Abstract
Reef-building corals encompass various strategies to defend against harmful ultraviolet (UV) radiation. Coral mucus contains UV-absorbing compounds and has rich prokaryotic diversity associated with it. In this study, we isolated and characterized the UV-absorbing bacteria from the mucus of the corals Porites lutea and Acropora hyacinthus during the pre-summer and summer seasons. A total of 17 UV-absorbing bacteria were isolated and sequenced. The UV-absorbing bacteria showed UV absorption at wavelengths ranging from λ max = 333 nm to λ min = 208 nm. Analysis of the DNA sequences revealed that the majority of the UV-absorbing bacteria belonged to the family Firmicutes and the remaining belonged to the family Proteobacteria (class Gammaproteobacteria). Comparison of the sequences with the curated database yielded four distinct bacterial groups belonging to the genus Bacillus, Staphylococcus, Salinicoccus and Vibrio. The absorption peaks for the UV-absorbing bacteria shifted to the UV-A range (320–400 nm) when they were incubated at higher temperatures. Deciphering the complex relationship between corals and their associated bacteria will help us to understand their adaptive strategies to various stresses.
References
Anderson S, Zepp RG, Machula J, Santavy D, Hansen L, Mueller E (2001) Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. Human and Ecological Risk Assessment 7:1271–1282
Arai T, Nishijima M, Adachi K, Sano H (1992) Isolation and structure of UV absorbing substance from the marine bacterium Micrococcus sp. AK-334. MBI Report. Marine Biotechnology Institute, Tokyo, Japan, pp 88–94
Banaszak AT, Trench RK (1995) Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbiosis. II. The synthesis of mycosporine-like amino acids in response to UV in Anthopleura elegantissima and Cassiopeia xamachana. J Exp Mar Biol Ecol 194:233–250
Bentley R (1990) The Shikimate pathway—a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307–384
Bhatia S, Garg A, Sharma K, Kumar S, Sharma A, Purohit AP (2011) Mycosporine and mycosporine like amino acids: A paramount tool against ultraviolet irradiation. Pharmacogn Rev 5:138–146
Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309
Ceh J, Keulen MV, Bourne DG (2011) Coral associated bacterial communities on Ningaloo Reef, Western Australia. FEMS Microbiol Ecol 75:134–144
Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259
De J, Ramaiah N (2007) Characterization of marine bacteria highly resistant to mercury exhibiting multiple resistances to toxic chemicals. Ecol Indicators 7:511–520
Ducklow H, Mitchell R (1979) Bacterial populations and adaptations in the mucus layer on living corals. Limnol Oceanogr 24:715–725
Dunlap WC, Chalker BE (1986) Identification and quantification of near UV absorbing compounds in a hermatypic scleractinian. Coral Reefs 5:155–159
Dunlap WC, Shick M (1998) Review—Ultraviolet radiation-absorbing Mycosporine-like amino acids in coral reef organisms: A biochemical and environmental perspective. J Phycol 34:418–430
Favre-Bonvin J, Bernillion J, Salin N, Arpin N (1987) Biosynthesis of Mycosporine: mycosporine glutaminol in Trichodesmium roseum. Phytochemistry 26:2509–2514
Felsenstein J (2004) Inferring phytogenies. Sinauer Associates, Sunderland, MA
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:e7319
Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838
Hader DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285
Hader DP, Helbling EW, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosytems and interactions with climate change. Photochem Photobiol Sci 10:242–260
Hubbard JAEB, Pocock YP (1972) Sediment rejection by recent scleractinian corals: a key to palaeo-environmental reconstruction. Geol Rdsch 61:598–626
Ishikura M, Kato C, Maruyama T (1997) UV-absorbing substances in zooxanthellae and azooxanthellate clams. Mar Biol 128:649–655
Jones JM, Ritchie KB, Jones LE, Ellner SP (2010) How microbial community composition regulates coral disease development. PLoS Biol 8:1–16
Karentz D, Bothwell ML, Coffin RB, Hanson A, Herndl GJ, Kilham SS, Lesser MP, Lindell M, Moeller RE, Morris DP, Neale PJ, Sanders RW, Weiler CS, Wetzel RG (1994) Report of working group on bacteria and phytoplankton. In: Williamson CE, Zagarese HE (eds) Impact of UV-B radiation on pelagic freshwater ecosystems. Arch Hydrobiol 43:31–69
