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 ( a) promoting coral nutrition and growth, ( b) mitigating stress and impacts of toxic compounds, ( c) deterring pathogens, and ( d) 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 mechanisms that 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. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 9 is February 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Original language | English (US) |
---|---|
Pages (from-to) | 265-288 |
Number of pages | 24 |
Journal | Annual Review of Animal Biosciences |
Volume | 9 |
Issue number | 1 |
DOIs | |
State | Published - Dec 15 2020 |
Bibliographical note
Publisher Copyright:© 2021 Annual Reviews Inc.. All rights reserved.
Export Date: 5 May 2021
Correspondence Address: Peixoto, R.S.; Laboratory of Molecular Microbial Ecology, Rio de Janeiro, Brazil; email: raquelpeixoto@micro.ufrj.br
References: Bosch, TCG, McFall-Ngai, MJ., Metaorganisms as the new frontier (2011) Zoology, 114, pp. 185-190; Bang, C, Dagan, T, Deines, P, Dubilier, N, Duschl, WJ, Metaorganisms in extreme environments: Do microbes play a role in organismal adaptation? (2018) Zoology, 127, pp. 1-19; LaJeunesse, TC, Parkinson, JE, Gabrielson, PW, Jeong, HJ, Reimer, JD, Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts (2018) Curr. Biol, 28, pp. 2570-2580. , e6; Muscatine, L., The role of symbiotic algae in carbon and energy flux in reef corals (1990) Ecosystems of the World: Coral Reefs, pp. 75-87. , ed. Z Dubinsky, New York: Elsevier; Pogoreutz, C, Voolstra, CR, Rädecker, N, Weis, V, Cardenas, A, Raina, J-B., The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes (2020) Cellular Dialogues in the Holobiont, , ed. T Bosch, M Hadfield. Boca Raton, FL: CRC Press; Hughes, TP, Anderson, KD, Connolly, SR, Heron, SF, Kerry, JT, Spatial and temporal patterns of mass bleaching of corals in the Anthropocene (2018) Science, 359 (6371), pp. 80-83; Duarte, GAS, Villela, HDM, Deocleciano, M, Silva, D, Barno, A, Heat waves are a major threat to turbid coral reefs in Brazil (2020) Front. Mar. Sci, 7, p. 179; Zaneveld, JR, Burkepile, DE, Shantz, AA, Pritchard, CE, McMinds, R, Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales (2016) Nat. Commun, 7, p. 11833; Sweet, M, Burian, A, Fifer, J, Bulling, M, Elliott, D, Raymundo, L., Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease (2019) Microbiome, 7, p. 139; Putnam, HM, Barott, KL, Ainsworth, TD, Gates, RD., The vulnerability and resilience of reefbuilding corals (2017) Curr. Biol, 27 (11), pp. R528-R540; O?Brien, PA, Morrow, KM, Willis, BL, Bourne, DG., Implications of ocean acidification for marine microorganisms from the free-living to the host-Associated (2016) Front. Mar. Sci, 3, p. 47; Peixoto, R, Rosado, PM, de Assis Leite, DC, Rosado, AS, Bourne, DG., Beneficial Microorganisms for Corals (BMC): proposed mechanisms for coral health and resilience (2017) Front. Microbiol, 8, p. 341; Neave, MJ, Rachmawati, R, Xun, L, Michell, CT, Bourne, DG, Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales (2017) ISME J, 11, pp. 186-200; Rosenberg, E, Koren, O, Reshef, L, Efrony, R, Zilber-Rosenberg, I., The role of microorganisms in coral health, disease and evolution (2007) Nat. Rev. Microbiol, 5, pp. 355-362; Bourne, DG, Morrow, KM, Webster, NS., Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems (2016) Annu. Rev. Microbiol, 70, pp. 317-340; Sweet, MJ, Bulling, MT., On the importance of the microbiome and pathobiome in coral health and disease (2017) Front. Mar. Sci, 4, p. 9; Ziegler, M, Seneca, FO, Yum, LK, Palumbi, SR, Voolstra, CR., Bacterial community dynamics are linked to patterns of coral