-64
38. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW. 1984. Light and the bioenergetics of a symbiotic coral. Bioscience 34:705-9
39. Fan L, Liu M, Simister R, Webster NS, Thomas T. 2013. Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J. 7:991-1002
40. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, et al. 2012. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. PNAS 109:E1878-87
41. Ferrier-Pages C, Houlbreque F, Wyse E, Richard C, Allemand D, Boisson F. 2005. Bioaccumulation of zinc in the scleractinian coral Stylophora pistillata. Coral Reefs 24:636-45
42. Fine M, Loya Y. 2002. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. R. Soc. Lond. B 269:1205-10
43. Fiore CL, Jarett JK, Olson ND, Lesser MP. 2010. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 18:455-63
44. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, et al. 2009. Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J. Exp. Mar. Biol. Ecol. 373:102-10
45. Fraune S, Bosch TCG. 2010. Why bacteria matter in animal development and evolution. BioEssays 32:571-80
46. Garren M, Azam F. 2012. Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment. ISME J. 6:1159-65
47. GarrenM, Son K, Raina J-B, Rusconi R, Menolascina F, et al. 2014. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J. 8:999-1007
48. Gilbert JA, Thomas S, Cooley NA, Kulakova A, Field D, et al. 2009. Potential for phosphonoacetate utilization by marine bacteria in temperate coastal waters. Environ. Microbiol. 11:111-25
49. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, et al. 2005. Evolutionary innovation: a bone-eating marine symbiosis. Environ. Microbiol. 7:1369-78
50. Golubic S, Radtke G, Le Campion-Alsumard T. 2005. Endolithic fungi in marine ecosystems. Trends Microbiol. 13:229-35
51. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, et al. 2012. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLOS ONE 7:e33353
52. Haas AF, Fairoz MFM, Kelly LW,Nelson CE, Dinsdae EA, et al. 2016. Globalmicrobialization of coral reefs. Nat. Microbiol. 1:16042
53. Haas AF, Nelson CE, Rohwer F, Wegley-Kelly L, Quistad SD, et al. 2013. Influence of coral and algal exudates on microbially mediated reef metabolism. PeerJ. 1:e108
54. Herndl GJ, Velimirov B. 1986. Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora cespitosa. Mar. Biol. 90:363-69
55. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-42
56. Hong M-J, Yu Y-T, Chen CA, Chiang P-W, Tang S-L. 2009. Influence of species specificity and other factors on bacteria associated with the coral Stylophora pistillata in Taiwan. Appl. Environ. Microbiol. 75:7797-806
57. Janouskovec J, Horak A, Barott KL, Rohwer FL, Keeling PJ. 2012. Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr. Biol. 22:R518-19
58. Jin P, Gao K, Beardall J. 2013. Evolutionary responses of a coccolithophorid Gephyrocapsa oceanica to ocean acidification. Evolution 67:1869-78
59. Katz SM, Pollock FJ, Bourne DG, Willis BL. 2014. Crown-of-thorns starfish predation and physical injuries promote brown band disease on corals. Coral Reefs 33:705-16
60. Kelly LW,Williams GJ, Barott KL, Carlson CA, Dinsdale EA, et al. 2014. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. PNAS 111:10227-32
61. Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ. 2010. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellowband diseased colonies. Environ. Microbiol. 12:541-56
62. Kline DI, KuntzNM, BreitbartM, KnowltonN, Rohwer F. 2006. Role of elevated organic carbon levels and microbial activity in coral mortality. Mar. Ecol. Prog. Ser. 314:119-25
63. Knowlton N, Jackson JBC. 2001. The ecology of coral reefs. In Marine Community Ecology, ed. MD Bertness, SD Gaines, ME Hay, pp. 395-422. Sunderland, MA: Sinauer Assoc.
