Marine Biology

, 164:91 | Cite as

Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems

  • Bettina GlaslEmail author
  • Nicole S. Webster
  • David G. Bourne
Review, concept, and synthesis


Microorganisms play a fundamental role in the functioning and stability of coral reef ecosystems. However, environmental disturbances can trigger alterations to the natural microbial community composition and their functional traits with potentially detrimental consequences for host organisms, such as corals, sponges and algae and concomitant implications for the entire coral reef ecosystem. Coral reefs are increasingly affected by localized impacts such as declining water quality and global pressures derived from human-induced climate change, which severely alters the natural conditions on reefs and can push dominating benthic life forms towards the limit of their resistance and resilience. Microorganisms can respond very rapidly to these altered environmental conditions so defining their natural variability over spatial and temporal gradients is critical for early and accurate identification of environmental disturbances. The rapid response of microbes to environmental change is likely to confer significant advantages over traditional reef monitoring methods, which are based on visual signs of health deterioration in benthic coral reef macroorganisms. This review discusses the potential of microbes as early warning indicators for environmental stress and coral reef health and proposes priorities for future research.


Microbial Community Sponge Coral Reef Macroalgae Dissolve Organic Matter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Pedro R. Frade for inspiring scientific discussions. This study was funded by an AIMS@JCU PhD Scholarship and the Advance Queensland PhD Scholarship to BG. NSW was funded through an Australian Research Council Future Fellowship FT120100480.

Compliance with ethical standards

Conflict of interest

All authors declare they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.


  1. AIMS (2017) Australian Institute of Marine Science. Accessed 3 Feb 2017
  2. Ainsworth TD, Fine M, Roff G, Hoegh-Guldberg O (2008) Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. ISME J 2:67–73CrossRefGoogle Scholar
  3. Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M, Gates RD, Padilla-Gamino JL, Spalding HL, Smith C, Woolsey ES, Bourne DG, Bongaerts P, Hoegh-Guldberg O, Leggat W (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274CrossRefGoogle Scholar
  4. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519CrossRefGoogle Scholar
  5. Angermeier H, Glöckner V, Pawlik JR, Lindquist NL, Hentschel U (2012) Sponge white patch disease affecting the Caribbean sponge Amphimedon compressa. Dis Aquat Organ 99(2):95–102CrossRefGoogle Scholar
  6. Angly FE, Heath C, Morgan TC, Tonin H, Rich V, Schaffelke B, Bourne DG, Tyson GW (2016) Marine microbial communities of the Great Barrier Reef lagoon are influenced by riverine floodwaters and seasonal weather events. PeerJ 4:e1511CrossRefGoogle Scholar
  7. Armstrong E, Rogerson A, Leftley JW (2000) The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar Coast Shelf Sci 50:415–424CrossRefGoogle Scholar
  8. Arotsker L, Kramarsky-Winter E, Ben-Dov E, Kushmaro A (2016) Microbial transcriptome profiling of black band disease in a Faviid coral during a seasonal disease peak. Dis Aquat Org 118:77–89CrossRefGoogle Scholar
  9. Arrieta MC, Finlay BB (2012) The commensal microbiota drives immune homeostasis. Front Immunol 3:33CrossRefGoogle Scholar
  10. Ashbolt NJ, Grabow WOK, Snozzi M (2001) Indicators of microbial water quality. In: Fewtrell L, Bartram J (eds) Water quality: guidelines, standards and health. IWA Publishing, London, pp 289–316Google Scholar
  11. Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4:182–190CrossRefGoogle Scholar
  12. Aylagas E, Borja Á, Tangherlini M, Dell’Anno A, Corinaldesi C, Michell CT, Irigoien X, Danovaro R, Rodríguez-Ezpeleta N (2016) A bacterial community-based index to assess the ecological status of estuarine and costal environments. Mar Pollut Bull. doi: 10.1016/j.marpolbul.2016.10.050 Google Scholar
  13. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  14. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf 80:435–471CrossRefGoogle Scholar
  15. Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE (2016) Network analysis reveals functional redundancy and keystone taxa amongst bacterial und fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem 97:188–198CrossRefGoogle Scholar
  16. Barott KL, Rohwer FL (2012) Unseen players shape benthic competition on coral reefs. Trends Microbiol 20(12):621–628CrossRefGoogle Scholar
  17. Barott KL, Rodriguez-Brito B, Janouskovec J, Marhaver KL, Smith JE, Keeling P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192–1204CrossRefGoogle Scholar
  18. Barott KL, Rodriguez-Mueller B, Youle M, Marhaver KL, Vermeij MJ, Smith JE, Rohwer FL (2012) Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc Biol Sci 279:1655–1664CrossRefGoogle Scholar
  19. Bayer K, Schmitt S, Hentschel U (2008) Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ Microbiol 10:2942–2955CrossRefGoogle Scholar
