1932

Abstract

The use of Beneficial Microorganisms for Corals (BMCs) has been proposed recently as a tool for the improvement of coral health, with knowledge in this research topic advancing rapidly. BMCs are defined as consortia of microorganisms that contribute to coral health through mechanisms that include () promoting coral nutrition and growth, () mitigating stress and impacts of toxic compounds, () deterring pathogens, and () benefiting early life-stage development. Here, we review the current proposed BMC approach and outline the studies that have proven its potential to increase coral resilience to stress. We revisit and expand the list of putative beneficial microorganisms associated with corals and their proposed mechanismsthat facilitate improved host performance. Further, we discuss the caveats and bottlenecks affecting the efficacy of BMCs and close by focusing on the next steps to facilitate application at larger scales that can improve outcomes for corals and reefs globally.

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2021-02-15
2024-03-28
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Literature Cited

  1. 1. 
    Bosch TCG, McFall-Ngai MJ. 2011. Metaorganisms as the new frontier. Zoology 114:185–90
    [Google Scholar]
  2. 2. 
    Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ et al. 2018. Metaorganisms in extreme environments: Do microbes play a role in organismal adaptation. Zoology 127:1–19
    [Google Scholar]
  3. 3. 
    LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD et al. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:2570–80.e6
    [Google Scholar]
  4. 4. 
    Muscatine L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. Ecosystems of the World: Coral Reefs Z Dubinsky 75–87 New York: Elsevier
    [Google Scholar]
  5. 5. 
    Pogoreutz C, Voolstra CR, Rädecker N, Weis V, Cardenas A, Raina J-B 2020. The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes. Cellular Dialogues in the Holobiont T Bosch, M Hadfield Boca Raton, FL: CRC Press
    [Google Scholar]
  6. 6. 
    Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT et al. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:637180–83
    [Google Scholar]
  7. 7. 
    Duarte GAS, Villela HDM, Deocleciano M, Silva D, Barno A et al. 2020. Heat waves are a major threat to turbid coral reefs in Brazil. Front. Mar. Sci. 7:179
    [Google Scholar]
  8. 8. 
    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 to microbial scales. Nat. Commun. 7:11833
    [Google Scholar]
  9. 9. 
    Sweet M, Burian A, Fifer J, Bulling M, Elliott D, Raymundo L 2019. Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease. Microbiome 7:139
    [Google Scholar]
  10. 10. 
    Putnam HM, Barott KL, Ainsworth TD, Gates RD 2017. The vulnerability and resilience of reef-building corals. Curr. Biol. 27:11R528–40
    [Google Scholar]
  11. 11. 
    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
    [Google Scholar]
  12. 12. 
    Peixoto R, Rosado PM, de Assis Leite DC, Rosado AS, Bourne DG 2017. Beneficial Microorganisms for Corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8:341
    [Google Scholar]
  13. 13. 
    Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG et al. 2017. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J 11:186–200
    [Google Scholar]
  14. 14. 
    Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5:355–62
    [Google Scholar]
  15. 15. 
    Bourne DG, Morrow KM, Webster NS 2016. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70:317–40
    [Google Scholar]
  16. 16. 
    Sweet MJ, Bulling MT. 2017. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4:9
    [Google Scholar]
  17. 17. 
    Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR 2017. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8:14213
    [Google Scholar]
  18. 18. 
    Ziegler M, Grupstra CGB, Barreto MM, Eaton M, BaOmar J et al. 2019. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10:3092
    [Google Scholar]
  19. 19. 
    Hume BCC, Mejia-Restrepo A, Voolstra CR, Berumen ML 2020. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 39:583–601
    [Google Scholar]
  20. 20. 
    Röthig T, Ochsenkühn 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. 25:61308–23
    [Google Scholar]
  21. 21. 
    Voolstra CR, Ziegler M. 2020. Adapting with microbial help: Microbiome flexibility facilitates rapid responses to environmental change. BioEssays 42:72000004
    [Google Scholar]
  22. 22. 
    Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:122068–73
    [Google Scholar]
  23. 23. 
    Pollock FJ, Morris PJ, Willis BL, Bourne DG 2011. The urgent need for robust coral disease diagnostics. PLOS Pathog. 7:10e1002183
    [Google Scholar]
  24. 24. 