64. Krediet CJ, Ritchie KB, Alagely A, Teplitski M. 2013. Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J. 7:980-90
65. Kvennefors ECE, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC. 2008. An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev. Comp. Immunol. 32:1582-92
66. Kvennefors ECE, LeggatW, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, Barnes AC. 2010. Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev. Comp. Immunol. 34:1219-29
67. Lema KA, Bourne DG, Willis BL. 2014. Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora. Mol. Ecol. 23:4682-95
68. Lema KA, Clode PL, Kilburn MR, Thornton R, Willis BL, Bourne DG. 2016. Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora. ISME J. 10:1804-8
69. Lema KA,Willis BL, Bourne DG. 2012. Corals form characteristic associations with symbiotic nitrogenfixing bacteria. Appl. Environ. Microbiol. 78:3136-44
70. Lesser MP, Falcon LI, Rodriguez-Roman A, Enriquez S, Hoegh-Guldberg O, Iglesias-Prieto R. 2007. Nitrogen fixation by symbiotic cyanobactieria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 347:143-52
71. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG. 2004. Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997-1000
72. Littman R, Willis BL, Bourne DG. 2011. Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ. Microbiol. Rep. 3:651-60
73. Littman RA,Willis BL, Pfeffer C, Bourne DG. 2009. Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol. Ecol. 68:152-63
74. Liu J, Weinbauer MG, Maier C, Dai M, Gattuso J-P. 2010. Effect of ocean acidification on microbial diversity and onmicrobe-driven biogeochemistry and ecosystem functioning. Aquat. Microb. Ecol. 61:291-305
75. Lobban CS, Raymundo LM, Montagnes DJS. 2011. Porpostoma guamensis n. sp., a philasterine scuticociliate associated with brown-band disease of corals. J. Eukaryot. Microbiol. 58:103-13
76. Magurran AE, Henderson PA. 2003. Explaining the excess of rare species in natural species abundance distributions. Nature 422:714-16
77. Marhaver KL, Edwards RA, Rohwer F. 2008. Viral communities associated with healthy and bleaching corals. Environ. Microbiol. 10:2277-86
78. McDole T, Nulton J, Barott KL, Felts B, Hand C, et al. 2012. Assessing coral reefs on a Pacific-wide scale using the microbialization score. PLOS ONE 7:e43233
79. McFall-Ngai M. 2014. Divining the essence of symbiosis: insights from the squid-Vibrio model. PLOS Biol. 12:e1001783
80. Meron D, Atias E, Iasur Kruh L, Elifantz H, Minz D, et al. 2011. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5:51-60
81. Moberg F, Folke C. 1999. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29:215-33
82. Moore RB, Obornik M, Janouskovec J, Chrudimsky T, Vancovva M, et al. 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959-63
83. Moran NA, Sloan DB. 2015. The hologenome concept: helpful or hollow? PLOS Biol. 13:e1002311
84. Morrow KM, Bourne DG, Humphrey C, Botte ES, Laffy P, et al. 2014. Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 9:894-908
85. Morrow KM, Ritson-Williams R, Ross C, LilesMR, Paul VJ. 2012. Macroalgal extracts induce bacterial assemblage shifts and sublethal tissue stress in Caribbean corals. PLOS ONE 7:e44859
86. MouchkaME, Hewson I, Harvell CD. 2010. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 50:662-74
87. Muscatine L, Porter JW. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454-60
88. Muyzer G, Stams AJM. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6:441-54
89. Neave M, Rachmawati R, Xun L, Michell C, Bourne DG, et al. 2016. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. In press. doi:10.1038/ismej.2016.95
90. Neave MJ, Michell CT, Apprill A, Voolstra CR. 2014. Whole-genome sequences of three symbiotic endozoicomonas strains. Genome Announc. 2:e00802-14
91. Nelson CE,Goldberg SJ, Kelly LW,Haas AF, Smith JE, et al. 2013. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 7:962-79
92. Nguyen MTHD, Liu M, Thomas T. 2014. Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol. Ecol. 23:1635-45
93. Nyholm SV, McFall-Ngai M. 2004. The winnowing: establishing the squid-Vibrio symbiosis. Nat. Rev. Microbiol. 2:632-42
94. O'Brien PA, Morrow KM, Willis BL, Bourne DG. 2016. Implications of ocean acidification for marine microorganisms from the free-living to the host-associated. Front. Mar. Sci. 3:47
