Abstract
Coral populations have precipitously declined on Caribbean reefs while algal abundance has increased, leading to enhanced competitive damage to corals, which likely is mediated by the potent allelochemicals produced by both macroalgae and benthic cyanobacteria. Allelochemicals may affect the composition and abundance of coral-associated microorganisms that control host responses and adaptations to environmental change, including susceptibility to bacterial diseases. Here, we demonstrate that extracts of six Caribbean macroalgae and two benthic cyanobacteria have both inhibitory and stimulatory effects on bacterial taxa cultured from the surfaces of Caribbean corals, macroalgae, and corals exposed to macroalgal extracts. The growth of 54 bacterial isolates was monitored in the presence of lipophilic and hydrophilic crude extracts derived from Caribbean macroalgae and cyanobacteria using 96-well plate bioassays. All 54 bacterial cultures were identified by ribotyping. Lipophilic extracts from two species of Dictyota brown algae inhibited >50% of the reef coral bacteria assayed, and hydrophilic compounds from Dictyota menstrualis particularly inhibited Vibrio bacteria, a genus associated with several coral diseases. In contrast, both lipo- and hydrophilic extracts from 2 species of Lyngbya cyanobacteria strongly stimulated bacterial growth. The brown alga Lobophora variegata produced hydrophilic compounds with broad-spectrum antibacterial effects, which inhibited 93% of the bacterial cultures. Furthermore, bacteria cultured from different locations (corals vs. macroalgae vs. coral surfaces exposed to macroalgal extracts) responded differently to algal extracts. These results reveal that extracts from macroalgae and cyanobacteria have species-specific effects on the composition of coral-microbial assemblages, which in turn may increase coral host susceptibility to disease and result in coral mortality.
References
Amman RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Amsler CD, Iken KB, McClintock JB, Baker BJ (2001) Secondary metabolites from antarctic marine organisms and their ecological implications. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Florida, pp 267–300
Anthony KRN, Kline DI, Diaz-Pulida G, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446
Antonius A (1977) Coral mortality in reefs: a problem for science and management. Proc 3rd Int Coral Reef Symp 2:617–623
Baker JH, Orr DR (1986) Distribution of epiphytic bacteria on freshwater plants. J Ecol 74:155–165
Ballantine DL, Gerwick WH, Velez SM, Alexander E, Guevara P (1987) Antibiotic activity of lipid-soluble extracts from Caribbean marine algae. Hydrobiologia 151(152):463–469
Banin E, Vassilakos D, Orr E, Martinez R, Rosenberg E (2003) Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol 46:418–422
Ben Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55
Birrell CL, McCook LJ, Willis BL, Diaz-Pulido GA (2008) Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr Mar Biol Annu Rev 46:25–63
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5(6):1220–1227
Castillo I, Lodeiros C, Nunez M, Campos I (2001) In vitro study of antibacterial substances produced by bacteria associated with various marine organisms. Rev Biol Trop 49:1213–1221
Cervino JM, Hayes RL, Goreau TJ, Smith GW (2004) Zooxanthellae regulation of yellow blotch/band and other coral diseases contrasted with temperature related bleaching: in situ destruction vs. expulsion. Symbiosis 37:63–85
Cervino JM, Thompson FL, Gomez-Gil B, Lorence EA, Goreau TJ, Hayes RL, Winiarski-Cervino KB, Smith GW, Hughen K, Bartels E (2008) The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J Appl Microbiol 105(5):1658–1671
Cetrulo GL, Hay ME (2000) Activated chemical defenses in tropical versus temperate seaweeds. Mar Ecol Prog Ser 207:243–253
Chadwick NE, Morrow KM (2011) Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, New York, pp 347–371
Chet I, Mitchell R (1976) Ecological aspects of microbial chemotactic behavior. Annu Rev Microbio1 30:221–239
Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through symbiotic relationship with bacteria. Nature 438(3):33–35
Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers of living corals. Limnol Oceanogr 24:715–725
Egan S, James S, Holmstrom C, Kjelleberg S (2001) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. FEMS Microbiol Ecol 35:67–73
Engel S, Puglisi MP, Jensen PR, Fenical W (2006) Antimicrobial activities of extracts from tropical Atlantic marine plants against marine pathogens and saprophytes. Mar Biol 149:991–1002
Fong P, Paul VJ (2011) Coral reef algae. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, New York, pp 241–272
Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–300
Gruppo V, Johnson CM, Marietta KS, Scherman H, Zink EE, Crick DC, Adams LB, Orme IM, Lenaerts AJ (2006) Rapid microbiologic and pharmacologic evaluation of experimental compounds against Mycobacterium tuberculosis. Antimicrob Agents Chemother 50:1245–1250
Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263
Ivanova EP, Mikhailov VV (2001) A new family, Alteromonadaceae fam. nov., including marine proteobacteria of the genera Alteromonas, Pseudoalteromonas, Idiomarina, and Colwellia. Microbiology 70:10–17
Jones RJ, Bowyer J, Hoegh-Guldberg O, Blackall LL (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol Prog Ser 281:63–77
Kjelleberg S, Steinberg P, Givskov M, Gram L, Manefield M, de Nys R (1997) Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat Microbiol Ecol 13:85–93
Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity on coral mortality. Mar Ecol Prog Ser 314:119–125
Koh EGL (1997) Secretion of bioactive compounds by a scleractinian coral. Proc 8th Int Coral Reef Symp 2: 1263–1266
Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117
Lane AL, Nyadong L, Galhena AS, Shearer TL, Paige Stout E, Mitchell Parry R, Kwasnik M, Wang MD, Hay ME, Fernandez FM, Kubanek J (2009) Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc Natl Acad Sci USA 106:7314–7319