  20. Bazelet CS, Samways MJ (2011) Identifying grasshopper bioindicators for habitat quality assessment of ecological networks. Ecol Indic 11:1259–1269CrossRefGoogle Scholar
  21. Bengtsson MM, Sjotun K, Lanzen A, Ovreas L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188–2198CrossRefGoogle Scholar
  22. Blackall LL, Wilson B, Van Oppen AJH (2015) Coral-the world’s most diverse symbiotic ecosystem. Mol Ecol 24:5330–5347CrossRefGoogle Scholar
  23. Blanquer A, Uriz MJ, Cebrian E, Galand PE (2016) Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the western Mediterranean. Front Microbiol 7:752CrossRefGoogle Scholar
  24. Boehm AB, Sassoubre LM (2014) Enterococci as indicators of environmental fecal contamination. In: Gilmore MS, Clewell DB, Ike Y, Shankar N (eds) Enterococci: from commensals to leading causes of drug resistant infection. Massachusetts Eye and Ear Infirmary, BostonGoogle Scholar
  25. Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174CrossRefGoogle Scholar
  26. Bourne DG, Webster NS (2013) Coral reef bacterial communities. In: Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer Berlin, Heidelberg, pp 163–187CrossRefGoogle Scholar
  27. Bourne DG, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363CrossRefGoogle Scholar
  28. Bourne DG, Dennis PG, Uthicke S, Soo RM, Tyson GW, Webster N (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7:1452–1458CrossRefGoogle Scholar
  29. Bourne DG, Morrow KM, Webster NS (2016) Coral holobionts: insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340CrossRefGoogle Scholar
  30. Brown EB (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  31. Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061CrossRefGoogle Scholar
  32. Bruno JF, Precht WF, Vroom PS, Aronson RB (2014) Coral reef baselines: how much macroalgae is natural? Mar Pollut Bull 80:24–29CrossRefGoogle Scholar
  33. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108:14288–14293CrossRefGoogle Scholar
  34. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011b) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600CrossRefGoogle Scholar
  35. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139CrossRefGoogle Scholar
  36. Cairns J, Pratt JR (1993) A history of biological monitoring using benthic macroinvertebrates. In: Rosenberg DM, Resh VH (eds) Freshwater biomonitoring and benthic macroinvertebrates. Chapman & Hall, New York, pp 10–27Google Scholar
  37. Cardini U, Bednarz VN, Foster RA, Wild C (2014) Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol Evol 4:1706–1727CrossRefGoogle Scholar
  38. Cardini U, Bednarz VN, Naumann MS, van Hoytema N, Rix L, Foster RA, Al-Rshaidat MMD, Wild C (2015) Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc B 282:2015257CrossRefGoogle Scholar
  39. Carignan V, Villard M-A (2002) Selecting indicator species to monitor ecological integrity: a review. Environ Monit Assess 78:45–61CrossRefGoogle Scholar
  40. Carlos C, Torres TT, Ottoboni LM (2013) Bacterial communities and species-specific associations with the mucus of Brazilian coral species. Sci Rep 3:1624CrossRefGoogle Scholar
  41. Case RJ, Longford SR, Campbell AH, Low A, Tujula N, Steinberg PD, Kjelleberg S (2011) Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ Microbiol 13:529–537CrossRefGoogle Scholar
  42. Charpy L, Casareto BE, Langlade MJ, Suzuki Y (2012) Cyanobacteria in coral reef ecosystems: a review. J Mar Biol 2012:259571CrossRefGoogle Scholar
  43. Chessman BC (1995) Rapid assessment of rivers using macroinvertebrates: a procedure based on habitat-specific sampling, family-level identification and a biotic index. Austral Ecol 20:122–129CrossRefGoogle Scholar
  44. Chun CK, Troll JV, Koroleva I, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo MdF, Casavant TL, Soares MB, Ruby EG, McFall-Ngai MJ (2008) Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc Natl Acad Sci USA 105:11323–11328CrossRefGoogle Scholar
  45. Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28(3):589–606CrossRefGoogle Scholar
  46. D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93CrossRefGoogle Scholar
  47. Daniels CA, Baumgarten S, Yum LK, Michell CT, Bayer T, Arif C, Roder C, Weil E, Voolstra CR (2015) Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease. Front Mar Sci 2:62CrossRefGoogle Scholar
  48. De Goeij J, Van den Berg H, Van Oostveen M, Epping E, Van Duyl F (2008) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357:139–151CrossRefGoogle Scholar
  49. De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684CrossRefGoogle Scholar
  50. de Oliveira LS, Gregoracci GB, Silva GGZ, Salgado LT, Filho AG, Alves-Ferreira M, Pereira RC, Thompson FL (2012) Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13:487CrossRefGoogle Scholar
  51. De Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110CrossRefGoogle Scholar
  52. de Voogd NJ, Cleary DF, Polónia AR, Gomes NC (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West Java, Indonesia. FEMS Microbiol Ecol 91(4):fiv019CrossRefGoogle Scholar
  53. De‘ath G, Fabricius KE (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850CrossRefGoogle Scholar