heat tolerance (2017) Nat. Commun, 8, p. 14213; Ziegler, M, Grupstra, CGB, Barreto, MM, Eaton, M, BaOmar, J, Coral bacterial community structure responds to environmental change in a host-specific manner (2019) Nat. Commun, 10, p. 3092; Hume, BCC, Mejia-Restrepo, A, Voolstra, CR, Berumen, ML., Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations (2020) Coral Reefs, 39, pp. 583-601; Röthig, T, Ochsenköhn, MA, Roik, A, Van DerMerwe, R, Voolstra, CR., Long-Term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome (2016) Mol. Ecol, 25 (6), pp. 1308-1323; Voolstra, CR, Ziegler, M., Adapting with microbial help: Microbiome flexibility facilitates rapid responses to environmental change (2020) BioEssays, 42 (7), p. 2000004; Reshef, L, Koren, O, Loya, Y, Zilber-Rosenberg, I, Rosenberg, E., The coral probiotic hypothesis (2006) Environ.Microbiol, 8 (12), pp. 2068-2073; Pollock, FJ, Morris, PJ, Willis, BL, Bourne, DG., The urgent need for robust coral disease diagnostics (2011) PLOS Pathog, 7 (10), p. e1002183; Pollock, FJ, Wilson, B, Johnson, WR, Morris, PJ, Willis, BL, Bourne, DG., Phylogeny of the coral pathogen Vibrio coralliilyticus (2010) Environ.Microbiol. Rep, 2 (1), pp. 172-178; Ushijima, B, Videau, P, Burger, AH, Shore-Maggio, A, Runyon, CM, Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome (2014) Appl. Environ.Microbiol, 80 (7), pp. 2102-2109; Sutherland, KP, Berry, B, Park, A, Kemp, DW, Kemp, KM, Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994?2014 (2016) Philos. Trans. R. Soc. B, 371 (1689), p. 20150205; Beurmann, S, Ushijima, B, Videau, P, Svoboda, CM, Smith, AM, Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata (2017) PLOS One, 12 (11), p. e0188319; Séré, MG, Tortosa, P, Chabanet, P, Quod, JP, Sweet, MJ, Schleyer, MH., Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean (2015) Mol. Ecol, 24 (17), pp. 4570-4581; Kushmaro, A, Banin, E, Loya, Y, Stackebrandt, E, Rosenberg, E., Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica (2001) Int. J. Syst. Evol.Microbiol, 51 (4), pp. 1383-1388; Thompson, FL, Barash, Y, Sawabe, T, Sharon, G, Swings, J, Rosenberg, E., Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef (2006) Int. J. Syst. Evol. Microbiol, 56 (2), pp. 365-368; Bourne, DG, Garren, M, Work, TM, Rosenberg, E, Smith, GW, Harvell, CD., Microbial disease and the coral holobiont (2009) Trends Microbiol, 17 (12), pp. 554-562; Mera, H, Bourne, DG., Disentangling causation: complex roles of coral-Associated microorganisms in disease (2018) Environ.Microbiol, 20 (2), pp. 431-449; Saharan, BS, Nehra, V., Plant growth promoting rhizobacteria: A critical review (2011) Life Sci. Med. Res, 21, pp. 1-30; Woodhams, DC, Bletz, M, Kueneman, J, McKenzie, V., Managing amphibian disease with skin microbiota (2016) Trends Microbiol, 24 (3), pp. 161-164; Alberoni, D, Gagg?a, F, Baffoni, L, Di Gioia, D., Beneficial microorganisms for honey bees: problems and progresses (2016) Appl.Microbiol. Biotechnol, 100 (22), pp. 9469-9482; West, AG, Waite, DW, Deines, P, Bourne, DG, Digby, A, Themicrobiome in threatened species conservation (2019) Biol. Conserv, 229, pp. 85-98; McKenzie, VJ, Kueneman, JG, Harris, RN., Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine (2018) Ann. N.Y. Acad. Sci, 1429 (1), pp. 18-30; Cheng, TL, Mayberry, H, McGuire, LP, Hoyt, JR, Langwig, KE, Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome (2017) J. Appl. Ecol, 54 (3), pp. 701-708; Rosado, P, Leite, DCA, Duarte, GAS, Chaloub, RM, Jospin, G, Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation (2019) ISME J, 13, pp. 921-936; Hoyt, JR, Langwig, KE, White, JP, Kaarakka, HM, Redell, JA, Field trial of a probiotic