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Coral Microbiomes as Bioindicators of Reef Health

  • Sofia Roitman
  • F. Joseph Pollock
  • Mónica Medina
Chapter
Part of the Population Genomics book series

Abstract

Coral reefs are currently in steep decline worldwide due to changes in climate and anthropogenic activity. Given reefs’ key roles as centers of biodiversity and the variety of services they provide for humans, it is imperative that we develop reef management strategies that are sensitive to environmental changes and that allow timely interventions in response to specific threats. The use of bioindicators has been demonstrated as an effective way to monitor a broad range of ecosystems, and coral microbiomes show immense potential as bioindicators for coral reefs. Given the decline of coral reefs worldwide, and the diversity of species that are currently under threat, coral microbiomes can provide much-needed insights and information for the purposes of reef conservation and protection.

Keywords

16S Bacteria Bioindicator Conservation Coral reef Ecosystem management Metagenomics Metatranscriptomics Microbiome Sequencing 

Notes

Acknowledgments

We thank Ryan McMinds and Jesse Zaneveld for constructive comments on the manuscript. We also thank the members of the Medina Lab for input on the ideas advanced in this chapter. This work was partially funded by NSF grants OCE 1442206 and OCE 1642311 to Monica Medina.

References

  1. AIMS. Australian Institute of Marine Science Annual Report 2012–13. Townsville: Australian Institute of Marine Science; 2013.Google Scholar
  2. Ainsworth TD, Thurber RV, Gates RD. The future of coral reefs: a microbial perspective. Trends Ecol Evol. 2010;25:233–40.Google Scholar
  3. Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M, Gates RD, Padilla-Gamiño JL, Spalding HL, Smith C, et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 2015;9:2261–74.Google Scholar
  4. Apprill A, Weber LG, Santoro AE. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems. 2016;1:e00143–16.Google Scholar
  5. Babu TG, Nithyanand P, Kannapiran E, Ravi AV, Pandian KS. Molecular identification of bacteria associated with the coral reef ecosystem of Gulf of Mannar Marine Biosphere Reserve using 16S rRNA sequences. In: Proceedings national seminar on new frontiers in marine bioscience research. Karaikudi: Alagappa University; 2004. p. 47–53.Google Scholar
  6. Ben-Haim Y, Thompson FL, Thompson CC, Cnockaert MC, Hoste B, Swings J, Rosenberg E. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Microbiol. 2003;53:309–15.Google Scholar
  7. Bispo A, Cluzeau D, Creamer R, Dombos M, Graefe U, Krogh PH, Sousa JP, Peres G, Rutgers M, Winding A, et al. Indicators for monitoring soil biodiversity. Integr Environ Assess Manag. 2009;5:717–9.Google Scholar
  8. Bloem J, Breure AM. Microbial indicators. Trace Met Other Contam Environ. 2003;6:259–82.Google Scholar
  9. Bouchet P. The exploration of marine biodiversity: scientific and technological challenges. In: Duarte CM, editor. The exploration of marine biodiversity: scientific and technological challenges. Bilbao: Fundación BBVA; 2006. p. 31–6.Google Scholar
  10. Bourne DG, Munn CB. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol. 2005;7:1162–74.Google Scholar
  11. Bourne DG, Webster NS. Coral reef bacterial communities. In: The prokaryotes. Berlin: Springer; 2013. p. 163–87.Google Scholar
  12. Brookes PC. The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils. 1995;19:269–79.Google Scholar
  13. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 2007;5:e124.Google Scholar
  14. Burns A, Ryder DS. Potential for biofilms as biological indicators in Australian riverine systems. Ecol Manage Restor. 2001;2:53–64.Google Scholar
  15. Cardenas E, Tiedje JM. New tools for discovering and characterizing microbial diversity. Curr Opin Biotechnol. 2008;19:544–9.Google Scholar
  16. Cárdenas A, Rodriguez-r LM, Pizarro V, Cadavid LF, Arévalo-Ferro C. Shifts in bacterial communities of two Caribbean reef-building coral species affected by white plague disease. ISME J. 2012;6:502.Google Scholar
