Gorgonian corals possess many novel natural products that could potentially mediate coral-bacterial interactions. Since many bacteria use quorum sensing (QS) signals to facilitate colonization of host organisms, regulation of prokaryotic cell-to-cell communication may represent an important bacterial control mechanism. In the present study, we examined extracts of twelve species of Caribbean gorgonian corals, for mechanisms that regulate microbial colonization, such as antibacterial activity and QS regulatory activity. Ethanol extracts of gorgonians collected from Puerto Rico and the Florida Keys showed a range of both antibacterial and QS activities using a specific Pseudomonas aeruginosa QS reporter, sensitive to long chain AHLs and a short chain N-acylhomoserine lactones (AHL) biosensor, Chromobacterium violaceium. Overall, the gorgonian corals had higher antimicrobial activity against non-marine strains when compared to marine strains. Pseudopterogorgia americana, Pseusopterogorgia acerosa, and Pseudoplexuara flexuosa had the highest QS inhibitory effect. Interestingly, Pseudoplexuara porosa extracts stimulated QS activity with a striking 17-fold increase in signal. The stimulation of QS by P. porosa or other elements of the holobiont may encourage colonization or recruitment of specific microbial species. Overall, these results suggest the presence of novel stimulatory QS, inhibitory QS and bactericidal compounds in gorgonian corals. A better understanding of these compounds may reveal insight into coral-microbial ecology and whether a therapeutic potential exists.
References
[1]
Bayer, F.M. The Shallow-Water Octocorallia of the West Indian Region: A Manual for Marine Biologists; Martinus Nijhoff: The Hague, The Netherland, 1961; Volume 55.
[2]
Lasker, H.R. Prey preferences and browsing pressure of the butterflyfish Chaetodon capistratus on Caribbean gorgonians. Mar. Ecol. Prog. Ser. 1985, 21, 213–220, doi:10.3354/meps021213.
[3]
Fenical, W.; Pawlik, J.R. Defensive properties of secondary metabolites from the Caribbean gorgonian coral Erythropodium caribaeorum. Mar. Ecol. Prog. Ser. 1991, 75, 1–8, doi:10.3354/meps075001.
[4]
Goldberg, W. The ecology of the coral-octocoral communities off the southeast Florida coast: Geomorphology, species composition and zonation. Bull. Mar. Sci. 1973, 23, 465–488.
[5]
Mitchell, N.D.; Dardeau, M.R.; Schroeder, W.W.; Benke, A.C. Secondary production of gorgonian corals in the Northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 1992, 87, 275–281, doi:10.3354/meps087275.
[6]
Harvell, C.D.; Fenical, W.; Greene, C.H. Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.). 1. Development of an in situ feeding assay. Mar. Ecol. Prog. Ser. 1988, 49, 287–294, doi:10.3354/meps049287.
[7]
van Alstyne, K.L.; Wylie, C.R.; Paul, V.J.; Meyer, K. Antipredator defenses in tropical Pacific soft corals (Coelenterata: Alcyonacea). I. Sclerites as defenses against generalist carnivorous fishes. Biol. Bull. 1992, 182, 231–240, doi:10.2307/1542116.
[8]
Slattery, M.; Mcclintock, J.B.; Heine, J.N. Chemical defenses in Antarctic soft corals : Evidence for antifouling compounds. J. Exp. Mar. Biol. Ecol. 1995, 190, 61–77, doi:10.1016/0022-0981(95)00032-M.
[9]
Jensen, P.R.; Harvell, C.D.; Wirtz, K.; Fenical, W. Antimicrobial activity of extracts of Caribbean gorgonian corals. Mar. Biol. 1996, 125, 411–419, doi:10.1007/BF00346321.
[10]
Kim, K. Antimicrobial activity in gorgonian corals (Coelenterata, Octocorallia). Coral Reefs 1994, 13, 75–80, doi:10.1007/BF00300764.
[11]
Ritchie, K.B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 2006, 322, 1–14, doi:10.3354/meps322001.
[12]
Bruck, T.B.; Bruck, W.M.; Santiago-Vazquez, L.Z.; McCarthy, P.J.; Kerr, R.G. Diversity of the bacterial communities associated with the azooxanthellate deep water octocorals Leptogorgia minimata, Iciligorgia schrammi, and Swiftia exertia. Mar. Biotechnol. 2007, 9, 561–576, doi:10.1007/s10126-007-9009-1.