    Pollock FJ, Wilson B, Johnson WR, Morris PJ, Willis BL, Bourne DG 2010. Phylogeny of the coral pathogen Vibrio coralliilyticus. Environ. Microbiol. Rep 2:1172–78
    [Google Scholar]
  25. 25. 
    Ushijima B, Videau P, Burger AH, Shore-Maggio A, Runyon CM et al. 2014. Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl. Environ. Microbiol. 80:72102–9
    [Google Scholar]
  26. 26. 
    Sutherland KP, Berry B, Park A, Kemp DW, Kemp KM et al. 2016. Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994–2014. Philos. Trans. R. Soc. B 371:168920150205
    [Google Scholar]
  27. 27. 
    Beurmann S, Ushijima B, Videau P, Svoboda CM, Smith AM et al. 2017. Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata. PLOS One 12:11e0188319
    [Google Scholar]
  28. 28. 
    Séré MG, Tortosa P, Chabanet P, Quod JP, Sweet MJ, Schleyer MH 2015. Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean. Mol. Ecol. 24:174570–81
    [Google Scholar]
  29. 29. 
    Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E 2001. Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int. J. Syst. Evol. Microbiol 51:41383–88
    [Google Scholar]
  30. 30. 
    Thompson FL, Barash Y, Sawabe T, Sharon G, Swings J, Rosenberg E 2006. Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int. J. Syst. Evol. Microbiol. 56:2365–68
    [Google Scholar]
  31. 31. 
    Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD 2009. Microbial disease and the coral holobiont. Trends Microbiol 17:12554–62
    [Google Scholar]
  32. 32. 
    Mera H, Bourne DG. 2018. Disentangling causation: complex roles of coral-associated microorganisms in disease. Environ. Microbiol. 20:2431–49
    [Google Scholar]
  33. 33. 
    Saharan BS, Nehra V. 2011. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res. 21:1–30
    [Google Scholar]
  34. 34. 
    Woodhams DC, Bletz M, Kueneman J, McKenzie V 2016. Managing amphibian disease with skin microbiota. Trends Microbiol 24:3161–64
    [Google Scholar]
  35. 35. 
    Alberoni D, Gaggìa F, Baffoni L, Di Gioia D 2016. Beneficial microorganisms for honey bees: problems and progresses. Appl. Microbiol. Biotechnol. 100:229469–82
    [Google Scholar]
  36. 36. 
    West AG, Waite DW, Deines P, Bourne DG, Digby A et al. 2019. The microbiome in threatened species conservation. Biol. Conserv. 229:85–98
    [Google Scholar]
  37. 37. 
    McKenzie VJ, Kueneman JG, Harris RN 2018. Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine. Ann. N.Y. Acad. Sci. 1429:118–30
    [Google Scholar]
  38. 38. 
    Cheng TL, Mayberry H, McGuire LP, Hoyt JR, Langwig KE et al. 2017. Efficacy of a probiotic bacterium to treat bats affected by the disease white‐nose syndrome. J. Appl. Ecol. 54:3701–8
    [Google Scholar]
  39. 39. 
    Rosado P, Leite DCA, Duarte GAS, Chaloub RM, Jospin G et al. 2019. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J 13:921–36
    [Google Scholar]
  40. 40. 
    Hoyt JR, Langwig KE, White JP, Kaarakka HM, Redell JA et al. 2019. Field trial of a probiotic bacteria to protect bats from white-nose syndrome. Sci. Rep. 9:9158
    [Google Scholar]
  41. 41. 
    Teplitski M, Ritchie K. 2009. How feasible is the biological control of coral diseases. Trends Ecol. Evol. 24:7378–85
    [Google Scholar]
  42. 42. 
    Peixoto RS, Sweet M, Bourne DG 2019. Customized medicine for corals. Front. Mar. Sci. 6:686
    [Google Scholar]
  43. 43. 
    Santos HF, Duarte GAS, da Costa Rachid CT, Chaloub RM, Calderon EN et al. 2015. Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota. Sci. Rep. 5:18268
    [Google Scholar]
  44. 44. 
    Morgans CA, Hung JY, Bourne DG, Quigley KM 2020. Symbiodiniaceae probiotics for use in bleaching recovery. Restor. Ecol. 28:2282–88
    [Google Scholar]
  45. 45. 