bacteria to protect bats from white-nose syndrome (2019) Sci. Rep, 9, p. 9158; Teplitski, M, Ritchie, K., How feasible is the biological control of coral diseases? (2009) Trends Ecol. Evol, 24 (7), pp. 378-385; Peixoto, RS, Sweet, M, Bourne, DG., Customized medicine for corals (2019) Front. Mar. Sci, 6, p. 686; Santos, HF, Duarte, GAS, da Costa Rachid, CT, Chaloub, RM, Calderon, EN, Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota (2015) Sci. Rep, 5, p. 18268; Morgans, CA, Hung, JY, Bourne, DG, Quigley, KM., Symbiodiniaceae probiotics for use in bleaching recovery (2020) Restor. Ecol, 28 (2), pp. 282-288; Damjanovic, K, van, OppenMJH, Menéndez, P, Blackall, LL., Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea (2019) Front. Microbiol, 10, p. 1702; Dunphy, CM, Gouhier, TC, Chu, ND, Vollmer, SV., Structure and stability of the coral microbiome in space and time (2019) Sci. Rep, 9, p. 6785; Mathur, V, del Campo, J, Kolisko, M, Keeling, PJ., Global diversity and distribution of close relatives of apicomplexan parasites (2018) Environ.Microbiol, 20 (8), pp. 2824-2833; Kwong, WK, del Campo, J, Mathur, V, Vermeij, MJA, Keeling, PJ., A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes (2019) Nature, 568 (7750), pp. 103-107; McFadden, GI, Reith, ME, Munholland, J, Lang-Unnasch, N., Plastid in human parasites (1996) Nature, 381 (6582), p. 482; Vohsen, SA, Anderson, KE, Gade, AM, Gruber-Vodicka, HR, Dannenberg, RP, Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans (2020) Microbiome, 8, p. 34; Robbins, SJ, Singleton, CM, Chan, CX, Messer, LF, Geers, AU, A genomic view of the reefbuilding coral Porites lutea and its microbial symbionts (2019) Nat.Microbiol, 4 (12), pp. 2090-2100; Smith, SM., (2018) Complementarity in the coral holobiont: A genomic analysis of bacterial isolates of Orbicella faveolata and Symbiodinium spp, , https://etda.libraries.psu.edu/files/final_submissions/17896, Masters Thesis, Coll. Sci., Pa. StateUniv., State Park, PA; Agostini, S, Suzuki, Y, Higuchi, T, Casareto, BE, Yoshinaga, K, Biological and chemical characteristics of the coral gastric cavity (2012) Coral Reefs, 31, pp. 147-156; Hopkinson, BM, Morel, FMM., The role of siderophores in iron acquisition by photosynthetic marine microorganisms (2009) Biometals, 22, pp. 659-669; Reich, HG, Rodriguez, IB, LaJeunesse, TC, Ho, T-Y., Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae (2020) Coral Reefs, 39, pp. 915-927; Shick, JM, Iglic, K, Wells, ML, Trick, CG, Doyle, J, Dunlap, WC., Responses to iron limitation in two colonies of Stylophora pistillata exposed to high temperature: implications for coral bleaching (2011) Limnol. Oceanogr, 56 (3), pp. 813-828; Schalk, IJ, Hannauer, M, Braud, A., New roles for bacterial siderophores in metal transport and tolerance (2011) Environ.Microbiol, 13 (11), pp. 2844-2854; Barnes, DJ., Coral skeletons: An explanation of their growth and structure (1970) Science, 170 (3964), pp. 1305-1308; Al-Horani, F, Al-Moghrabi, SM, de Beer, D., The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis (2003) Mar. Biol, 142, pp. 419-426; Biscéré, T, Ferrier-Pagès, C, Grover, R, Gilbert, A, Rottier, C, Enhancement of coral calcification via the interplay of nickel and urease (2018) Aquat. Toxicol, 200, pp. 247-256; Barnes, DJ, Crossland, CJ., Urease activity in the staghorn coral, Acropora acuminata (1976) Comp. Biochem. Physiol. B, 55 (3), pp. 371-376; Villela, HDM, Vilela, CLS, Assis, JM, Varona, N, Burke, C, Prospecting microbial strains for bioremediation and probiotics development for metaorganism research and preservation (2019) J. Vis. Exp, 152, p. e60238; Domart-Coulon, IJ, Sinclair, CS, Hill, RT, Tambutté, S, Puverel, S, Ostrander, GK., A