  54. 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. Proc Natl Acad Sci USA 109:17995–17999CrossRefGoogle Scholar
  55. Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546Google Scholar
  56. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin SA, Thurber RV, Willis BL, Azam F, Knowlton N, Rohwer F (2008) Microbial ecology of four coral atolls in the northern Line Islands. PLoS One 3:e 1584CrossRefGoogle Scholar
  57. Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Glob Chang Biol 11:2251–2265CrossRefGoogle Scholar
  58. Ducklow H (1990) The biomass, production and fate of bacteria in coral reefs. Ecosyst World 25:265–289Google Scholar
  59. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  60. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiol Rev 37:462–476CrossRefGoogle Scholar
  61. Eloe-Fadrosh EA, Rasko DA (2013) The human microbiome: from symbiosis to pathogenesis. Annu Rev Med 64:145–163CrossRefGoogle Scholar
  62. Erwin PM, Pita L, López-Legentil S, Turon X (2012) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol 78:7358–7368CrossRefGoogle Scholar
  63. European Parliament (2000) Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for the Community action in the field of water policy. Off J Eur Union 327:1–73Google Scholar
  64. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population-control in symbiotic corals. Bioscience 43:606–611CrossRefGoogle Scholar
  65. Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive earth’s biogeochemical cycles. Science 320:1034–1039CrossRefGoogle Scholar
  66. 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 7:991–1002CrossRefGoogle Scholar
  67. Fernandes N, Case RJ, Longford SR, Seyedsayamdost MR, Steinberg PD, Kjelleberg S, Thomas T (2011) Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. Plos One 6Google Scholar
  68. Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732CrossRefGoogle Scholar
  69. Fiore CL, Labrie M, Jarett JK, Lesser MP (2015) Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: molecular evidence for metabolic interchange. Front Microbiol 6:364CrossRefGoogle Scholar
  70. Fortunato CS, Eiler A, Herfort L, Needoba JA, Peterson TD, Crump BC (2013) Determining indicator taxa across spatial and seasonal gradients in the Columbia River coastal margin. ISME J 7:1899–1911CrossRefGoogle Scholar
  71. Frade PR, Roll K, Bergauer K, Herndl GJ (2016) Archaeal and bacterial communities associated with the surface mucus of Caribbean corals differ in their degree of host specificity and community turnover over reefs. PLoS One 11:e0144702CrossRefGoogle Scholar
  72. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68:2214–2228CrossRefGoogle Scholar
  73. Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134:461–470CrossRefGoogle Scholar
  74. Gardner T (2010) Monitoring forest biodiversity: improving conservation through ecologically responsible management. Earthscan Publications Ltd, LondonGoogle Scholar
  75. Garren M, Azam F (2010) New method for counting bacteria associated with coral mucus. Appl Environ Microbiol 76:6128–6133CrossRefGoogle Scholar
  76. Garren M, Azam F (2012) New directions in coral reef microbial ecology. Environ Microbiol 14:833–844CrossRefGoogle Scholar
  77. Garren M, Raymundo L, Guest J, Harvell CD, Azam F (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4:e7319CrossRefGoogle Scholar
  78. Gast GJ, Wiegman S, Wieringa E, Duyl FCV, Bak RPM (1998) Bacteria in coral reef water types: removal of cells, stimulation of growth and mineralization. Mar Ecol Prog Ser 167:37–45CrossRefGoogle Scholar
  79. GBRMPA (2016) Coral bleaching. http://wwwgbrmpagovau/media-room/coral-bleaching. Accessed 27 April 2016Google Scholar
  80. Ghaisas S, Maher J, Kanthasamy A (2016) Gut microbiome in health and disease: linking the microbiome-gut-brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacol Ther 158:52–62CrossRefGoogle Scholar
  81. Gili J-M, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321CrossRefGoogle Scholar
  82. Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:2280–2292CrossRefGoogle Scholar
  83. Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria - phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24CrossRefGoogle Scholar
  84. Gupta S, Allen-Vercoe E, Petrof EO (2016) Fecal microbiota transplantation: in perspective. Therap Adv Gastroenterol 9(2):229–239CrossRefGoogle Scholar
  85. Haas AF, Nelson CE, Kelly LW, Carlson CA, Rohwer F, Leichter JJ, Wyatt A, Smith JE (2011) Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PloS One 6Google Scholar
  86. Haas AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA, Giles S, Hatay M, Hisakawa N, Knowles B, Lim YW, Maughan H, Pantos O, Roach TNF, Sanchez SE, Silveira CB, Sandin S, Smith JE, Rohwer F (2016) Global microbialization of coral reefs. Nat Microbiol 1:16042CrossRefGoogle Scholar
  87. Hallock P, Lidz BH, Cockey-Burkhard EM, Donnelly KB (2003) Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM index In: Melzian BD, Engle VMS, Eads LK (eds) Coastal monitoring through partnerships. Springer, pp 221–238Google Scholar