    Damjanovic K, van Oppen MJH, Menéndez P, Blackall LL 2019. Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea. Front. Microbiol 10:1702
    [Google Scholar]
  46. 46. 
    Dunphy CM, Gouhier TC, Chu ND, Vollmer SV 2019. Structure and stability of the coral microbiome in space and time. Sci. Rep. 9:6785
    [Google Scholar]
  47. 47. 
    Mathur V, del Campo J, Kolisko M, Keeling PJ 2018. Global diversity and distribution of close relatives of apicomplexan parasites. Environ. Microbiol. 20:82824–33
    [Google Scholar]
  48. 48. 
    Kwong WK, del Campo J, Mathur V, Vermeij MJA, Keeling PJ 2019. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568:7750103–7
    [Google Scholar]
  49. 49. 
    McFadden GI, Reith ME, Munholland J, Lang-Unnasch N 1996. Plastid in human parasites. Nature 381:6582482
    [Google Scholar]
  50. 50. 
    Vohsen SA, Anderson KE, Gade AM, Gruber-Vodicka HR, Dannenberg RP et al. 2020. Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans. Microbiome 8:34
    [Google Scholar]
  51. 51. 
    Robbins SJ, Singleton CM, Chan CX, Messer LF, Geers AU et al. 2019. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat. Microbiol. 4:122090–100
    [Google Scholar]
  52. 52. 
    Smith SM. 2018. Complementarity in the coral holobiont: a genomic analysis of bacterial isolates of Orbicella faveolata and Symbiodinium spp Masters Thesis, Coll. Sci., Pa. State Univ State Park, PA: https://etda.libraries.psu.edu/files/final_submissions/17896
    [Google Scholar]
  53. 53. 
    Agostini S, Suzuki Y, Higuchi T, Casareto BE, Yoshinaga K et al. 2012. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31:147–56
    [Google Scholar]
  54. 54. 
    Hopkinson BM, Morel FMM. 2009. The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659–69
    [Google Scholar]
  55. 55. 
    Reich HG, Rodriguez IB, LaJeunesse TC, Ho T-Y 2020. Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae. Coral Reefs 39:915–27
    [Google Scholar]
  56. 56. 
    Shick JM, Iglic K, Wells ML, Trick CG, Doyle J, Dunlap WC 2011. Responses to iron limitation in two colonies of Stylophora pistillata exposed to high temperature: implications for coral bleaching. Limnol. Oceanogr. 56:3813–28
    [Google Scholar]
  57. 57. 
    Schalk IJ, Hannauer M, Braud A 2011. New roles for bacterial siderophores in metal transport and tolerance. Environ. Microbiol. 13:112844–54
    [Google Scholar]
  58. 58. 
    Barnes DJ. 1970. Coral skeletons: an explanation of their growth and structure. Science 170:39641305–8
    [Google Scholar]
  59. 59. 
    Al-Horani F, Al-Moghrabi SM, de Beer D. 2003. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar. Biol 142:419–26
    [Google Scholar]
  60. 60. 
    Biscéré T, Ferrier-Pagès C, Grover R, Gilbert A, Rottier C et al. 2018. Enhancement of coral calcification via the interplay of nickel and urease. Aquat. Toxicol. 200:247–56
    [Google Scholar]
  61. 61. 
    Barnes DJ, Crossland CJ. 1976. Urease activity in the staghorn coral. Acropora acuminata. Comp. Biochem. Physiol. B 55:3371–76
    [Google Scholar]
  62. 62. 
    Villela HDM, Vilela CLS, Assis JM, Varona N, Burke C et al. 2019. Prospecting microbial strains for bioremediation and probiotics development for metaorganism research and preservation. J. Vis. Exp. 152:e60238
    [Google Scholar]
  63. 63. 
    Domart-Coulon IJ, Sinclair CS, Hill RT, Tambutté S, Puverel S, Ostrander GK 2004. A basidiomycete isolated from the skeleton of Pocillopora damicornis (Scleractinia) selectively stimulates short-term survival of coral skeletogenic cells. Mar. Biol. 144:3583–92
    [Google Scholar]
  64. 64. 