[13]
Gil-Agudelo, D.L.; Myers, C.; Smith, G.W.; Kim, K. Changes in the microbial communities associated with Gorgonia ventalina during aspergillosis infection. Dis. Aquat. Org. 2006, 69, 89–94, doi:10.3354/dao069089.
[14]
Rublee, P.A.; Lasker, H.R.; Gottfried, M.; Roman, M.R. Production and bacterial colonization of mucus from the soft coral Briarium asbestinum. Bull. Mar. Sci. 1980, 30, 888–893.
[15]
Santiago-Vazquez, L.Z.; Bruck, T.B.; Bruck, W.M.; Duque-Alarcon, A.P.; McCarthy, P.J.; Kerr, R.G. The diversity of the bacterial communities associated with the azooxanthellate hexacoral Cirrhipathes lutkeni. ISME J. 2007, 1, 654–659, doi:10.1038/ismej.2007.77.
[16]
Knowlton, N.; Rohwer, F. Multispecies microbial mutualisms on coral reefs: The host as a habitat. Am. Nat. 2003, 162, S51–S62, doi:10.1086/378684.
[17]
Ritchie, K.B.; Smith, G.W. Microbial Communities of Coral Surface Mucopolysaccharide Layers. In Coral Health and Disease; Rosenberg, E., Loya, Y., Eds.; Springer-Verlag: Berlin, Germany, 2004; pp. 259–263.
[18]
Rohwer, F.; Seguritan, V.; Azam, F.; Knowlton, N. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 2002, 243, 1–10, doi:10.3354/meps243001.
[19]
Rosenberg, E.; Koren, O.; Reshef, L.; Efrony, R.; Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microboil. 2007, 5, 355–362.
[20]
Luna, G.M.; Biavasco, F.; Danovaro, R. Bacteria associated with the rapid tissue necrosis of stony corals. Environ. Microbiol. 2007, 9, 1851–1857, doi:10.1111/j.1462-2920.2007.01287.x.
[21]
Pantos, O.; Cooney, R.P.; Le Tissier, M.D.A.; Barer, M.R. The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ. Microbiol. 2003, 5, 370–382, doi:10.1046/j.1462-2920.2003.00427.x.
[22]
Mydlarz, L.; Harvell, C. Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2007, 146, 54–62, doi:10.1016/j.cbpa.2006.09.005.
[23]
Mydlarz, L.; Jacobs, R. An inducible release of reactive oxygen radicals in four species of gorgonian corals. Mar. Freshw. Behav. Physiol. 2006, 39, 143–152, doi:10.1080/10236240600708512.
[24]
Brown, B.E.; Bythell, J.C. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 2005, 296, 291–309, doi:10.3354/meps296291.
[25]
Little, B.J.; Wagner, P.; Maki, J.S.; Walch, M.; Mitchell, R. Factors influencing the adhesion of microorganisms to surfaces. J. Adhes. 1986, 20, 187–210, doi:10.1080/00218468608071236.
[26]
Fuqua, C.; Greenberg, E.P. Listening in on bacteria: Acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 2002, 3, 685–695, doi:10.1038/nrm907.
[27]
Swift, S.; Williams, P.; Stewart, G.S.A.B. N-Acylhomoserine Lactones and Quorum Sensing in Proteobacteria. In Cell-Cell Signaling in Bacteria; Dunny, G.M., Winans, S.C., Eds.; ASM Press: Washington, DC, USA, 1999; pp. 291–312.
Glessner, A.; Smith, R.S.; Iglewski, B.H.; Robinson, J.B. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J. Bacteriol. 1999, 181, 1623–1629.
[30]
Sato, Y.; Sasaki, S. Control of the bioluminescence starting time by inoculated cell density. Anal. Sci. 2006, 22, 1237–1239, doi:10.2116/analsci.22.1237.
[31]
Rice, S.A.; Koh, K.S.; Queck, S.Y.; Labbate, M.; Lam, K.W.; Kjelleberg, S. Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J. Bacteriol. 2005, 187, 3477–3485.
[32]
Zhu, J.; Miller, M.B.; Vance, R.E.; Dziejman, M.; Bassler, B.L.; Mekalanos, J.J. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 2002, 99, 3129–3134.
[33]
Lupp, C.; Ruby, E.G. Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J. Bacteriol. 2005, 187, 3620–3629, doi:10.1128/JB.187.11.3620-3629.2005.
[34]
Visick, K.L.; Ruby, E.G. Vibrio fischeri and its host: It takes two to tango. Curr. Opin. Microbiol. 2006, 9, 632–638.