  88. Hanson CE, McLaughlin MJ, Hyndes GA, Strzelecki J (2009) Selective uptake of prokaryotic picoplankton by a marine sponge (Callyspongia sp.) within an oligotrophic coastal system. Estuar Coast Shelf Sci 84:289–297CrossRefGoogle Scholar
  89. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35:305–312CrossRefGoogle Scholar
  90. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440CrossRefGoogle Scholar
  91. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Weg M (ed) Molecular marine biology of sponges. Springer Verlag, Heidelberg, pp 60–88Google Scholar
  92. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177CrossRefGoogle Scholar
  93. Herndl GJ, Velimirov B (1985) Bacteria in the coelenteron of Anthozoa: control of coelomic bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93:115–130CrossRefGoogle Scholar
  94. Hewson I, Fuhrman JA (2006) Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities. Mar Ecol Prog Ser 306:79–86CrossRefGoogle Scholar
  95. Hewson I, Poretsky RS, Tripp HJ, Montoya JP, Zehr JP (2010) Spatial patterns and light-driven variation of microbial population gene expression in surface waters of the oligotrophic open ocean. Environ Microbiol 12:1940–1956CrossRefGoogle Scholar
  96. Hill J, Wilkinson C (2004) Methods for ecological monitoring of coral reefs. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  97. Hodgson G (2001) Reef check: the first step in community-based management. Bull Mar Sci 69:861–868Google Scholar
  98. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866CrossRefGoogle Scholar
  99. Hoegh-Guldberg O (2011) The impact of climate change on coral reef ecosystems. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, pp 391–403Google Scholar
  100. 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 318:1737–1742CrossRefGoogle Scholar
  101. Hollants J, Decleyre H, Leliaert F, De Clerck O, Willems A (2011a) Life without a cell membrane: Challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta). BMC Microbiol 11Google Scholar
  102. Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A (2011b) Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PloS One 6Google Scholar
  103. Holt EA, Miller SW (2011) Bioindicators: using organisms to measure environmental impacts. Nat Educ Knowl 3(10):8Google Scholar
  104. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365CrossRefGoogle Scholar
  105. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR,  Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, Lough CM, Lowe RJ, Liu G,  McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543(7645):373–377CrossRefGoogle Scholar
  106. IMOS (2016) National Mooring Network. Accessed 24 Dec 2016
  107. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638CrossRefGoogle Scholar
  108. Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA, Haas AF, Haynes M, Lim YW, McDole T, Nelson CE, Sala E, Sandin SA, Smith JE, Vermeij MJA, Youle M, Rohwer F (2014) Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. PNAS 111:10227–10232CrossRefGoogle Scholar
  109. Kennedy J, Marchesi JR, Dobson ADW (2007) Metagenomic approaches to exploit the biotechnological potential of the microbial consortia of marine sponges. Appl Microbiol Biotechnol 75:11–20CrossRefGoogle Scholar
  110. 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 yellow-band diseased colonies. Environ Microbiol 12:541–556CrossRefGoogle Scholar
  111. Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314:119–125CrossRefGoogle Scholar
  112. Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:e54CrossRefGoogle Scholar
  113. Knutson TR, McBride JL, Chan J, Emanuel K, Holland G, Landsea C, Held I, Kossin JP, Srivastava AK, Sugi M (2010) Tropical cyclones and climate change. Nat Geosci 3:157–163CrossRefGoogle Scholar
  114. Kolkwitz R, Marsson M (1908) Ökologie der pflanzlichen Saprobien. Ber Dtsch Bot Ges 26:505–519Google Scholar
  115. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259CrossRefGoogle Scholar
  116. Kostic AD, Gevers D, Siljander H, Vatanen T, Hyotylainen T, Hamalainen AM, Peet A, Tillmann V, Poho P, Mattila I, Lahdesmaki H, Franzosa EA, Vaarala O, de Goffau M, Harmsen H, Ilonen J, Virtanen SM, Clish CB, Oresic M, Huttenhower C, Knip M, Group DS, Xavier RJ (2015) The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 17:260–273CrossRefGoogle Scholar
  117. Lachnit T, Blumel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 5:181–186CrossRefGoogle Scholar
  118. Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665CrossRefGoogle Scholar
  119. Lamb JB, van de Water JAJM, Bourne DG, Altier C, Hein MY, Fiorenza EA, Abu N, Jompa J, Harvell CD (2017) Seagrass ecosystems moderate pathogens of marine animals. ScienceGoogle Scholar
  120. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16 S rRNA marker gene sequences. Nat Biotech 31:814–821CrossRefGoogle Scholar
  121. Lema KA, Willis BL, Bourneb DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78:3136–3144CrossRefGoogle Scholar
  122. Lema KA, Willis BL, Bourne DG (2014) Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16:3345–3359CrossRefGoogle Scholar