95. Page CA, Willis BL. 2008. Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease. Coral Reefs 27:257-72
96. Palardy JE, Rodrigues LJ, Grottoli AG. 2008. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J. Exp. Mar. Biol. Ecol. 367:180-88
97. Pernice M, Levy O. 2014. Novel tools integrating metabolic and gene function to study the impact of the environment on coral symbiosis. Front. Microbiol. 5:448
98. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, et al. 2012. A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J. 6:1314-24
99. Peters EC. 1984. A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals. Helgol. Meeresunters. 37:113-37
100. Phillips NW. 1984. Role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bull. Mar. Sci. 35:283-98
101. Piggot AM, Fouke BW, Sivaguru M, Sanford RA, Gaskins HR. 2009. Change in zooxanthellae and mucocyte tissue density as an adaptive response to environmental stress by the coral, Montastraea annularis. Mar. Biol. 156:2379-89
102. Pinzon JH, Kamel B, Burge CA, Harvell CD, Medina M, et al. 2015. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2:140214
103. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J. 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phylogenet. Evol. 38:20-30
104. Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, et al. 2014. Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLOS ONE 9:e102498
105. Radecker N, Pogoreutz C, Voolstra CR,Wiedenmann J,Wild C. 2015. Nitrogen cycling in corals: the key to understanding holobiont functioning? TrendsMicrobiol. 23:490-97. doi:10.1016/j.tim.2015.03.008
106. Raina J-B, Dinsdale E, Willis BL, Bourne DG. 2010. Do organic sulphur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 18:101-8
107. Raina J-B, Tapiolas DM, Foret S, Lutz A, Abrego D, et al. 2013. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502:677-80
108. Raina J-B, Tapiolas DM, Motti CA, Foret S, Seemann T, et al. 2016. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals. PeerJ. In press
109. Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME. 2011. Macroalgal terpenes function as allelopathic agents against reef corals. PNAS 108:17726-31
110. Ravindran J, Kannapiran E, Manikandan B, Francis K, Arora S, et al. 2013. UV-absorbing bacteria in coral mucus and their response to simulated temperature elevations. Coral Reefs 32:1043-50
111. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:2068-73
112. Ritchie KB. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322:1-14
113. Rohwer F, Seguritan V, Azam F, Knowlton N. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10
114. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. 5:355-62
115. Sandin SA, Walsh SM, Jackson JBC. 2010. Prey release, trophic cascades, and phase shifts in tropical nearshore ecosystems. In Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, ed. J Terborgh, JA Estes, pp. 71-90. Washington: Island Press
116. Sato Y, Civiello M, Bell SC, Willis BL, Bourne DG. 2015. Integrated approach to understanding the onset and pathogenesis of black band disease in corals. Environ. Microbiol. 18:752-65
117. Seymour JR, Simo R, Ahmed T, Stocker R. 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329:342-45
118. Shade A, Peter H, Allison SD, Baho DL, Berga M, et al. 2012. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3:417
119. Sharp KH, Distel D, Paul VJ. 2012. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 6:790-801
120. Shashar N, Banaszak AT, Lesser MP, Amrami D. 1997. Coral endolithic algae: life in a protected environment. Pac. Sci. 51:167-73
121. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, et al. 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320-23
122. Siboni N, Ben-Dov E, Sivan A, Kushmaro A. 2008. Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ. Microbiol. 10:2979-90
123. Sievert SM, Kiene RP, Schultz-Vogt HN. 2007. The sulfur cycle. Oceanography 20:117-23
124. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, et al. 2006. Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol. Lett. 9:835-45
125. Soffer N, Brandt ME, Correa AMS, Smith TB, Thurber RV. 2014. Potential role of viruses in white plague coral disease. ISME J. 8:271-83
126. Stefels J. 2000. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 43:183-97
127. Sunagawa S, Woodley CM,MedinaM. 2010. Threatened corals provide underexplored microbial habitats. PLOS ONE 5:e9554