[35]
Skindersoe, M.E.; Ettinger-Epstein, P.; Rasmussen, T.B.; Bjarnsholt, T.; de Nys, R.; Givskov, M. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 2008, 10, 56–63, doi:10.1007/s10126-007-9036-y.
[36]
Taylor, M.W.; Schupp, P.J.; Baillie, H.J.; Charlton, T.S.; de Nys, R.; Kjelleberg, S.; Steinberg, P.D. Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl. Environ. Microbiol. 2004, 70, 4387–4389.
[37]
Tait, K.; Hutchison, Z.; Thompson, F.L.; Munn, C.B. Quorum sensing signal production and inhibition by coral-associated vibrios. Environ. Microbiol. Rep. 2010, 2, 145–150, doi:10.1111/j.1758-2229.2009.00122.x.
[38]
Golberg, K.; Eltzov, E.; Shnit-Orland, M.; Marks, R.; Kushmaro, A. Characterization of quorum sensing signals in coral-associated bacteria. Microb. Ecol. 2011, 61, 783–792, doi:10.1007/s00248-011-9848-1.
[39]
Alagely, A.; Krediet, C.J.; Ritchie, K.B.; Teplitski, M. Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J. 2011, 5, 1609–1620, doi:10.1038/ismej.2011.45.
[40]
Teplitski, M.; Ritchie, K. How feasible is the biological control of coral diseases? Trends Ecol. Volution 2009, 24, 378–385, doi:10.1016/j.tree.2009.02.008.
[41]
Kelman, D.; Kashman, Y.; Rosenberg, E.; Kushmaro, A.; Loya, Y. Antimicrobial activity of Red Sea corals. Mar. Biol. 2006, 149, 357–363, doi:10.1007/s00227-005-0218-8.
[42]
Mydlarz, L.; Holthouse, S.; Peters, E.; Harvell, C.; May, R. Cellular responses in Sea Fan Corals: Granular amoebocytes react to Pathogen and climate stressors. PLoS One 2008, 3.
[43]
Alker, A.P.; Kim, K.; Dube, D.H.; Harvell, C.D. Localized induction of a generalized response against multiple biotic agents in Caribbean sea fans. Coral Reefs 2004, 23, 397–405, doi:10.1007/s00338-004-0405-y.
[44]
Schug, K.A.; Wang, E.; Shen, S.; Rao, S.; Smith, S.M.; Hunt, L.; Mydlarz, L.D. Direct affinity screening chromatography-mass spectrometry assay for identification of antibacterial agents from natural product sources. Anal. Chim. Acta 2012, 713, 103–110, doi:10.1016/j.aca.2011.11.038.
[45]
Davey, M.E.; Caiazza, N.C.; O’Toole, G.A. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 2003, 185, 1027–1036, doi:10.1128/JB.185.3.1027-1036.2003.
[46]
Huang, Y.L.; Dobretsov, S.; Ki, J.S.; Yang, L.H.; Qian, P.Y. Presence of acyl-homoserine lactone in subtidal biofilm and the implication in larval behavioral response in the polychaete Hydroides elegans. Microb. Ecol. 2007, 54, 384–392, doi:10.1007/s00248-007-9210-9.
[47]
Suntharalingam, P.; Cvitkovitch, D.G. Quorum sensing in streptococcal biofilm formation. Trends Microbiol. 2005, 13, 3–6, doi:10.1016/j.tim.2004.11.009.
[48]
Baumann, P.; Baumann, L.; Mandel, M. Taxonomy of marine bacteria: The genus Beneckea. J. Bacteriol. 1971, 107, 268–294.
[49]
Johnson, R.M.; Katarski, M.E.; Weisrock, W.P. Correlation of taxonomic criteria for a collection of marine bacteria. Appl. Microbiol. 1968, 16, 708–713.
[50]
Leone, S.; Silipo, A.; Nazarenko, E.L.; Lanzetta, R.; Parrilli, M.; Molinaro, A. Molecular structure of endotoxins from gram-negative marine bacteria: An update. Mar. Drugs 2007, 5, 85–112, doi:10.3390/md503085.
[51]
Gram, L.; Grossart, H.P.; Schlingloff, A.; Kiorboe, T. Possible quorum sensing in marine snow bacteria: Production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl. Environ. Microbiol. 2002, 68, 4111–4116.
[52]
Mohamed, N.M.; Cicirelli, E.M.; Kan, J.J.; Chen, F.; Fuqua, C.; Hill, R.T. Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ. Microbiol. 2008, 10, 75–86.