  123. Lesser MP (2006) Benthic–pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J Exp Mar Biol Ecol 328:277–288CrossRefGoogle Scholar
  124. Lesser MP, Mazel C, Gorbunov M, Falkowski P (2004) Discovery of symbiotic nitrogen-fixing Cyanobacteria in corals. Science 305:997–1000CrossRefGoogle Scholar
  125. Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic Cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152CrossRefGoogle Scholar
  126. Li J, Chen Q, Long L-J, Dong J-D, Yang J, Zhang S (2014) Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci Rep 4Google Scholar
  127. Lipp EK, Griffin DW (2004) Analysis of coral mucus as an improved medium for detection of enteric microbes and for determining patterns of sewage contamination in reef envrionments. Eco Health 1(3):317–323Google Scholar
  128. 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 3:651–660CrossRefGoogle Scholar
  129. Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T (2012) Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515–1525CrossRefGoogle Scholar
  130. Luter HM, Whalan S, Webster NS (2010) Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl Environ Microbiol 76(17):5736–5744CrossRefGoogle Scholar
  131. Luter HM, Whalan S, Webster NS (2012) Thermal and sedimentation stress are unlikely causes of brown spot syndrome in the coral reef sponge, Ianthella basta. PLoS One 7(6):e39779CrossRefGoogle Scholar
  132. Luter HM, Gibb K, Webster NS (2014) Eutrophication has no short-term effect on the Cymbastela stipitata holobiont. Front Microbiol 5:216CrossRefGoogle Scholar
  133. Martin M, Biver S, Steels S, Barbeyron T, Jam M, Portetelle D, Michel G, Vandenbol M (2014) Functional screening of a metagenomic library of seaweed-associated microbiota: identification and characterization of a halotolerant, cold-active marine endo-ß-1, 4-endoglucanase. Appl Environ Microbiol AEM 01194–01114Google Scholar
  134. Martiny AC, Treseder K, Pusch G (2013) Phylogenetic conservatism of functional traits in microorganisms. ISME J 7:830–838CrossRefGoogle Scholar
  135. McDole T, Nulton J, Barott KL, Felts B, Hand C, Hatay M, Lee H, Nadon MO, Nosrat B, Salamon P, Bailey B, Sandin SA, Vargas-Angel B, Youle M, Zgliczynski BJ, Brainard RE, Rohwer F (2012) Assessing coral reefs on a pacific-wide scale using the microbialization score. PloS One 7Google Scholar
  136. McGeoch MA, Chown SL (1998) Scaling up the value of bioindicators. Trends Ecol Evol 13:46–47CrossRefGoogle Scholar
  137. McGeoch MA, Van Rensburg BJ, Botes A (2002) The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. J Appl Ecol 39:661–672CrossRefGoogle Scholar
  138. Meyer JL, Paul VJ, Teplitski M (2014) Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS One 9:e100316CrossRefGoogle Scholar
  139. Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4:38–48CrossRefGoogle Scholar
  140. Moriarty DJW, Pollard PC, Hunt WG (1985) Temporal and spatial variation in bacterial production in the water column over a coral reef. Mar Biol 85:285–292CrossRefGoogle Scholar
  141. Morrow KM, Paul VJ, Liles MR, Chadwick NE (2011) Allelochemicals produced by Caribbean macroalgae and Cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 30:309–320CrossRefGoogle Scholar
  142. Morrow KM, Bourne DG, Humphrey C, Botte ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE, Webster NS (2015) Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J 9:894–908CrossRefGoogle Scholar
  143. Mueller B, de Goeij JM, Vermeij MJA, Mulders Y, van der Ent E, Ribes M, van Duyl FC (2014) Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC). PLoS One 9Google Scholar
  144. Muotka T, Paavola R, Haapala A, Novikmec M, Laasonen P (2002) Long-term recovery of stream habitat structure and benthic invertebrate communities from in-stream restoration. Biol Conserv 105:243–253CrossRefGoogle Scholar
  145. Nakanishi K, Nishijima M, Nishimura M, Kuwano K, Saga N (1996) Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J Phycol 32:479–482CrossRefGoogle Scholar
  146. Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG, Apprill A, Voolstra CR (2017) Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J 11(1):186–200CrossRefGoogle Scholar
  147. Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F, Carlson CA (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7:962–979CrossRefGoogle Scholar
  148. Nguyen MTHD, Liu M, Thomas T (2014) Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol Ecol 23:1635–1645CrossRefGoogle Scholar
  149. Normile D (2016) Massive bleaching killed 35% of the coral on the northern end of the Great Barrier Reef. Accessed 30 May 2016
  150. Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923CrossRefGoogle Scholar
  151. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304CrossRefGoogle Scholar
  152. Olson JB, Thacker RW, Gochfeld DJ (2014) Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge. FEMS Microbiol Ecol 87(1):268–279CrossRefGoogle Scholar
  153. Pasolli E, Truong DT, Malik F, Waldron L, Segata N (2016) Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLoS Comput Biol 12:e1004977CrossRefGoogle Scholar
