Abstract
Development of the bacterial community associated with the coral Acropora muricata (=formosa) was monitored using 16S rRNA gene-based techniques and abundance counts over time following experimental modification of the existing microbial community using the antibiotic ciprofloxacin. Abundance of bacteria was reduced >99% by the treatment, resulting in significant changes in bacterial community structure. Following redeployment to their natural environment, some settlement and re-growth of bacteria took place within a few hours, including ribosomal types that were not present, or in low abundance, in the natural microbiota. However, complete recovery of the bacterial community required longer than 96 h, which indicates a relatively slow settlement and growth of bacteria from the water column and suggests that turnover of the natural community is similarly slow. The early developing community was dominated by antibiotic-resistant bacteria from the natural microbiota that survived the treatment and proliferated in the absence of natural competitors, but also included some non-resident ribotypes colonizing from the water column. Almost, all these opportunists were significantly reduced or eliminated within 96 h after treatment, demonstrating a high resilience in the natural bacterial community. Potential pathogens, including a Clostridium sp., inhabited the coral at low abundances, only becoming prevalent when the natural microbiota was disturbed by the treatment. The healthy coral-associated microbiota appears to be strongly controlled by microbial interactions.
References
Ainsworth TD, Hoegh-Guldberg O (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4:289–296
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Apprill A, Marlow HQ, Martindale MQ, Rappe MS (2009) The onset of microbial associations in the coral Pocillopora meandrina. ISME 3:685–699
Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55
Ben-Haim Y, Thompson FL, Thompson CC, Cnockaert MC, Hoste B, Swings J, Rosenberg E (2003) Vibrio coralliilyticus sp nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Microbiol 53:309–315
Bourne DG (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24:304–312
Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562
Brandt ME, McManus JW (2009) Disease incidence is related to bleaching extent in reef-building corals. Ecology 90:2859–2867
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol-Prog Ser 296:291–309
Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70:27–32
Bythell JC, Barer MR, Cooney RP, Guest JR, O’Donnell AG, Pantos O, Le Tissier MDA (2002) Histopathological methods for the investigation of microbial communities associated with disease lesions in reef corals. Lett Appl Microbiol 34:359–364
Castillo I, Lodeiros C, Nunez M, Campos I (2001) In vitro evaluation of antibacterial substances produced by bacteria isolated from different marine organisms. Rev Biol Trop 49:1213–1221
Ceran N, Mert D, Kocdogan FY, Erdem I, Adalati R, Ozyurek S, Goktas P (2011) A randomized comparative study of single-dose fosfomycin and 5-day ciprofloxacin in female patients with uncomplicated lower urinary tract infections. J Infect Chemother 16:424–430
Clarke KR, Warwick RM (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol-Prog Ser 216:265–278
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37(Database issue):D141–D145. doi:10.1093/nar/gkn879
Crogan NL, Evans BC (2007) Clostridium difficile: An emerging epidemic in nursing homes. Geriatric Nursing 28:161–164
Croswell A, Amir E, Teggatz P, Barman M, Salzman NH (2009) Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun 77:2741–2753
Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208:75–81
Forrest A, Nix DE, Ballow CH, Goss TF, Birmingham MC, Schentag JJ (1993) Pharmacodynamics of intravenous Ciprofloxacin in seriously ill-patients. Antimicrob Agents Chemother 37:1073–1081
Foster KR (2005) Biomedicine—Hamiltonian medicine: Why the social lives of pathogens matter. Science 308:1269–1270
Frank DN, Amand ALS, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104:13780–13785
Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partioning of bacterial communities between seawater and healthy black band diseased and dead coral surfaces. Appl Environ Microbiol 68:2214–2228
Frias-Lopez J, Bonheyo GT, Jin QS, Fouke BW (2003) Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific Reefs. Appl Environ Microbiol 69:2409–2413