  17. Cooney RP, Pantos O, Le Tissier MD, Barer MR, Bythell JC, et al. Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol. 2002;4:401–13.Google Scholar
  18. Cooper TF, Gilmour JP, Fabricius KE. Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs. 2009;28:589–606.Google Scholar
  19. Daniels C, Baumgarten S, Yum LK, Michell CT, Bayer T, Arif C, Roder C, Weil E, Voolstra CR. Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease. Front Mar Sci. 2015;2:62.Google Scholar
  20. de O Santos E, Alves N Jr, Dias GM, Mazotto AM, Vermelho A, Vora GJ, Wilson B, Beltran VH, Bourne DG, Le Roux F. Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J. 2011;5:1471.Google Scholar
  21. De’ath G, Fabricius K. Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl. 2010;20:840–50.Google Scholar
  22. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8:881–90.Google Scholar
  23. Ehrlich P, Ehrlich A. Extinction: the causes and consequences of the disappearance of species. New York: Random House; 1981.Google Scholar
  24. Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319.Google Scholar
  25. Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, LeGrand H, Thompson A, Schaffelke B. A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Pollut Bull. 2012;65:320–32.Google Scholar
  26. Foissner W, Berger H. A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw Biol. 1996;35:375–482.Google Scholar
  27. Galloway-Peña JR, Smith DP, Sahasrabhojane P, Ajami NJ, Wadsworth WD, Daver NG, Chemaly RF, Marsh L, Ghantoji SS, Pemmaraju N, et al. The role of the gastrointestinal microbiome in infectious complications during induction chemotherapy for acute myeloid leukemia. Cancer. 2016;122:2186–96.Google Scholar
  28. Gil-Agudelo DL, Smith GW, Garzón-Ferreira J, Weil E, Petersen D. Dark spots disease and yellow band disease, two poorly known coral diseases with high incidence in Caribbean reefs. In: Coral health disease. Berlin: Springer; 2004. p. 337–49.Google Scholar
  29. Gladfelter WB. White-band disease in Acropora palmata: implications for the structure and growth of shallow reefs. Bull Mar Sci. 1982;32:639–43.Google Scholar
  30. Glasl B, Webster NS, Bourne DG. Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems. Mar Biol. 2017;164:91.Google Scholar
  31. Hallock P, Lidz BH, Cockey-Burkhard EM, Donnelly KB. Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM index. In: Coastal monitoring through partnerships. Dordrecht: Springer; 2003. p. 221–38.Google Scholar
  32. Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography. 2007;20:172–95.Google Scholar
  33. Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ. Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotechnol. 1999;1:33–43.Google Scholar
  34. Hentschel U, Piel J, Degnan SM, Taylor MW. Genomic insights into the marine sponge microbiome. Nat Rev Microbiol. 2012;10:641.Google Scholar
  35. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, et al. Coral reefs under rapid climate change and ocean acidification. Science. 2007;318:1737–42.Google Scholar
  36. Holling CS. Adaptive environmental assessment and management. New York: Wiley; 1978.Google Scholar
  37. Holt EA, Miller SW. Bioindicators: using organisms to measure environmental impacts. Nat Educ Knowl. 2011;3:8.Google Scholar
  38. Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol. 2007;45:2761–4.Google Scholar
  39. Jessen C, Lizcano JFV, Bayer T, Roder C, Aranda M, Wild C, Voolstra CR. In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS One. 2013;8:e62091.Google Scholar
  40. Jones RJ, Muller J, Haynes D, Schreiber U. Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia. Mar Ecol Prog Ser. 2003;251:153–67.Google Scholar
  41. Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, Mavromatis K, Woyke T, Hentschel U. Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J. 2013;7:2287.Google Scholar
  42. Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol. 2010;12:541–56.Google Scholar
  43. Klaus JS, Janse I, Heikoop JM, Sanford RA, Fouke BW. Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol. 2007;9:1291–305.Google Scholar
  44. Knowlton N, Rohwer F. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat. 2003;162:S51–62.Google Scholar