  154. Pedersen M, Nissen S, Mitarai N, Lo Svenningsen S, Sneppen K, Pedersen S (2011) The functional half-life of an mRNA depends on the ribosome spacing in an early coding region. J Mol Biol 407(1):35–44CrossRefGoogle Scholar
  155. Penhale PA, Capone DG (1981) Primary productivity and nitrogen fixation in two macroalgae-Cyanobacteria associations. Bull Mar Sci 31:164–169Google Scholar
  156. Phlips E, Zeman C (1990) Photosynthesis, growth and nitrogen fixation by epiphytic forms of filamentous Cyanobacteria from pelagic Sargassum. Bull Mar Sci 47:613–621Google Scholar
  157. Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on plankton <10 µm by the boreal sponge Mycale lingua. Mar Ecol Prog Ser 141:95–102CrossRefGoogle Scholar
  158. Pile AJ, Patterson MR, Savarese M, Chernykh VI, Fialkov VA (1997) Trophic effects of sponge feeding within Lake Baikal’s littoral zone. 2. Sponge abundance, diet, feeding efficiency, and carbon flux. Limnol Oceanogr 42:178–184CrossRefGoogle Scholar
  159. Pineda MC, Strehlow B, Duckworth A, Doyle J, Jones R, Webster NS (2016) Effects of light attenuation on the sponge holobiont-implications for dredging management. Sci Rep 6:39038CrossRefGoogle Scholar
  160. Poretsky RS, Hewson I, Sun S, Allen AE, Zehr JP, Moran MA (2009) Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environ Microbiol 11:1358–1375CrossRefGoogle Scholar
  161. Provasoli L, Pintner IJ (1980) Bacteria induced polymorphism in an axenic laboratory strain of Ulva lactuca (Chlorophyceae). J Phycol 16:196–201CrossRefGoogle Scholar
  162. Putnam HM, Davidson JM, Gates RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmental susceptible corals. Evol Appl 9:1165–1178CrossRefGoogle Scholar
  163. Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23:490–497CrossRefGoogle Scholar
  164. Raina J-B, Tapiolas D, Motti CA, Foret S, Seemann T, Tebben J, Willis BL, Bourne DG (2016) Isolation of an antimicrobial copound produced by bacteria associated with reef-building corals. PeerJ 4:e2275CrossRefGoogle Scholar
  165. Rasheed M, Badran MI, Huettel M (2003) Influence of sediment permeability and mineral composition on organic matter degradation in three sediments from the Gulf of Aqaba, Red Sea. Estuar Coast Shelf Sci 57:369–384CrossRefGoogle Scholar
  166. Reardon S (2014) Drug development microbiome therapy gains market traction. Nature 509:269–270CrossRefGoogle Scholar
  167. Reiswig HM (1971a) In situ pumping activities of tropical Demospongiae. Mar Biol 9:38–50CrossRefGoogle Scholar
  168. Reiswig HM (1971b) Particle feeding in natural populations of three marine Demosponges. Biol Bull 141:568–591CrossRefGoogle Scholar
  169. Reshef L, Koren O, Lova Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8(12):2068–2073CrossRefGoogle Scholar
  170. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  171. Ritchie KB, Smith GW (1997) Physiological comparison of bacterial communities from various species of scleractinian corals. Proc 8th Int Coral Reef Sym 1:521–526Google Scholar
  172. Rix L, de Goeij JM, Mueller CE, Struck U, Middelburg JJ, van Duyl FC, Al-Horani FA, Wild C, Naumann MS, van Oevelen D (2016) Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems. Sci Rep 6:18715CrossRefGoogle Scholar
  173. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastrea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  174. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  175. Rothig T, Ochsenkuhn MA, Roik A, van der Merwe R, Voolstra CR (2016) Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25:1308–1323CrossRefGoogle Scholar
  176. Ruby EG (2008) Symbiotic conversations are revealed under genetic interrogation. Nat Rev Micro 6:752–762CrossRefGoogle Scholar
  177. Rusch A, Hannides AK, Gaidos E (2009) Diverse communities of active Bacteria and Archaea along oxygen gradients in coral reef sediments. Coral Reefs 28:15–26CrossRefGoogle Scholar
  178. Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR (2013) Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J 7:1556–1567CrossRefGoogle Scholar
  179. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. Plos One 3Google Scholar
  180. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576CrossRefGoogle Scholar
  181. Schöttner S, Pfitzner B, Grünke S, Rasheed M, Wild C, Ramette A (2011) Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environ Microbiol 13:1815–1826CrossRefGoogle Scholar
  182. Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18CrossRefGoogle Scholar
  183. Selvin J, Shanmugha Priya S, Seghal Kiran G, Thangavelu T, Sapna Bai N (2009) Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiol Res 164:352–363CrossRefGoogle Scholar
  184. Séré MG, Tortosa P, Chabanet P, Turquet J, Quod J-P, Schleyer MH (2013) Bacterial communities associated with Porites White Patch Syndrome (PWPS) on three Western Indian Ocean (WIO) coral reefs. PLoS One 8:e83746CrossRefGoogle Scholar
  185. Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417CrossRefGoogle Scholar
  186. Sharshar N, Banaszak AT, Lesser MP, Amrami D (1997) Coral endolithic algae: life in a protected environment. Pac Sci 51:167–173Google Scholar
  187. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380CrossRefGoogle Scholar