Garren M, Raymundo L, Guest J, Harvell CD, Azam F (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4
Geffen Y, Ron EZ, Rosenberg E (2009) Regulation of release of antibacterials from stressed scleractinian corals. FEMS Microbiol Lett 295:103–109
Gil-Agudelo DL, Fonseca DP, Weil E, Garzon-Ferreira J, Smith GW (2007) Bacterial communities associated with the mucopolysaccharide layers of three coral species affected and unaffected with dark spots disease. Can J Microbiol 53:465–471
Goldenberg SD, Dieringer T, French GL (2010) Detection of toxigenic Clostridium difficile in diarrheal stools by rapid real-time polymerase chain reaction. Diagn Microbiol Infect Dis 67:304–307
Gunthorpe L, Cameron AM (1990) Widespread but variable toxicity in scleractinian corals. Toxicon 28:1199–1219
Guppy R, Bythell JC (2006) Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol-Prog Ser 328:133–142
Hayashida-Soiza G, Uchida A, Mori N, Kuwahara Y, Ishida Y (2008) Purification and characterization of antibacterial substances produced by a marine bacterium Pseudoalteromonas haloplanktis strain. J Appl Microbiol 105:1672–1677
Hill R, Ralph PJ (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol-Prog Ser 352:137–144
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Jernberg C, Lofmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME 1:56–66
Jokiel PL, Coles SL (2004) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162
Keel MK, Songer JG (2007) The distribution and density of Clostridium difficile toxin receptors on the intestinal mucosa of neonatal pigs. Vet Pathol 44:814–822
Kellogg CA (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol-Prog Ser 273:81–88
Kim K (1994) Antimicrobial activity in gorgonian corals (Coelenterata, Octocorallia). Coral Reefs 13:75–80
Kim K, Kim PD, Alker AP, Harvell CD (2000) Chemical resistance of gorgonian corals against fungal infections. Mar Biol 137:393–401
Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2005) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24:129–137
Koo HL, Garey KW, DuPont HL (2010) Future novel therapeutic agents for Clostridium difficile infection. Expert Opinion on Investigational Drugs 19:825–836
Kooperman N, Ben-Dov E, Kramarsky-Winter E, Barak Z, Kushmaro A (2007) Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol Lett 276:106–113
Kushmaro A, Rosenberg E, Fine M, Ben-Haim Y, Loya Y (1998) Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol-Prog Ser 171:131–137
Kushmaro A, Banin E, Loya Y, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Microbiol 51:1383–1388
Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS One 5:e10401
Lawley TD, Croucher NJ, Yu L, Clare S, Sebaihia M, Goulding D, Pickard DJ, Parkhill J, Choudhary J, Dougan G (2009) Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J Bacteriol 191:5377–5386
Lecampionalsumard T, Golubic S, Priess K (1995) Fungi in corals - Symbiosis or disease - Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol-Prog Ser 117:137–147
Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44
Liu C-h, Yang X-q, Liu C-h, He Y, Wang L-j (2007) Allergic airway response associated with the intestinal microflora disruption induced by antibiotic therapy. Zhonghua Er Ke Za Zhi 45:450–454
Mao-Jones J, Ritchie KB, Jones LE, Ellner SP (2010) How microbial community composition regulates coral disease development. PLoS Biol 8(3):e1000345. doi:10.1371/journal.pbio.1000345
Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Develop 9:355–367
Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Org 87:67–78
Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215
Nix DE, Sands MF, Peloquin CA, Vari AJ, Cumbo TJ, Vance JW, Fracasso JE, Schentag JJ (1987) Dual individualization of intravenous Ciprofloxacin in patients with nosocomial lower respiratory-tract infections. Am J Med 82:352–356
Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348
Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ Microbiol 5:370–382
Papatheodorou P, Zamboglou C, Genisyuerek S, Guttenberg G, Aktories K (2010) Clostridial glucosylating toxins enter cells via clathrin-mediated endocytosis. PLoS One 5:e10673
Penders J, Stobberingh EE, Van den Brandt PA, Thijs C (2007) The role of the intestinal microbiota in the development of atopic disorders. Allergy 62:1223–1236
Ralph PJ, Larkum AWD, Kuhl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28