    Pernice M, Raina J-B, Rädecker N, Cárdenas A, Pogoreutz C, Voolstra CR 2019. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J 14:325–34
    [Google Scholar]
  65. 65. 
    Fine M, Loya Y. 2002. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. Biol. Sci. 269:14971205–10
    [Google Scholar]
  66. 66. 
    Jeong HJ, Du Yoo Y, Kang NS, Lim AS, Seong KA et al. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. PNAS 109:3112604–9
    [Google Scholar]
  67. 67. 
    Lawson CA, Raina J-B, Kahlke T, Seymour JR, Suggett DJ 2018. Defining the core microbiome of the symbiotic dinoflagellate. Symbiodinium. Environ. Microbiol. Rep. 10:17–11
    [Google Scholar]
  68. 68. 
    Bernasconi R, Stat M, Koenders A, Huggett MJ 2019. Global networks of Symbiodinium-bacteria within the coral holobiont. Microb. Ecol. 77:3794–807
    [Google Scholar]
  69. 69. 
    Matthews JL, Raina J, Kahlke T, Seymour JR, van Oppen MJH, Suggett DJ 2020. Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks. Environ. Microbiol. 22:51675–87
    [Google Scholar]
  70. 70. 
    Frommlet JC, Sousa ML, Alves A, Vieira SI, Suggett DJ, Serôdio J 2015. Coral symbiotic algae calcify ex hospite in partnership with bacteria. PNAS 112:196158–63
    [Google Scholar]
  71. 71. 
    Leite D, Salles JF, Calderon EN, Castro CB, Bianchini A et al. 2018. Coral bacterial-core abundance and network complexity as proxies for anthropogenic pollution. Front. Microbiol. 9:833
    [Google Scholar]
  72. 72. 
    Wear SL, Thurber RV. 2015. Sewage pollution: Mitigation is key for coral reef stewardship. Ann. N.Y. Acad. Sci. 1355:115–30
    [Google Scholar]
  73. 73. 
    Weis VM. 2008. Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis. J. Exp. Biol. 211:3059–66
    [Google Scholar]
  74. 74. 
    Jain RK, Kapur M, Labana S, Lal B, Sarma PM et al. 2005. Microbial diversity: application of microorganisms for the biodegradation of xenobiotics. Curr. Sci. 89:1101–12
    [Google Scholar]
  75. 75. 
    Cabiscol E, Tamarit J, Ros J 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. 313–8
  76. 76. 
    Gegner HM, Rädecker N, Ochsenkühn M, Barreto MM, Ziegler M et al. 2019. High levels of floridoside at high salinity link osmoadaptation with bleaching susceptibility in the cnidarian-algal endosymbiosis. Biol. Open. 8:12bio045591
    [Google Scholar]
  77. 77. 
    Oakley CA, Davy SK. 2018. Cell biology of coral bleaching. Coral Bleaching: Patterns Processes, Causes and Consequences MJH van Oppen, JM Lough 189–211 Ecol. Stud. 233 Cham, Switz: Springer Nat. , 1st ed..
    [Google Scholar]
  78. 78. 
    Lesser MP. 1997. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:3187–92
    [Google Scholar]
  79. 79. 
    Diaz JM, Hansel CM, Apprill A, Brighi C, Zhang T et al. 2016. Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat. Commun. 7:13801
    [Google Scholar]
  80. 80. 
    Ochsenkühn MA, Röthig T, D'Angelo C, Wiedenmann J, Voolstra CR 2017. The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci. Adv. 3:8e1602047
    [Google Scholar]
  81. 81. 
    Gegner HM, Ziegler M, Rädecker N, Buitrago-López C, Aranda M, Voolstra CR 2017. High salinity conveys thermotolerance in the coral model Aiptasia. Biol. Open 6:121943–48
    [Google Scholar]
  82. 82. 
    Ngugi DK, Ziegler M, Duarte CM, Voolstra CR 2020. Genomic blueprint of glycine betaine metabolism in coral metaorganisms and their contribution to genomic blueprint of glycine betaine. iScience 23:5101120
    [Google Scholar]
  83. 83. 
    Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI 2007. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 1767:414–21
    [Google Scholar]
  84. 84. 