  45. Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ. Coral reef biodiversity. In: Life in the world’s oceans: diversity distribution and abundance. Chichester: Wiley; 2010. p. 65–74.Google Scholar
  46. Kriwy P, Uthicke S. Microbial diversity in marine biofilms along a water quality gradient on the Great Barrier Reef. Syst Appl Microbiol. 2011;34:116–26.Google Scholar
  47. LaJeunesse TC. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol. 2001;37:866–80.Google Scholar
  48. Lee ST, Davy SK, Tang S-L, Fan T-Y, Kench PS. Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress. FEMS Microbiol Ecol. 2015;91:fiv142.Google Scholar
  49. Lee ST, Davy SK, Tang S-L, Kench PS. Mucus sugar content shapes the bacterial community structure in thermally stressed Acropora muricata. Front Microbiol. 2016;7:371.Google Scholar
  50. Leite D, Falcão Salles J, Calderon E, Castro CBE, Bianchini A, Marques J, Van Elsas JD, Peixoto R. Coral bacterial-core abundance and network complexity as proxies for anthropogenic pollution. Front Microbiol. 2018;9:833.Google Scholar
  51. Littman R, Willis BL, Bourne DG. Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Rep. 2011;3:651–60.Google Scholar
  52. Liu J, Weinbauer MG, Maier C, Dai M, Gattuso J-P. Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol. 2010;61:291–305.Google Scholar
  53. Luo B, Gu W, Zhong J, Wang Y, Zhang G. Revealing crosstalk of plant and fungi in the symbiotic roots of sewage-cleaning Eichhornia crassipes using direct de novo metatranscriptomic analysis. Sci Rep. 2015;5:15407.Google Scholar
  54. Mages M, Óvári M, Tümpling WV, Kröpfl K. Biofilms as bio-indicator for polluted waters? Anal Bioanal Chem. 2004;378:1095–101.Google Scholar
  55. Martinez X, Pozuelo M, Pascal V, Campos D, Gut I, Gut M, Azpiroz F, Guarner F, Manichanh C. MetaTrans: an open-source pipeline for metatranscriptomics. Sci Rep. 2016;6:26447.Google Scholar
  56. McDevitt-Irwin JM, Baum JK, Garren M, Vega Thurber RL. Responses of coral-associated bacterial communities to local and global stressors. Front Mar Sci. 2017;4:262.Google Scholar
  57. Mendes S, Azul AM, Castro P, Römbke J, Sousa JP. Protecting soil biodiversity and soil functions: current status and future challenges. In: Biodiversity and education for sustainable development. Berlin: Springer; 2016. p. 249–63.Google Scholar
  58. Moitinho-Silva L, Seridi L, Ryu T, Voolstra CR, Ravasi T, Hentschel U. Revealing microbial functional activities in the Red Sea sponge Stylissa carteri by metatranscriptomics. Environ Microbiol. 2014;16:3683–98.Google Scholar
  59. Morrow KM, Moss AG, Chadwick NE, Liles MR. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol. 2012;78:6438–49.Google Scholar
  60. Mouchka ME, Hewson I, Harvell CD. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol. 2010;50:662–74.Google Scholar
  61. Mulhall M. Saving the rainforest of the sea: an analysis of international efforts to conserve coral reefs. In: Duke environmental law and policy forum, vol. 19; 2008. p. 321.Google Scholar
  62. Nielsen MN, Winding A, Binnerup S, Hansen BM, Hendriksen NB, Kroer N. Microorganisms as indicators of soil health. Copenhagen: National Environmental Research Institute; 2002.Google Scholar
  63. Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RP. Algal contact as a trigger for coral disease. Ecol Lett. 2004;7:919–23.Google Scholar
  64. Nwuche CO, Ugoji EO. Effects of heavy metal pollution on the soil microbial activity. Int J Environ Sci Technol. 2008;5:409–14.Google Scholar
  65. Parmar TK, Rawtani D, Agrawal YK. Bioindicators: the natural indicator of environmental pollution. Front Life Sci. 2016;9:110–8.Google Scholar
  66. Parry M, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, et al. Climate change 2007: impacts, adaptation and vulnerability. Cambridge: Cambridge University Press; 2007.Google Scholar
  67. Peixoto RS, Rosado PM, Leite DC, Rosado AS, Bourne DG. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol. 2017;8:341.Google Scholar
  68. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S. A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis. ISME J. 2012;6:1314.Google Scholar