basidiomycete isolated from the skeleton of Pocillopora damicornis (Scleractinia) selectively stimulates short-Term survival of coral skeletogenic cells (2004) Mar. Biol, 144 (3), pp. 583-592; Pernice, M, Raina, J-B, Rädecker, N, Cárdenas, A, Pogoreutz, C, Voolstra, CR., Down to the bone: The role of overlooked endolithic microbiomes in reef coral health (2019) ISME J, 14, pp. 325-334; Fine, M, Loya, Y., Endolithic algae: An alternative source of photoassimilates during coral bleaching (2002) Proc. Biol. Sci, 269 (1497), pp. 1205-1210; Jeong, HJ, Du Yoo, Y, Kang, NS, Lim, AS, Seong, KA, Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium (2012) PNAS, 109 (31), pp. 12604-12609; Lawson, CA, Raina, J-B, Kahlke, T, Seymour, JR, Suggett, DJ., Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium (2018) Environ.Microbiol. Rep, 10 (1), pp. 7-11; Bernasconi, R, Stat, M, Koenders, A, Huggett, MJ., Global networks of Symbiodinium-bacteria within the coral holobiont (2019) Microb. Ecol, 77 (3), pp. 794-807; Matthews, JL, Raina, J, Kahlke, T, Seymour, JR, van Oppen, MJH, Suggett, DJ., Symbiodiniaceaebacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks (2020) Environ.Microbiol, 22 (5), pp. 1675-1687; Frommlet, JC, Sousa, ML, Alves, A, Vieira, SI, Suggett, DJ, Serôdio, J., Coral symbiotic algae calcify ex hospite in partnership with bacteria (2015) PNAS, 112 (19), pp. 6158-6163; Leite, D, Salles, JF, Calderon, EN, Castro, CB, Bianchini, A, Coral bacterial-core abundance and network complexity as proxies for anthropogenic pollution (2018) Front. Microbiol, 9, p. 833; Wear, SL, Thurber, RV., Sewage pollution: Mitigation is key for coral reef stewardship (2015) Ann. N.Y. Acad. Sci, 1355 (1), pp. 15-30; Weis, VM., Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis (2008) J. Exp. Biol, 211, pp. 3059-3066; Jain, RK, Kapur, M, Labana, S, Lal, B, Sarma, PM, Microbial diversity: Application of microorganisms for the biodegradation of xenobiotics (2005) Curr. Sci, 89 (1), pp. 101-112; Cabiscol, E, Tamarit, J, Ros, J., (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species, 3 (1), pp. 3-8; Gegner, HM, Rädecker, N, Ochsenköhn, M, Barreto, MM, Ziegler, M, High levels of floridoside at high salinity link osmoadaptation with bleaching susceptibility in the cnidarian-Algal endosymbiosis (2019) Biol. Open, 8 (12), p. bio045591; Oakley, CA, Davy, SK., Cell biology of coral bleaching (2018) Coral Bleaching: Patterns Processes, Causes and Consequences, pp. 189-211. , ed. MJH van Oppen, JM Lough, Ecol. Stud. 233. Cham, Switz.: Springer Nat. 1st ed; Lesser, MP., Oxidative stress causes coral bleaching during exposure to elevated temperatures (1997) Coral Reefs, 16 (3), pp. 187-192; Diaz, JM, Hansel, CM, Apprill, A, Brighi, C, Zhang, T, Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event (2016) Nat. Commun, 7, p. 13801; Ochsenköhn, MA, Röthig, T, D?Angelo, C, Wiedenmann, J, Voolstra, CR., The role of floridoside in osmoadaptation of coral-Associated algal endosymbionts to high-salinity conditions. Sci. Adv. 3(8):e1602047 Gegner HM, Ziegler M, Rädecker N, Buitrago-López C, Aranda M, Voolstra CR. 2017. High salinity conveys thermotolerance in the coral model Aiptasia (2017), pp. 1943-1948. , Biol. Open 6(12); Ngugi, DK, Ziegler, M, Duarte, CM, Voolstra, CR., Genomic blueprint of glycine betaine metabolism in coral metaorganisms and their contribution to genomic blueprint of glycine betaine (2020) iScience, 23 (5), p. 101120; Murata, N, Takahashi, S, Nishiyama, Y, Allakhverdiev, SI., Photoinhibition of photosystem II under environmental stress (2007) Biochim. Biophys. Acta, 1767, pp. 