    Bailey S, Grossman A. 2008. Photoprotection in cyanobacteria: regulation of light harvesting. Photochem. Photobiol. 84:61410–20
    [Google Scholar]
  85. 85. 
    Dunlap WC, Shick JM. 1998. Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J. Phycol. 34:3418–30
    [Google Scholar]
  86. 86. 
    Banaszak AT, LaJeunesse TC, Trench RK 2000. The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 249:2219–33
    [Google Scholar]
  87. 87. 
    Kirilovsky D, Kerfeld CA. 2012. The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim. Biophys. Acta 1817:1158–66
    [Google Scholar]
  88. 88. 
    Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ 2010. PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar. Ecol. Prog. Ser. 406:57–70
    [Google Scholar]
  89. 89. 
    Osman EO, Suggett DJ, Voolstra CR, Pettay DT, Clark DR et al. 2020. Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities. Microbiome 8:8
    [Google Scholar]
  90. 90. 
    Yost DM, Jones RJ, Mitchelmore CL 2010. Alterations in dimethylsulfoniopropionate (DMSP) levels in the coral Montastraea franksi in response to copper exposure. Aquat. Toxicol. 98:4367–73
    [Google Scholar]
  91. 91. 
    Sunda W, Kieber DJ, Kiene RP, Huntsman S 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–20
    [Google Scholar]
  92. 92. 
    Ritchie KB. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322:1–14
    [Google Scholar]
  93. 93. 
    Kvennefors ECE, Sampayo E, Kerr C, Vieira G, Roff G, Barnes AC 2012. Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb. Ecol. 63:3605–18
    [Google Scholar]
  94. 94. 
    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 7:5980–90
    [Google Scholar]
  95. 95. 
    Raina JB, Dinsdale EA, Willis BL, Bourne DG 2010. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations. Trends Microbiol 18:3101–8
    [Google Scholar]
  96. 96. 
    Raina JB, Tapiolas D, Motti CA, Foret S, Seemann T et al. 2016. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals. PeerJ 2016. 4:e2275
    [Google Scholar]
  97. 97. 
    Garren M, Son K, Raina JB, Rusconi R, Menolascina F et al. 2014. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J 8:5999–1007
    [Google Scholar]
  98. 98. 
    Sharp KH, Ritchie KB. 2012. Multi-partner interactions in corals in the face of climate change. Biol. Bull. 223:66–77
    [Google Scholar]
  99. 99. 
    Tait K, Hutchison Z, Thompson FL, Munn CB 2010. Quorum sensing signal production and inhibition by coral-associated vibrios. Environ. Microbiol. Rep. 2:1145–50
    [Google Scholar]
  100. 100. 
    Zimmer BL, May AL, Bhedi CD, Dearth SP, Prevatte CW et al. 2014. Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLOS ONE 9:9e108541
    [Google Scholar]
  101. 101. 
    Certner RH, Vollmer SV. 2015. Evidence for autoinduction and quorum sensing in white band disease-causing microbes on Acropora cervicornis. Sci. Rep 5:11134
    [Google Scholar]
  102. 102. 
    Zhou J, Lin ZJ, Cai ZH, Zeng YH, Zhu JM, Du XP 2020. Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching. Environ. Microbiol. 22:51944–62
    [Google Scholar]
  103. 103. 
    Modolon F, Barno AR, Villela HDM, Peixoto RS 2020. Ecological and biotechnological importance of secondary metabolites produced by coral-associated bacteria. J. Appl. Microbiol. 129:61441–57
    [Google Scholar]
  104. 104. 
    Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML et al. 2013. Bacteriophage adhering to mucus provide a non-host-derived immunity. PNAS 110:2610771–76
    [Google Scholar]
  105. 105. 
    Efrony R, Loya Y, Bacharach E, Rosenberg E 2007. Phage therapy of coral disease. Coral Reefs 26:17–13
    [Google Scholar]
  106. 106. 
    Efrony R, Atad I, Rosenberg E 2009. Phage therapy of coral white plague disease: properties of phage BA3. Curr. Microbiol. 58:2139–45
    [Google Scholar]
  107. 107. 
    Welsh RM, Rosales SM, Zaneveld JR, Payet JP, McMinds R et al. 2017. Alien versus predator: Bacterial challenge alters coral microbiomes unless controlled by Halobacteriovorax predators. PeerJ 5:e3315
    [Google Scholar]
  108. 108. 