Karsten U, Franklin LA, Luning K, Wiencke C (1998) Natural ultraviolet radiation and photosynthetically active radiationinduce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257–262
Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259
Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377
Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232
Liss TJ (1980) Fractionation of DNA fragments by polyethylene glycol induced precipitation. Methods Enzymol 65:347–353
Ludwig W, Strunk O, Westram R, Richter L, Meier H (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363
Meikle P, Richards G, Yellowlees D (1988) Structural investigations on the mucus from 6 species of corals. Mar Biol 99:187–193
Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215
Ochs CA, Eddy LP (1998) Effects of UV-A (320–399 Nanometers) on grazing pressure of a marine heterotrophic nanoflagellate on strains of the unicellular cyanobacteria Synechococcus sp. Appl Environ Microbiol 64:287–293
Orland MS, Kushmaro A (2009) Coral mucus- associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380
Orland MS, Sivan A, Kushmaro A (2012) Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb Ecol 64:851–859
Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501
Rastogi RP, Sinha RP (2011) Solar ultraviolet radiation-induced DNA damage and protection/repair strategies in cyanobacteria. Int J Pharma Biosci 2:B271–B288
Reef R, Kaniewska P, Hoegh-Guldberg O (2009) Coral skeletons defend against ultraviolet radiation. PLoS ONE 4(11):e7995
Reshelf L, Koren O, Loya Y, Rosenberg IZ, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification of rDNA genes by polymerase chain reaction. Appl Environ Microbiol 58:3417–3418
Ritchie KB, Smith GW (1995) Preferential carbon utilization by surface bacterial communities from water mass, normal and white-band diseased Acropora cervicornis. Mol Mar Biol Biotechnol 4:345–354
Ritchie KB, Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 263–269
Ritchie KB, Dennis JH, McGrath T, Smith GW (1994) Bacteria associated with bleached and nonbleached areas of Montastrea annularis. Proceedings 5th symposium: Natural history of Bahamas. San Salvador, Bahamas, Bahamas field station, pp 75–80
Rohwer F, Breithart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral—associated bacteria. Mar Ecol Prog Ser 243:1–10
Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406
Shashar S, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: Evidence for coral bacteria interactions. Mar Ecol Prog Ser 111:259–264
Shick JM, Lesser MP, Jokiel PL (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol 2:527–545
Singh SP, Kumari S, Rastogi RP, Singh SL, Sinha RP (2008) Mycosporine-like amino acids (MAAs): Chemical structure, biosynthesis and significance as UV-absorbing/screening compounds. Indian J Exp Biol 46:7–17
Sinha RP, Klisch M, Groniger A, Hader DP (1998) Ultraviolet absorbing/screening substances in cyanobacterial, phytoplankton and macroalgae. J Photochem Photobiol B: Biol 47:83
Sinha RP, Klisch M, Helbling EW, Hader DP (2001) Induction of mycosporine—like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. J Photochem Photobiol B: Biol 60:129–135
Sweet MJ, Croquer A, Bythell JC (2011a) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
Sweet MJ, Croquer A, Bythell JC (2011b) Dynamics of bacterial community development in the reef coral Acropora muricata following experimental antibiotic treatment. Coral Reefs 30:1121–1133
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Ushijima B, Smith A, Aeby GS, Callahan SM (2012) Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS ONE 7:e46717
Weisberg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70
Acknowledgments
The first author acknowledges the financial support necessary for carrying out this work from Science & Engineering Research Council, Department of Science and Technology (SERC-DST), Government of India . Third author acknowledges the DST, Government of India, for awarding INSPIRE fellowship. CSIR-NIO contribution No. 5403.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Ruth Gates
Rights and permissions
About this article
Cite this article
Ravindran, J., Kannapiran, E., Manikandan, B. et al. UV-absorbing bacteria in coral mucus and their response to simulated temperature elevations. Coral Reefs 32, 1043–1050 (2013). https://doi.org/10.1007/s00338-013-1053-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-013-1053-x