  188. 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 10:2979–2990CrossRefGoogle Scholar
  189. Simister R, Taylor MW, Tsai P, Webster NS (2012) Sponge-microbe associations survive high nutrients and temperatures. PLoS One 7(12):e52220CrossRefGoogle Scholar
  190. Singh RP, Mantri VA, Reddy CRK, Jha B (2011) Isolation of seaweed-associated bacteria and their morphogenesis-inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol 12:13–21CrossRefGoogle Scholar
  191. Smith MJ, Kay WR, Edward DHD, Papas PJ, Richardson KSJ, Simpson JC, Pinder AM, Cale DJ, Horwitz PHJ, Davis JA, Yung FH, Norris RH, Halse SA (1999) AusRivAS: using macroinvertebrates to assess ecological condition of rivers in Western Australia. Freshwat Biol 41:269–282CrossRefGoogle Scholar
  192. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845CrossRefGoogle Scholar
  193. Sorokin YI (1973) Trophical role of bacteria in ecosystem of coral reef. Nature 242:415–417CrossRefGoogle Scholar
  194. Sorokin YI (1978) Microbial production in the coral-reef community. Arch Hydrobiol 83:281–323Google Scholar
  195. Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr 53:986–996CrossRefGoogle Scholar
  196. Stanley GD, Fautin DG (2001) The origins of modern corals. Science 291:1913–1914CrossRefGoogle Scholar
  197. Stewart F, Dmytrenko O, DeLong E, Cavanaugh C (2011) Metatranscriptomic analysis of sulfur oxidation genes in the endosymbiont of Solemya velum. Front Microbiol 2Google Scholar
  198. Stockner JG (1988) Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol Oceanogr 33:765–775Google Scholar
  199. Sunagawa S, Woodley CM, Medina MN (2010) Threatened corals provide underexplored microbial habitats. PloS One 5:e9554CrossRefGoogle Scholar
  200. Sweet MJ, Croquer A, Bythell JC (2011) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52CrossRefGoogle Scholar
  201. Sweet MJ, Bythell JC, Nugues MM (2013) Algae as reservoirs for coral pathogens. PLoS One 8:e69717CrossRefGoogle Scholar
  202. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347CrossRefGoogle Scholar
  203. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Populations induced by a phytoplankton bloom substrate-controlled succession of marine bacterioplankton. Science 336:608–611CrossRefGoogle Scholar
  204. Thacker RW, Freeman CJ (2012) Sponge-microbe symbiosis: recent advances and new directions. Adv Mar Biol 62:57–111CrossRefGoogle Scholar
  205. Thomas T, Evans FF, Schleheck D, Mai-Prochnow A, Burke C, Penesyan A, Dalisay DS, Stelzer-Braid S, Saunders N, Johnson J, Ferriera S, Kjelleberg S, Egan S (2008) Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. Plos One 3Google Scholar
  206. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD, Kjelleberg S (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4:1557–1567CrossRefGoogle Scholar
  207. Thomas T, Moitinho-Silva L, Lurgi M, Bjork JR, Easson C, Astudillo-Garcia C, Olson JB, Erwin PM, Lopez-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870CrossRefGoogle Scholar
  208. Thompson JR, Rivera HE, Closek CJ, Medina M (2015) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4Google Scholar
  209. Thoms C, Horn M, Wagner M, Hentschel U, Proksch P (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142:685–692CrossRefGoogle Scholar
  210. Thornton DCO (2014) Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 49:46–49CrossRefGoogle Scholar
  211. Thurber RLV, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, Desnues C, Edwards RA, Haynes M, Angly FE, Wegley L, Rohwer FL (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc Natl Acad Sci USA 105:18413–18418CrossRefGoogle Scholar
  212. Thurber RLV, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR (2014) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Global Change Biol 20:544–554CrossRefGoogle Scholar
  213. Tout J, Jeffries TC, Webster NS, Stocker R, Ralph PJ, Seymour JR (2014) Variability in microbial community composition and function between different niches within a coral reef. Microb Ecol 67:540–552CrossRefGoogle Scholar
  214. Trias R, Garcia-Lledo A, Sanchez N, Lopez-Jurado JL, Hallin S, Baneras L (2012) Abundance and composition of epiphytic bacterial and archaeal ammonia oxidizers of marine red and brown macroalgae. Appl Environ Microbiol 78:318–325CrossRefGoogle Scholar
  215. Uthicke S, McGuire K (2007) Bacterial communities in Great Barrier Reef calcareous sediments: contrasting 16 S rDNA libraries from nearshore and outer shelf reefs. Estuar Coast Shelf Sci 72:188–200CrossRefGoogle Scholar
  216. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314CrossRefGoogle Scholar
  217. Valentine JF, Heck KL (2005) Perspective review of the impacts of overfishing on coral reef food web linkages. Coral Reefs 24:209–213CrossRefGoogle Scholar
  218. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2014) Building coral reef resilience through assisted evolution. PNAS 112(8):2307–2313CrossRefGoogle Scholar
  219. Vega Thurber RL, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale EA, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163CrossRefGoogle Scholar