    Pernthaler J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3:537–47
    [Google Scholar]
  109. 109. 
    Williams HN, Lymperopoulou DS, Athar R, Chauhan A, Dickerson TL et al. 2015. Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality. ISME J491–99
    [Google Scholar]
  110. 110. 
    Welsh RM, Zaneveld JR, Rosales SM, Payet JP, Burkepile DE, Thurber RV 2016. Bacterial predation in a marine host-associated microbiome. ISME J 10:1540–44
    [Google Scholar]
  111. 111. 
    Nitschke MR, Davy SK, Ward S 2016. Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs 35:1335–44
    [Google Scholar]
  112. 112. 
    Leite D, Leão P, Garrido AG, Lins U, Santos HF et al. 2017. Broadcast spawning coral Mussismilia hispida can vertically transfer its associated bacterial core. Front. Microbiol. 8:176
    [Google Scholar]
  113. 113. 
    Apprill A, Marlow HQ, Martindale MQ, Rappé MS 2009. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 3:6685–99
    [Google Scholar]
  114. 114. 
    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 6:4790–801
    [Google Scholar]
  115. 115. 
    Damjanovic K, Menéndez P, Blackall LL, van Oppen MJH 2020. Mixed‐mode bacterial transmission in the common brooding coral Pocillopora acuta. Environ. Microbiol 22:1397–412
    [Google Scholar]
  116. 116. 
    Ceh J, Raina J-B, Soo RM, van Keulen M, Bourne DG 2012. Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef. PLOS ONE 7:5e36920
    [Google Scholar]
  117. 117. 
    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 23:194682–95
    [Google Scholar]
  118. 118. 
    Negri AP, Webster NS, Hill RT, Heyward AJ 2001. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar. Ecol. Prog. Ser. 223:121–31
    [Google Scholar]
  119. 119. 
    Sneed JM, Sharp KH, Ritchie KB, Paul VJ 2014. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. R. Soc. B Biol. Sci. 281:178620133086
    [Google Scholar]
  120. 120. 
    Shikuma NJ, Antoshechkin I, Medeiros JM, Pilhofer M, Newman DK 2016. Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. PNAS 113:3610097–102
    [Google Scholar]
  121. 121. 
    Beckmann M, Harder T, Qian P-Y 1999. Induction of larval attachment and metamorphosis in the serpulid polychaete Hydroides elegans by dissolved free amino acids: mode of action in laboratory bioassays. Mar. Ecol. Prog. Ser. 190:167–78
    [Google Scholar]
  122. 122. 
    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 346:143–52
    [Google Scholar]
  123. 123. 
    Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C 2015. Nitrogen cycling in corals: The key to understanding holobiont functioning. Trends Microbiol 23:8490–97
    [Google Scholar]
  124. 124. 
    Wiedenmann J, D'Angelo C, Smith EG, Hunt AN, Legiret FE et al. 2013. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3:2160–64
    [Google Scholar]
  125. 125. 
    Jaspers C, Fraune S, Arnold AE, Miller DJ, Bosch TCG, Voolstra CR 2019. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. Zoology 133:81–87
    [Google Scholar]
  126. 126. 
    Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T 2010. Wolbachia as a bacteriocyte-associated nutritional mutualist. PNAS 107:2769–74
    [Google Scholar]
  127. 127. 
    Wada N, Ishimochi M, Matsui T, Pollock FJ, Tang SL et al. 2019. Characterization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. Sci. Rep 9:14662
    [Google Scholar]
  128. 128. 
    Login FH, Balmand S, Vallier A, Vincent-Monégat C, Vigneron A et al. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334:362–65
    [Google Scholar]
  129. 129. 
    Jernigan KK, Bordenstein SR. 2015. Tandem-repeat protein domains across the tree of life. PeerJ 3:e732
    [Google Scholar]
  130. 130. 
    Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS 2012. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. PNAS 109:271878–87
    [Google Scholar]
  131. 131. 
    Nguyen MTHD, Liu M, Thomas T 2014. Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol. Biol. Evol. 23:61635–45
    [Google Scholar]
  132. 132. 