414-421; Bailey, S, Grossman, A., Photoprotection in cyanobacteria: regulation of light harvesting (2008) Photochem. Photobiol, 84 (6), pp. 1410-1420; Dunlap, WC, Shick, JM., Ultraviolet radiation-Absorbing mycosporine-like amino acids in coral reef organisms: A biochemical and environmental perspective (1998) J. Phycol, 34 (3), pp. 418-430; Banaszak, AT, LaJeunesse, TC, Trench, RK., The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates (2000) J. Exp. Mar. Biol. Ecol, 249 (2), pp. 219-233; Kirilovsky, D, Kerfeld, CA., The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria (2012) Biochim. Biophys. Acta, 1817 (1), pp. 158-166; Ragni, M, Airs, RL, Hennige, SJ, Suggett, DJ, Warner, ME, Geider, RJ., PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes (2010) Mar. Ecol. Prog. Ser, 406, pp. 57-70; Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities (2020) Microbiome, 8, p. 8; Yost, DM, Jones, RJ, Mitchelmore, CL., Alterations in dimethylsulfoniopropionate (DMSP) levels in the coral Montastraea franksi in response to copper exposure (2010) Aquat. Toxicol, 98 (4), pp. 367-373; Sunda, W, Kieber, DJ, Kiene, RP, Huntsman, S., An antioxidant function for DMSP and DMS in marine algae (2002) Nature, 418, pp. 317-320; Ritchie, KB., Regulation of microbial populations by coral surface mucus and mucus-Associated bacteria (2006) Mar. Ecol. Prog. Ser, 322, pp. 1-14; Kvennefors, ECE, Sampayo, E, Kerr, C, Vieira, G, Roff, G, Barnes, AC., Regulation of bacterial communities through antimicrobial activity by the coral holobiont (2012) Microb. Ecol, 63 (3), pp. 605-618; Krediet, CJ, Ritchie, KB, Alagely, A, Teplitski, M., Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen (2013) ISME J, 7 (5), pp. 980-990; Raina, JB, Dinsdale, EA, Willis, BL, Bourne, DG., Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? (2010) Trends Microbiol, 18 (3), pp. 101-108; Raina, JB, Tapiolas, D, Motti, CA, Foret, S, Seemann, T, Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals (2016) PeerJ, 2016 (4), p. e2275; Garren, M, Son, K, Raina, JB, Rusconi, R, Menolascina, F, A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals (2014) ISME J, 8 (5), pp. 999-1007; Sharp, KH, Ritchie, KB., Multi-partner interactions in corals in the face of climate change (2012) Biol. Bull, 223, pp. 66-77; Tait, K, Hutchison, Z, Thompson, FL, Munn, CB., Quorum sensing signal production and inhibition by coral-Associated vibrios (2010) Environ.Microbiol. Rep, 2 (1), pp. 145-150; Zimmer, BL, May, AL, Bhedi, CD, Dearth, SP, Prevatte, CW, Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer (2014) PLOS ONE, 9 (9), p. e108541; Certner, RH, Vollmer, SV., Evidence for autoinduction and quorum sensing in white band diseasecausing microbes on Acropora cervicornis (2015) Sci. Rep, 5, p. 11134; Zhou, J, Lin, ZJ, Cai, ZH, Zeng, YH, Zhu, JM, Du, XP., Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching (2020) Environ.Microbiol, 22 (5), pp. 1944-1962; Modolon, F, Barno, AR, Villela, HDM, Peixoto, RS., Ecological and biotechnological importance of secondary metabolites produced by coral-Associated bacteria (2020) J. Appl.Microbiol, 129 (6), pp. 1441-1457; Barr, JJ, Auro, R, Furlan, M, Whiteson, KL, Erb, ML, Bacteriophage adhering tomucus provide a non-host-derived immunity (2013) PNAS, 110 (26), pp. 10771-10776; Efrony, R, Loya, Y, Bacharach, E, Rosenberg, E., Phage therapy of coral disease (2007) Coral Reefs, 26 (1), pp. 7-13; Efrony, R, Atad, I, Rosenberg, E., Phage therapy of coral white plague disease: properties of phage BA3 (2009) Curr. Microbiol, 58 (2), pp. 139-145; Welsh, RM, Rosales, SM, Zaneveld, JR, Payet, JP, McMinds, R, Alien versus predator: Bacterial challenge