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000
Lovejoy C, Bowman JP, Hallegraeff GM (1998) Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl Environ Microbiol 64:2806–2813
Luna GM, Biavasco F, Danovaro R (2007) Bacteria associated with the rapid tissue necrosis of stony corals. Environ Microbiol 9(7):1851–1857
Manfield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg SA (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology (UK) 145:283–291
Mann KH (1973) Seaweeds: Their productivity and strategy for growth. Science 182(4116):975–981
Maximilien R, de Nys R, Holmstrom C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD (1998) Chemical mediation of bacterial surface colonization by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233–246
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144
McClanahan TR, Aronso RB, Precht WF, Muthiga NA (1999) Fleshy algae dominate remote coral reefs of Belize. Coral Reefs 18:61–62
McClanahan TR, Berbman K, Huitric M, McField M, Elfwing T, Nystrom N, Nordemar I (2000) Response of fishes to algae reduction on Glovers Reef, Belize. Mar Ecol Prog Ser 206:273–282
Medlin LK, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499
Nagle DG, Paul VJ (1999) Production of secondary metabolites by filamentous tropical marine cyanobacteria: ecological functions of the compounds. J Phycol 35:1412–1421
Nylund GM, Cervin G, Hermansson M, Pavia H (2005) Chemical inhibition of bacterial colonization by the red alga Bonnemaisonia hamifera. Mar Ecol Prog Ser 302:27–36
Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264
Paul VJ, Van Alstyne K (1992) Activation of chemical defenses in the tropical green algae Halimeda spp. J Exp Mar Biol Ecol 160:191–203
Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical mediation of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In: McClintock J, Baker B (eds) Marine chemical ecology CRC Press. Boca Raton, FL, pp 227–265
Paul NA, de Nys R, Steinberg PD (2006) Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function. Mar Ecol Prog Ser 306:87–101
Puglisi MP, Engel S, Jensen PR, Fenical W (2007) Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens and saprophytes. Mar Biol 150:531–540
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Reshef L, Ron E, Rosenberg E (2008) Genome analysis of the coral bleaching pathogen Vibrio shiloi. Arch Microbiol 190:185–194
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Ritchie KB, Smith GW (1998) Type II white-band disease. Rev Biol Trop 46:199–203
Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJA, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457
Rogers CS, Garrison V, Grober-Dunsmore R (1997) A fishy story about hurricanes and herbivory, seven years of research on a reef in St. John, U.S. Virgin Islands. Proc 8th Int Coral Reef Symp 1:555–560
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease, and evolution. Nature 5:255–362
Schmitt TM, Hay ME, Lindquist N (1995) Antifouling and herbivore deterrent roles of seaweed secondary metabolites: constraints on chemically-mediated coevolution. Ecology 76:107–123
Segel LA, Ducklow HW (1982) A theoretical investigation into the influence of sublethal stresses on coral-bacterial ecosystem dynamics. Bull Mar Sci 32:919–935
Shanmugam M, Sethupathi P, Rhee KJ, Yong S, Knight KL (2005) Bacterial-induced inflammation in germ-free rabbit appendix. Inflamm Bowel Dis 11:992–996
Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacterial interactions. Mar Ecol Prog Ser 111:259–264
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 9:835–845
Steinberg P, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, FL, pp 355–387
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3(5):512–521
Tsuda RT, Kami HT (1973) Algal succession on artificial reefs in a marine lagoon environment in Guam. J Phycol 9:260–264
Vu I, Smelick G, Harris S, Lee S, Weil E, Whitehead RF, Bruno JF (2009) Macroalgae has no effect on the severity and dynamics of Caribbean yellow band disease. PloS ONE 4(2):e4514
Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329–340
Wang G, Shuai L, Li Y, Lin W, Zhao X, Duan D (2008) Phylogenetic analysis of epiphytic marine bacteria on hole rotten diseased sporophytes of Laminaria japonica. J Appl Phycol 20:403–409
Wommack KE, Ravel J, Hill RT, Colwell RR (1999) Population dynamics of Chesapeake Bay virioplankton: total community analysis using pulsed field gel electrophoresis. Appl Environ Microbiol 65:231–240
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735
Acknowledgments
We thank the Florida Keys National Marine Sanctuary for granting collection and research permits (FKNMS-2008-019) and the Belize Fisheries Department for permits to collect coral mucus samples. The Harbor Branch Oceanographic Institute at Florida Atlantic University Center for Marine Biomedical and Biotechnology Research, Mote Marine Laboratory, University of the Virgin Islands MacLean Marine Science Center, and the Smithsonian Marine Station at Fort Pierce and the Smithsonian’s Carrie Bow Cay Field Station all provided invaluable logistical support. E. A. Guzmán, A. Moss and R Ritson-Williams provided field and laboratory assistance. This work was supported by a National Oceanic and Atmospheric Administration National Marine Sanctuary Program Nancy Foster Scholarship to KMM, NOAA’s ECOHAB program project NA05NOS4781194 (VJP), a Mote Marine Laboratory Protect our Reefs grant award POR 2007-30 (VJP), the Smithsonian Marine Science Network, and a Puerto Rico Sea Grant R-101-1-08 (NEC). This is contribution #846 of the Smithsonian Marine Station at Fort Pierce, contribution #900 of the Caribbean Coral Reef Ecosystems Program, and contribution #80 of the Auburn University Marine Biology Program.
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Morrow, K.M., Paul, V.J., Liles, M.R. et al. Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 30, 309–320 (2011). https://doi.org/10.1007/s00338-011-0747-1
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DOI: https://doi.org/10.1007/s00338-011-0747-1