  69. Phillips DJ, Rainbow PS. Biomonitoring of trace aquatic contaminants. Berlin: Springer; 2013.Google Scholar
  70. Plaisance L, Caley MJ, Brainard RE, Knowlton N. The diversity of coral reefs: what are we missing? PLoS One. 2011;6:e25026.Google Scholar
  71. Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL. Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS One. 2014;9:e102498.Google Scholar
  72. Rogers CS, Garrison G, Grober R, Hillis Z-M, Franke MA. Coral reef monitoring manual for the Caribbean and Western Atlantic. Virgin Islands National Park: St. John; 1994.Google Scholar
  73. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1–10.Google Scholar
  74. Röthig T, Ochsenkühn MA, Roik A, Van Der Merwe R, Voolstra CR. Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol. 2016;25:1308–23.Google Scholar
  75. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T, Hentschel U. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 2011;5:61.Google Scholar
  76. Sims A, Zhang Y, Gajaraj S, Brown PB, Hu Z. Toward the development of microbial indicators for wetland assessment. Water Res. 2013;47:1711–25.Google Scholar
  77. Sobolev D, Begonia M. Effects of heavy metal contamination upon soil microbes: lead-induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int J Environ Res Public Health. 2008;5:450–6.Google Scholar
  78. Stone D, Ritz K, Griffiths BG, Orgiazzi A, Creamer RE. Selection of biological indicators appropriate for European soil monitoring. Appl Soil Ecol. 2016;97:12–22.Google Scholar
  79. Streit WR, Schmitz RA. Metagenomics – the key to the uncultured microbes. Curr Opin Microbiol. 2004;7:492–8.Google Scholar
  80. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 2009;3:512–21.Google Scholar
  81. Tan B, Ng CM, Nshimyimana JP, Loh L-L, Gin KY-H, Thompson JR. Next-generation sequencing (NGS) for assessment of microbial water quality: current progress, challenges, and future opportunities. Front Microbiol. 2015;6:1027.Google Scholar
  82. Tarca AL, Carey VJ, Chen X, Romero R, Drăghici S. Machine learning and its applications to biology. PLoS Comput Biol. 2007;3:e116.Google Scholar
  83. Thakur RK, Jindal R, Singh UB, Ahluwalia AS. Plankton diversity and water quality assessment of three freshwater lakes of Mandi (Himachal Pradesh, India) with special reference to planktonic indicators. Environ Monit Assess. 2013;185:8355.Google Scholar
  84. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F. Metagenomic analysis of stressed coral holobionts. Environ Microbiol. 2009;11:2148–63.Google Scholar
  85. Vega Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Chang Biol. 2014;20:544–54.Google Scholar
  86. Wang D, Bodovitz S. Single cell analysis: the new frontier in “omics”. Trends Biotechnol. 2010;28:281–90.Google Scholar
  87. Wei H, Dong L, Wang T, Zhang M, Hua W, Zhang C, Pang X, Chen M, Su M, Qiu Y, et al. Structural shifts of gut microbiota as surrogate endpoints for monitoring host health changes induced by carcinogen exposure. FEMS Microbiol Ecol. 2010;73:577–86.Google Scholar
  88. Witt V, Wild C, Uthicke S. Terrestrial runoff controls the bacterial community composition of biofilms along a water quality gradient in the Great Barrier Reef. Appl Environ Microbiol. 2012;78:7786–91.Google Scholar
  89. Yergeau E, Lawrence JR, Sanschagrin S, Waiser MJ, Korber DR, Greer CW. Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl Environ Microbiol. 2012;78:7626–37.Google Scholar
  90. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, Welsh R, Correa AM, Lemoine NP, Rosales S, et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun. 2016;7:11833.Google Scholar
  91. Zaneveld JR, McMinds R, Vega TR. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol. 2017;2:17121.Google Scholar
  92. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun. 2017;8:14213.Google Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sofia Roitman
    • 1
  • F. Joseph Pollock
    • 1
  • Mónica Medina
    • 1
  1. 1.Department of BiologyThe Pennsylvania State UniversityUniversity ParkUSA

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