alters coral microbiomes unless controlled by Halobacteriovorax predators (2017) PeerJ, 5, p. e3315; Pernthaler, J., Predation on prokaryotes in the water column and its ecological implications (2005) Nat. Rev. Microbiol, 3, pp. 537-547; Williams, HN, Lymperopoulou, DS, Athar, R, Chauhan, A, Dickerson, TL, Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality (2015) ISME J, 491, p. 99; Welsh, RM, Zaneveld, JR, Rosales, SM, Payet, JP, Burkepile, DE, Thurber, RV., Bacterial predation in a marine host-Associated microbiome (2016) ISME J, 10, pp. 1540-1544; Nitschke, MR, Davy, SK, Ward, S., Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment (2016) Coral Reefs, 35 (1), pp. 335-344; Leite, D, Leão, P, Garrido, AG, Lins, U, Santos, HF, Broadcast spawning coral Mussismilia hispida can vertically transfer its associated bacterial core (2017) Front. Microbiol, 8, p. 176; Apprill, A, Marlow, HQ, Martindale, MQ, Rappé, MS., The onset of microbial associations in the coral Pocillopora meandrina (2009) ISME J, 3 (6), pp. 685-699; Sharp, KH, Distel, D, Paul, VJ., Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides (2012) ISME J, 6 (4), pp. 790-801; Damjanovic, K, Menéndez, P, Blackall, LL, van Oppen, MJH., Mixed-mode bacterial transmission in the common brooding coral Pocillopora acuta (2020) Environ.Microbiol, 22 (1), pp. 397-412; Ceh, J, Raina, J-B, Soo, RM, van Keulen, M, Bourne, DG., Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef (2012) PLOS ONE, 7 (5), p. e36920; Lema, KA, Bourne, DG, Willis, BL., Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora (2014) Mol. Ecol, 23 (19), pp. 4682-4695; Negri, AP, Webster, NS, Hill, RT, Heyward, AJ., Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae (2001) Mar. Ecol. Prog. Ser, 223, pp. 121-131; Sneed, JM, Sharp, KH, Ritchie, KB, Paul, VJ., The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals (2014) Proc. R. Soc. B Biol. Sci, 281 (1786), p. 20133086; Shikuma, NJ, Antoshechkin, I, Medeiros, JM, Pilhofer, M, Newman, DK., Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling (2016) PNAS, 113 (36), pp. 10097-10102; Beckmann, M, Harder, T, Qian, P-Y., Induction of larval attachment and metamorphosis in the serpulid polychaete Hydroides elegans by dissolved free amino acids: mode of action in laboratory bioassays (1999) Mar. Ecol. Prog. Ser, 190, pp. 167-178; Lesser, MP, Falcón, LI, Rodríguez-Román, A, Enríquez, S, Hoegh-Guldberg, O, Iglesias-Prieto, R., Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa (2007) Mar. Ecol. Prog. Ser, 346, pp. 143-152; Rädecker, N, Pogoreutz, C, Voolstra, CR, Wiedenmann, J, Wild, C., Nitrogen cycling in corals: The key to understanding holobiont functioning? (2015) Trends Microbiol, 23 (8), pp. 490-497; Wiedenmann, J, D?Angelo, C, Smith, EG, Hunt, AN, Legiret, FE, Nutrient enrichment can increase the susceptibility of reef corals to bleaching (2013) Nat. Clim. Change, 3 (2), pp. 160-164; Jaspers, C, Fraune, S, Arnold, AE, Miller, DJ, Bosch, TCG, Voolstra, CR., Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches (2019) Zoology, 133, pp. 81-87; Hosokawa, T, Koga, R, Kikuchi, Y, Meng, XY, Fukatsu, T., Wolbachia as a bacteriocyte-Associated nutritional mutualist (2010) PNAS, 107 (2), pp. 769-774; Wada, N, Ishimochi, M, Matsui, T, Pollock, FJ, Tang, SL, Characterization of coral-Associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus (2019) Sci. Rep, 9, p. 14662; Login, FH, Balmand, S, Vallier, A, Vincent-Monégat, C, Vigneron, A, Antimicrobial peptides keep insect endosymbionts under control (2011) Science, 334, pp. 362-365; Jernigan, KK, Bordenstein, SR., Tandem-repeat protein domains across the tree of life (2015) PeerJ, 