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 (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenburg E, Loya Y (eds) Coral health and disease. Springer–Verlag. Berlin, Heidelberg, pp 259–263
Rohwer F, Kelley S (2004) Culture-independent analyses of coral-associated microbes. In: Rosenburg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 265–277
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, Falkovitiz L (2004) The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu Rev Microbiol 58:143–159
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 5:355–362
Rowan R (2004) Coral bleaching—Thermal adaptation in reef coral symbionts. Nature 430:742
Rypien KL, Baker DM (2009) Isotopic labeling and antifungal resistance as tracers of gut passage of the sea fan pathogen Aspergillus sydowii. Dis Aquat Org 86:1–7
Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39
Sekirov I, Tam NM, Jogova M, Robertson ML, Li YL, Lupp C, Finlay BB (2008) Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 76:4726–4736
Sekirov I, Russell SL, Caetano L, Antunes M, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904
Selinummi J, Seppala J, Yli-Harja O, Puhakka JA (2005) Software for quantification of labeled bacteria from digital microscope images by automated image analysis. Biotechniques 39:859–863
Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ (2010) Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS One 5:e10898. doi:10.1371/journal.pone.0010898
Shashar N, Banaszak AT, Lesser MP, Amrami D (1997) Coral endolithic algae: Life in a protected environment. Pac Sci 51:167–173
Slattery M, Rajbhandari I, Wesson K (2001) Competition-mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microb Ecol 41:90–96
Sobel JD (2007) Vulvovaginal candidosis. Lancet 369:1961–1971
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3:512–521
Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and indo-Pacific zooxanthellate corals. Mar Ecol-Prog Ser 266:273–302
Sweet MJ, Bythell JC, Croquer A (2010) Temporal and spatial patterns in waterborne bacterial communities of an island reef system. Aquat Microb Ecol 61:1–11
Sweet MJ, Croquer A, Bythell J (2011) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs. doi:10.1007/s00338-010-0695-1
Tait K, Hutchison Z, Thompson FL, Munn CB (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep 2:145–150
Teplitski M, Ritchie K (2009) How feasible is the biological control of coral diseases? Trends Ecol Evol 24:378–385
Thelestam M, Chaves-Olarte E (2000) Cytotoxic effects of the Clostridium difficile toxins. Clostridium Difficile 250:85–96
Toren A, Lanndau L, Kushmaro A, Loya Y, Rosenburg E (1998) Effect of temperature on adhesion of Vibrio strain AK-1 to Oculina patagonica and on coral bleaching. Environ Microbiol 64:1379–1384
Trischman JA, Oeffner RE, Luna MGD, Kazaoka M (2004) Competitive induction and enhancement of indole and a diketopiperazine in marine bacteria. Mar Biotech 6:215–220
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031
Utrup TR, Mueller EW, Healy DP, Callcut RA, Peterson JD, Hurford WE (2010) High-dose Ciprofloxacin for serious gram-negative infection in an obese, critically ill patient receiving continuous venovenous hemodiafiltration. Ann Pharmacother 44:1660–1664
Wegley L, Yu YN, Breitbart M, Casas V, Kline DI et al (2004) Coral-associated archaea. Mar Ecol-Prog Ser 273:89–96
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jergensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70
Williams DE, Miller MW (2005) Coral disease outbreak: pattern, prevalence and transmission in Acropora cervicornis. Mar Ecol-Prog Ser 301:119–128
Yap IKS, Li JV, Saric J, Martin FP, Davies H, Wang YL, Wilson ID, Nicholson JK, Utzinger J, Marchesi JR, Holmes E (2008) Metabonomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse. J Proteome Res 7:3718–3728
Acknowledgments
This work was supported by the Natural Environmental Research Council, UK (NE/E006949). We would like to thank the staff at Heron Island Research Station, Australia, for their support and cooperation in the field and Olga Pantos, University of Queensland for help with logistics and field sampling.
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Sweet, M.J., Croquer, A. & Bythell, J.C. Dynamics of bacterial community development in the reef coral Acropora muricata following experimental antibiotic treatment. Coral Reefs 30, 1121–1133 (2011). https://doi.org/10.1007/s00338-011-0800-0
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DOI: https://doi.org/10.1007/s00338-011-0800-0