  220. Vega Thurber R, Burkepile DE, Correa AM, Thurber AR, Shantz AA, Welsh R, Pritchard C, Rosales S (2012) Macroalgae decrease growth and alter microbial community structure of the reef-building coral, Porites astreoides. PLoS One 7:e44246CrossRefGoogle Scholar
  221. Vermeij MJA, Moorselaar IV, Engelhard S, Hörnlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS One 5:e14212CrossRefGoogle Scholar
  222. von Bergen M, Jehmlich N, Taubert M, Vogt C, Bastida F, Herbst FA, Schmidt F, Richnow HH, Seifert J (2013) Insights from quantitative metaproteomics and protein-stable isotope probing into microbial ecology. ISME J 7:1877–1885CrossRefGoogle Scholar
  223. Wade TJ, Sams E, Brenner KP, Haugland R, Chern E, Beach M, Wymer L, Rankin CC, Love D, Li Q, Noble R, Dufour AP (2010) Measured indicators of recreational water quality and swimming-associated illness at marine beaches: a prospective cohort study. Environ Health 9:66CrossRefGoogle Scholar
  224. Wang WL, Xu SY, Ren ZG, Tao L, Jiang JW, Zheng SS (2015) Application of metagenomics in the human gut microbiome. World J Gastroentero 21:803–814CrossRefGoogle Scholar
  225. Webster NS (2017) Conceptual and methodological advances for holobiont research. Environ Microbiol Rep. doi: 10.1111/1758-2229.12500 Google Scholar
  226. Webster NS, Thomas T (2016) The sponge hologenome. mBio 7(2):e00135–16CrossRefGoogle Scholar
  227. Webster NS, Watts EMJ, Hill TR (2001) Detection and phylogenetic analysis of novel Crenarchaeote and Euryarchaeote 16 S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol 3:600–608CrossRefGoogle Scholar
  228. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R (2008a) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol 10(12):3366–3376CrossRefGoogle Scholar
  229. Webster NS, Cobb RE, Negri AP (2008b) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2:830–842CrossRefGoogle Scholar
  230. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082Google Scholar
  231. Webster FJ, Babcock RC, Van Keulen M, Loneragan NR (2015) Macroalgae inhibits larval settlement and increases recruit mortality at Ningaloo Reef, Western Australia. Plos One 10Google Scholar
  232. 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 9:2807–2719CrossRefGoogle Scholar
  233. Wehrl M, Steinert M, Hentschel U (2007) Bacterial uptake by the marine sponge Aplysina aerophoba. Microb Ecol 53:355–365CrossRefGoogle Scholar
  234. Wemheuer B, Wemheuer F, Hollensteiner J, Meyer F-D, Voget S, Daniel R (2015) The green impact: bacterioplankton response toward a phytoplankton spring bloom in the southern North Sea assessed by comparative metagenomic and metatranscriptomic approaches. Front Microbiol 6:805CrossRefGoogle Scholar
  235. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. PNAS 95:6578–6583CrossRefGoogle Scholar
  236. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004a) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRefGoogle Scholar
  237. Wild C, Rasheed M, Werner U, Franke U, Johnstone R, Huettel M (2004b) Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267:159–171CrossRefGoogle Scholar
  238. Wild C, Laforsch C, Huettel M (2006) Detection and enumeration of microbial cells within highly porous calcareous reef sands. Mar Freshwater Res 57:415–420CrossRefGoogle Scholar
  239. Wilkinson C (1980) Cyanobacteria symbiotic in marine sponges. Endocytobiosis Cell Res 1:553–563Google Scholar
  240. Wilkinson CR, Garrone R, Vacelet J (1984) Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc R Soc Lond [Biol] 220:519–528CrossRefGoogle Scholar
  241. Wohl DL, Arora S, Gladstone JR (2004) Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecol 85(6):1534–1540CrossRefGoogle Scholar
  242. Wrede C, Dreier A, Kokoschka S, Hoppert M (2012) Archaea in symbioses. Archaea 2012:11CrossRefGoogle Scholar
  243. Wright JF (1995) Development and use of a system for predicting the macroinvertebrate fauna in flowing waters. Aust J Ecol 20:181–197CrossRefGoogle Scholar
  244. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. PNAS 96:1463–1468CrossRefGoogle Scholar
  245. Yang S, Sun W, Zhang FL, Li ZY (2013) Phylogenetically diverse denitrifying and ammonia-oxidizing bacteria in corals Alcyonium gracillimum and Tubastraea coccinea. Mar Biotechnol 15:540–551CrossRefGoogle Scholar
  246. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, RoryWelsh, Correa AMS, Lemoine NP, Rosales S, Fuchs C, Maynard JA, Thurber RV (2016) Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun 7:11833CrossRefGoogle Scholar
  247. Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105:629–640CrossRefGoogle Scholar
  248. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:14213CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Bettina Glasl
    • 1
    • 2
    • 3
    Email author
  • Nicole S. Webster
    • 1
    • 3
    • 4
  • David G. Bourne
    • 1
    • 2
    • 3
  1. 1.Australian Institute of Marine ScienceTownsvilleAustralia
  2. 2.College of Science and Engineering, James Cook UniversityTownsvilleAustralia
  3. 3.AIMS@JCUTownsvilleAustralia
  4. 4.Australian Centre for Ecogenomics, University of QueenslandBrisbaneAustralia

Personalised recommendations