3, p. e732; Fan, L, Reynolds, D, Liu, M, Stark, M, Kjelleberg, S, Webster, NS., Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts (2012) PNAS, 109 (27), pp. 1878-1887; Nguyen, MTHD, Liu, M, Thomas, T., Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis (2014) Mol. Biol. Evol, 23 (6), pp. 1635-1645; Reynolds, D, Thomas, T., Evolution and function of eukaryotic-like proteins from sponge symbionts (2016) Mol. Ecol, 25, pp. 5242-5253; Al-Khodor, S, Price, CT, Habyarimana, F, Kalia, A, Kwaik, YA., A Dot/Icm-Translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa (2008) Mol. Microbiol, 70 (4), pp. 908-923; Habyarimana, F, Al-Khodor, S, Kalia, A, Graham, JE, Price, CT, Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages (2008) Environ.Microbiol, 10 (6), pp. 1460-1474; Ogawa, M, Bisson, LF, García-Martínez, T, Mauricio, JC, Moreno-García, J., New insights on yeast and filamentous fungus adhesion in a natural co-immobilization system: proposed advances and applications in wine industry (2019) Appl.Microbiol. Biotechnol, 103 (12), pp. 4723-4731; Efremenko, EN, Nikolskaya, AB, Lyagin, IV, Senko, OV, Makhlis, TA, Production of biofuels from pretreated microalgae biomass by anaerobic fermentation with immobilized Clostridium acetobutylicum cells (2012) Bioresour. Technol, 114, pp. 342-348; Bouabidi, ZB, El-Naas, MH, Zhang, Z., Immobilization of microbial cells for the biotreatment of wastewater: A review (2019) Environ. Chem. Lett, 17 (1), pp. 241-257; Sun, X, Meng, J, Huo, S, Zhu, J, Zheng, S., Remediation of heavy metal pollution in soil by microbial immobilization with carbon microspheres (2020) Int. J. Environ. Sci. Dev, 11 (1), pp. 43-47; Sweet, M, Ramsey, A, Bulling, M., Designer reefs and coral probiotics: Great concepts but are they good practice? (2017) Biodiversity, 18 (1), pp. 19-22; Willaert, R., Cell immobilization and its applications in biotechnology: current trends and future prospects (2007) Fermentation Microbiology and Biotechnology, pp. 289-362. , ed.EMT El-Masi, CFA Bryce, AL Demain, AR Allman, Boca Raton, FL: CRC Press; Nunes, GS, Marty, J-L., Immobilization of enzymes on electrodes (2006) Immobilization of Enzymes and Cells, pp. 239-250. , ed. JM Guisan, Cham, Switz.: Springer Nat; Zhang, L-S, Wu, W, Wang, J., Immobilization of activated sludge using improved polyvinyl alcohol (PVA) gel (2007) J. Environ. Sci, 19 (11), pp. 1293-1297; Mozes, N, Marchal, F, Hermesse, MP, Van Haecht, JL, Reuliaux, L, Immobilization of microorganisms by adhesion: interplay of electrostatic and nonelectrostatic interactions (1987) Biotechnol. Bioeng, 30 (3), pp. 439-450; Declerck, SAJ, Papakostas, S., Monogonont rotifers as model systems for the study of microevolutionary adaptation and its eco-evolutionary implications (2017) Hydrobiologia, 796, pp. 131-144; Rudtanatip, T, Boonsri, B, Praiboon, J, Wongprasert, K., Bioencapsulation efficacy of sulfated galactans in adult Artemia salina for enhancing immunity in shrimp Litopenaeus vannamei (2019) Fish Shellfish Immunol, 94, pp. 90-98; Bengtson, DA., Status of marine aquaculture in relation to live prey: past, present and future (2003) Live Feed in Marine Aquaculture, pp. 1-16. , ed. JG Støttrup, LA McEvoy, Oxford, UK: Blackwell; Melo-Bolívar, JF, Ruiz-Pardo, RY, Hume, ME, Sidjabat, HE, Villamil-Diaz, LM., Probiotics for cultured freshwater fish (2020) Microbiol. Aust, 41 (2), pp. 105-108; Craggs, J, Guest, JR, Davis, M, Simmons, J, Dashti, E, Sweet, M., Inducing broadcast coral spawning ex situ: closed system mesocosm design and husbandry protocol (2017) Ecol. Evol, 7, pp. 11066-11078; Gibbin, E, Gavish, A, Domart-Coulon, I, Kramarsky-Winter, E, Shapiro, O, Using