128. Sweet MJ, Croquer A, Bythell JC. 2011. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39-52
129. Thurber RV, Willner-Hall D, Rodriguez-Mueller B,Desnues C, Edwards RA, et al. 2009. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11:2148-63
130. Tout J, Jeffries TC, Petrou K, Tyson GW,Webster NS, et al. 2015. Chemotaxis by natural populations of coral reef bacteria. ISME J. 9:1764-77
131. Tremblay P, Grover R, Maguer J-F, Hoogenboom M, Ferrier-Pages C. 2014. Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata. Coral Reefs 33:1-13
132. Ursell LK, Metcalf JL, Parfrey LW, Knight R. 2012. Defining the human microbiome. Nutr. Rev. 70:S38-44
133. Van Alstyne KL, Schupp P, Slattery M. 2006. The distribution of dimethylsulfoniopropionate in tropical Pacific coral reef invertebrates. Coral Reefs 25:321-27
134. vanOppenMJH, Leong J-A, Gates RD. 2009. Coral-virus interactions: a double-edged sword? Symbiosis 47:1-8
135. Vega Thurber RLV, Barott KL, Hall D, LiuH, Rodriguez-Mueller B, et al. 2008. Metagenomic analysis indicates that stressors induce production of herpeslike viruses in the coral Porites compressa. PNAS 105:18413-18
136. Voolstra CR,Miller DJ, RaganMA, Hoffmann AA, Hoegh-Guldberg O, et al. 2015. The ReFuGe 2020 Consortium-using "omics" approaches to explore the adaptability and resilience of coral holobionts to environmental change. Front. Mar. Sci. 2:00068
137. WeberM, de Beer D, Lott C, Polerecky L,Kohls K, et al. 2012. Mechanisms of damage to corals exposed to sedimentation. PNAS 109:E1558-67
138. Webster NS, Negri AP, Botté ES, Laffy PW, Flores F, et al. 2016. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6:19324
139. Webster NS, Thomas T. 2016. The sponge hologenome. mBio 7(2):e00135-16
140. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9:2707-19
141. Wegley L, Yu Y, BreitbartM, Casas V, Kline DI, Rohwer F. 2004. Coral-associated Archaea. Mar. Ecol. Prog. Ser. 273:89-96
142. Weis VM,Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringe JR. 2008. Cell biology inmodel systems as the key to understanding corals. Trends Ecol. Evol. 23:369-76
143. Welsh RM, Zaneveld JR, Rosales SM, Payet JP, Burkepile DE, Thurber RV. 2015. Bacterial predation in a marine host-associated microbiome. ISME J. 10:1540-44
144. Weynberg JD, Voolstra CR, Neave MJ, Buerger P, van Oppen MJH. 2014. From cholera to corals: viruses as drivers of virulence in a major coral bacterial pathogen. Sci. Rep. 5:17889
145. Weynberg KD,Wood-Charlson EM, Suttle CA, vanOppenMJH. 2014. Generating viralmetagenomes from the coral holobiont. Front. Microbiol. 5:206
146. Wiedenmann J, D'Angelo C, Smith EG, Hunt AN, Legiret F-E, et al. 2013. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3:160-64
147. Wild C, HuettelM, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB. 2004. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66-70
148. Wilson W, Francis I, Ryan K, Davy S. 2001. Temperature induction of viruses in symbiotic dinoflagellates. Aquat. Microb. Ecol. 25:99-102
149. Wilson WH, Dale AL, Davy JE, Davy SK. 2005. An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145-48
150. Wooldridge SA. 2009. A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis. Mar. Freshwater Res. 60:483-96
151. Work TM, Aeby GS. 2014. Microbial aggregates within tissues infect a diversity of corals throughout the Indo-Pacific. Mar. Ecol. Prog. Ser. 500:1-9
152. Yang S, Sun W, Zhang F, Li Z. 2013. Phylogenetically diverse denitrifying and ammonia-oxidizing bacteria in corals Alcyonium gracillimum and Tubastraea coccinea. Mar. Biotechnol. 15:540-51
153. Yellowlees D, Rees TAV, Leggat W. 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31:679-94
154. Yuen YS, Yamazaki SS, Baird AH, Nakamura T, Yamasaki H. 2013. Sulfate-reducing bacteria in the skeleton of the massive coral Goniastrea aspera from the Great Barrier Reef. Galaxea J. Coral Reef Stud. 15:154-59
155. Zan J, Cicirelli EM,Mohamed NM, Sibhatu H, Kroll S, et al. 2012. A complex LuxR-LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation. Mol. Microbiol. 85:916-33
156. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, et al. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down tomicrobial scales. Nat. Commun. 7:11833
157. Zhang F, Blasiak LC, Karolin JO, Powell RJ, Geddes CD, Hill RT. 2015. Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. PNAS 112:4381-86