    Reynolds D, Thomas T. 2016. Evolution and function of eukaryotic-like proteins from sponge symbionts. Mol. Ecol. 25:5242–53
    [Google Scholar]
  133. 133. 
    Al-Khodor S, Price CT, Habyarimana F, Kalia A, Kwaik YA 2008. A Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol. Microbiol. 70:4908–23
    [Google Scholar]
  134. 134. 
    Habyarimana F, Al-Khodor S, Kalia A, Graham JE, Price CT et al. 2008. Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages. Environ. Microbiol. 10:61460–74
    [Google Scholar]
  135. 135. 
    Ogawa M, Bisson LF, García-Martínez T, Mauricio JC, Moreno-García J 2019. New insights on yeast and filamentous fungus adhesion in a natural co-immobilization system: proposed advances and applications in wine industry. Appl. Microbiol. Biotechnol. 103:124723–31
    [Google Scholar]
  136. 136. 
    Efremenko EN, Nikolskaya AB, Lyagin IV, Senko OV, Makhlis TA et al. 2012. Production of biofuels from pretreated microalgae biomass by anaerobic fermentation with immobilized Clostridium acetobutylicum cells. Bioresour. Technol. 114:342–48
    [Google Scholar]
  137. 137. 
    Bouabidi ZB, El-Naas MH, Zhang Z 2019. Immobilization of microbial cells for the biotreatment of wastewater: a review. Environ. Chem. Lett. 17:1241–57
    [Google Scholar]
  138. 138. 
    Sun X, Meng J, Huo S, Zhu J, Zheng S 2020. Remediation of heavy metal pollution in soil by microbial immobilization with carbon microspheres. Int. J. Environ. Sci. Dev. 11:143–47
    [Google Scholar]
  139. 139. 
    Sweet M, Ramsey A, Bulling M 2017. Designer reefs and coral probiotics: Great concepts but are they good practice. Biodiversity 18:119–22
    [Google Scholar]
  140. 140. 
    Willaert R. 2007. Cell immobilization and its applications in biotechnology: current trends and future prospects. Fermentation Microbiology and Biotechnology EMT El-Masi, CFA Bryce, AL Demain, AR Allman 289–362 Boca Raton, FL: CRC Press
    [Google Scholar]
  141. 141. 
    Nunes GS, Marty J-L. 2006. Immobilization of enzymes on electrodes. Immobilization of Enzymes and Cells JM Guisan 239–50 Cham, Switz: Springer Nat.
    [Google Scholar]
  142. 142. 
    Zhang L-S, Wu W, Wang J 2007. Immobilization of activated sludge using improved polyvinyl alcohol (PVA) gel. J. Environ. Sci. 19:111293–97
    [Google Scholar]
  143. 143. 
    Mozes N, Marchal F, Hermesse MP, Van Haecht JL, Reuliaux L et al. 1987. Immobilization of microorganisms by adhesion: interplay of electrostatic and nonelectrostatic interactions. Biotechnol. Bioeng. 30:3439–50
    [Google Scholar]
  144. 144. 
    Declerck SAJ, Papakostas S. 2017. Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications. Hydrobiologia 796:131–44
    [Google Scholar]
  145. 145. 
    Rudtanatip T, Boonsri B, Praiboon J, Wongprasert K 2019. Bioencapsulation efficacy of sulfated galactans in adult Artemia salina for enhancing immunity in shrimp Litopenaeus vannamei. Fish Shellfish Immunol 94:90–98
    [Google Scholar]
  146. 146. 
    Bengtson DA. 2003. Status of marine aquaculture in relation to live prey: past, present and future. Live Feed in Marine Aquaculture JG Støttrup, LA McEvoy 1–16 Oxford, UK: Blackwell
    [Google Scholar]
  147. 147. 
    Melo-Bolívar JF, Ruiz-Pardo RY, Hume ME, Sidjabat HE, Villamil-Diaz LM 2020. Probiotics for cultured freshwater fish. Microbiol. Aust. 41:2105–8
    [Google Scholar]
  148. 148. 
    Craggs J, Guest JR, Davis M, Simmons J, Dashti E, Sweet M 2017. Inducing broadcast coral spawning ex situ: closed system mesocosm design and husbandry protocol. Ecol. Evol. 7:11066–78
    [Google Scholar]
  149. 149. 