[53]
Mayer, A.M.S.; Jacobson, P.B.; Fenical, W.; Jacobs, R.S.; Glaser, K.B. Pharmacological characterization of the pseudopterosins: Novel anti-inflammatory natural products isolated from the caribbean soft coral, Pseudopterogorgia elisabethae. Life Sci. 1998, 62, PL401–PL407, doi:10.1016/S0024-3205(98)00229-X.
[54]
Epifanio, R.D.A.; Maia, L.F.; Pawlik, J.R.; Fenical, W. Antipredatory secosterols from the octocoral Pseudopterogorgia americana. Mar. Ecol. Prog. Ser. 2006, 329, 307–310.
[55]
Dudler, R.; Eberl, L. Interactions between bacteria and eukaryotes via small molecules. Curr. Opin. Biotechnol. 2006, 17, 268–273, doi:10.1016/j.copbio.2006.04.004.
[56]
Hughes, D.T.; Sperandio, V. Inter-kingdom signalling: Communication between bacteria and their hosts. Nat. Rev. Microbiol. 2008, 6, 111–120, doi:10.1038/nrmicro1836.
[57]
Joint, I.; Tait, K.; Callow, M.E.; Callow, J.A.; Milton, D.; Williams, P.; Camara, M. Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 2002, 298, 1207–1207.
[58]
Kjelleberg, S.; Steinberg, P.; Givskov, M.; Gram, L.; Manefield, M.; de Nys, R. Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat. Microb. Ecol. 1997, 13, 85–93, doi:10.3354/ame013085.
[59]
Manefield, M.; Rasmussen, T.B.; Henzter, M.; Andersen, J.B.; Steinberg, P.; Kjelleberg, S.; Givskov, M. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiololy 2002, 148, 1119–1127.
[60]
Kim, K.; Harvell, C.D. The rise and fall of a six-year coral-fungal epizootic. Am. Nat. 2004, 164, S52–S63, doi:10.1086/424609.
[61]
Couch, C.S.; Mydlarz, L.D.; Harvell, C.D.; Douglas, N.L. Variation in measures of immunocompetence of sea fan coral, Gorgonia ventalina, in the Florida Keys. Mar. Biol. 2008, 155, 281–292, doi:10.1007/s00227-008-1024-x.
[62]
Ward, J.R.; Kim, K.; Harvell, C.D. Temperature affects coral disease resistance and pathogen growth. Mar. Ecol. Prog. Ser. 2007, 329, 115–121, doi:10.3354/meps329115.
[63]
Martinelli, D.; Grossmann, G.; Sequin, U.; Brandl, H.; Bachofen, R. Effects of natural and chemically synthesized furanones on quorum sensing in Chromobacterium violaceum. BMC Microbiol. 2004, 4.
[64]
McClean, K.H.; Winson, M.K.; Fish, L.; Taylor, A.; Chhabra, S.R.; Camara, M.; Daykin, M.; Lamb, J.H.; Swift, S.; Bycroft, B.W.; et al. Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997, 143, 3703–3711.
Patterson, K.L.; Porter, J.W.; Ritchie, K.B.; Polson, S.W. From the Cover: The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad. Sci. USA 2002, 99, 8725–8730.
[67]
Mydlarz, L.D.; Couch, C.S.; Weil, E.; Smith, G.; Harvell, C.D. Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis. Aquat. Org. 2009, 87, 67–78, doi:10.3354/dao02088.
[68]
Gochfeld, D.J.; Aeby, G.S. Antibacterial chemical defenses in Hawaiian corals provide possible protection from disease. Mar. Ecol. Prog. Ser. 2008, 362, 119–128, doi:10.3354/meps07418.
[69]
Weidner, S.; Arnold, W.; Puhler, A. Diversity of uncultured microorganisms associated with the seagrass Halophila stipulacea estimated by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl. Environ. Microbiol. 1996, 62, 766–771.
[70]
Pearson, J.P.; Feldman, M.; Iglewski, B.H.; Prince, A. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 2000, 68, 4331–4334.
[71]
Peters, L.; Konig, G.; Wright, A.; Pukall, R.; Stackebrandt, E.; Eberl, L.; Riedel, K. Secondary metabolites of Flustra foliacea and their influence on bacteria. Appl. Environ. Microbiol. 2003, 69, 3469–3475.
[72]
Riedel, K.; Hentzer, M.; Geisenberger, O.; Huber, B. N-Acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 2001, 147, 3249–3262.
[73]
Anderson, J.; Sternberg, C.; Poulsen, L.; Bjorn, S.; Givskov, M.; Molin, S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 1998, 64, 2240–2246.