NanoSIMS coupled with microfluidics to visualize the early stages of coral infection by Vibrio coralliilyticus (2018) BMC Microbiol, 18, p. 39; Wein, T, Dagan, T, Fraune, S, Bosch, TCG, Reusch, TBH, Hölter, NF., Carrying capacity and colonization dynamics of Curvibacter in the Hydra host habitat (2018) Front. Microbiol, 9, p. 443; Burriesci, MS, Raab, TK, Pringle, JR., Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis (2012) J. Exp. Biol, 215 (19), pp. 3467-3477; Davy, SK, Allemand, D, Weis, VM., Cell biology of cnidarian-dinoflagellate symbiosis (2012) Microbiol. Mol. Biol. Rev, 76 (2), pp. 229-261; Tremblay, P, Fine, M, Maguer, J-F, Grover, R, Ferrier-Pagès, C., Photosynthate translocation increases in response to low seawater pHin a coral-dinoflagellate symbiosis (2013) Biogeosciences, 10 (6), pp. 3997-4007; Olson, ND, Ainsworth, TD, Gates, RD, Takabayashi, M., Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates (2009) J. Exp. Mar. Biol. Ecol, 371 (2), pp. 140-146; Lema, KA, Willis, BL, Bourneb, DG., Corals form characteristic associations with symbiotic nitrogen-fixing bacteria (2012) Appl. Environ.Microbiol, 78 (9), pp. 3136-3144; 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 (2010) Environ.Microbiol, 12 (2), pp. 541-556; Vanwonterghem, I, Webster, NS., Coral reef microorganisms in a changing climate (2020) iScience, 23 (4), p. 100972; Webster, NS, Smith, LD, Heyward, AJ, Watts, JEM, Webb, RI, Metamorphosis of a scleractinian coral in response to microbial biofilms (2004) Appl. Environ.Microbiol, 70 (2), pp. 1213-1221; Heyward, AJ, Negri, AP., Plasticity of larval pre-competency in response to temperature: Observations on multiple broadcast spawning coral species (2010) Coral Reefs, 29 (3), pp. 631-636; Shikuma, NJ, Pilhofer, M, Weiss, GL, Hadfield, MG, Jensen, GJ, Newman, DK., Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures (2014) Science, 343 (6170), pp. 529-533; Gao, Y, Wang, X, Li, J, Lee, CT, Ong, PY, Effect of aquaculture salinity on nitrification and microbial community in moving bed bioreactors with immobilized microbial granules (2020) Bioresour. Technol, 297, p. 122427; Oh, YS, Maeng, J, Kim, SJ., Use of microorganism-immobilized polyurethane foams to absorb and degrade oil on water surface (2000) Appl.Microbiol. Biotechnol, 54 (3), pp. 418-423; Qiao, K, Tian, W, Bai, J, Wang, L, Zhao, J, Removal of high-molecular-weight polycyclic aromatic hydrocarbons by a microbial consortium immobilized in magnetic floating biochar gel beads (2020) Mar. Pollut. Bull, 159, p. 111489; Hai, N, Buller, N, Fotedar, R., Encapsulation capacity of Artemia nauplii with customized probiotics for use in the cultivation of western king prawns (Penaeus latisulcatus Kishinouye, 1896) (2010) Aquacult. Res, 41 (6), pp. 893-903; Sun, YZ, Yang, HL, Huang, KP, Ye, JD, Zhang, CX., Application of autochthonous Bacillus bioencapsulated in copepod to grouper Epinephelus coioides larvae (2013) Aquaculture, 392, pp. 44-50; Jahari, MA, Mustafa, S, Abd Manap, Y, udie Lamasudin, D, Roslan, MAH., Encapsulation of Lactobacillus plantarum with mannan and sodium alginate improves its cell production (2019) J. Biochem. Microbiol. Biotechnol, 7 (1), pp. 17-22; Rosas-Ledesma, P, León-Rubio, JM, Alarcón, FJ, Moriñigo, MA, Balebona, MC., Calcium alginate capsules for oral administration of fish probiotic bacteria: Assessment of optimal conditions for encapsulation (2012) Aquacult. Res, 43 (1), pp. 106-116
Keywords
- Beneficial Microorganisms for Corals
- BMCs
- coral reef
- environmental adaptation
- holobiont
- microbiome
- probiotics
ASJC Scopus subject areas
- Biotechnology
- Animal Science and Zoology
- Genetics
- veterinary(all)