    Gibbin E, Gavish A, Domart-Coulon I, Kramarsky-Winter E, Shapiro O et al. 2018. Using NanoSIMS coupled with microfluidics to visualize the early stages of coral infection by Vibrio coralliilyticus. BMC Microbiol 18:39
    [Google Scholar]
  150. 150. 
    Wein T, Dagan T, Fraune S, Bosch TCG, Reusch TBH, Hülter NF 2018. Carrying capacity and colonization dynamics of Curvibacter in the Hydra host habitat. Front. Microbiol. 9:443
    [Google Scholar]
  151. 151. 
    Burriesci MS, Raab TK, Pringle JR 2012. Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J. Exp. Biol. 215:193467–77
    [Google Scholar]
  152. 152. 
    Davy SK, Allemand D, Weis VM 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:2229–61
    [Google Scholar]
  153. 153. 
    Tremblay P, Fine M, Maguer J-F, Grover R, Ferrier-Pagès C 2013. Photosynthate translocation increases in response to low seawater pH in a coral-dinoflagellate symbiosis. Biogeosciences 10:63997–4007
    [Google Scholar]
  154. 154. 
    Olson ND, Ainsworth TD, Gates RD, Takabayashi M 2009. Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 371:2140–46
    [Google Scholar]
  155. 155. 
    Lema KA, Willis BL, Bourneb DG 2012. Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 78:93136–44
    [Google Scholar]
  156. 156. 
    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. 12:2541–56
    [Google Scholar]
  157. 157. 
    Vanwonterghem I, Webster NS. 2020. Coral reef microorganisms in a changing climate. iScience 23:4100972
    [Google Scholar]
  158. 158. 
    Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI et al. 2004. Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl. Environ. Microbiol. 70:21213–21
    [Google Scholar]
  159. 159. 
    Heyward AJ, Negri AP. 2010. Plasticity of larval pre-competency in response to temperature: Observations on multiple broadcast spawning coral species. Coral Reefs 29:3631–36
    [Google Scholar]
  160. 160. 
    Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, Newman DK 2014. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343:6170529–33
    [Google Scholar]
  161. 161. 
    Gao Y, Wang X, Li J, Lee CT, Ong PY et al. 2020. Effect of aquaculture salinity on nitrification and microbial community in moving bed bioreactors with immobilized microbial granules. Bioresour. Technol. 297:122427
    [Google Scholar]
  162. 162. 
    Oh YS, Maeng J, Kim SJ 2000. Use of microorganism-immobilized polyurethane foams to absorb and degrade oil on water surface. Appl. Microbiol. Biotechnol. 54:3418–23
    [Google Scholar]
  163. 163. 
    Qiao K, Tian W, Bai J, Wang L, Zhao J et al. 2020. Removal of high-molecular-weight polycyclic aromatic hydrocarbons by a microbial consortium immobilized in magnetic floating biochar gel beads. Mar. Pollut. Bull. 159:111489
    [Google Scholar]
  164. 164. 
    Hai N, Buller N, Fotedar R 2010. Encapsulation capacity of Artemia nauplii with customized probiotics for use in the cultivation of western king prawns (Penaeus latisulcatus Kishinouye, 1896). Aquacult. Res. 41:6893–903
    [Google Scholar]
  165. 165. 
    Sun YZ, Yang HL, Huang KP, Ye JD, Zhang CX 2013. Application of autochthonous Bacillus bioencapsulated in copepod to grouper Epinephelus coioides larvae. Aquaculture 392:44–50
    [Google Scholar]
  166. 166. 
    Jahari MA, Mustafa S, Abd Manap Y, udie Lamasudin D, Roslan MAH 2019. Encapsulation of Lactobacillus plantarum with mannan and sodium alginate improves its cell production. J. Biochem. Microbiol. Biotechnol. 7:117–22
    [Google Scholar]
  167. 167. 
    Rosas‐Ledesma P, León‐Rubio JM, Alarcón FJ, Moriñigo MA, Balebona MC 2012. Calcium alginate capsules for oral administration of fish probiotic bacteria: assessment of optimal conditions for encapsulation. Aquacult. Res. 43:1106–16
    [Google Scholar]
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