Abstract
The close association between marine invertebrates, zooxanthellae, and numerous bacteria gives rise to the question of the identity of the actual producer of secondary metabolites. In fall of 2005, a widespread bleaching event occurred throughout the Caribbean Sea in which some colonies of the gorgonian coral Plexaurella fusifera bleached. This study investigated whether zooxanthellae play a key role in the biosynthesis of secondary metabolite terpenes from P. fusifera. The extent of bleaching was examined by chlorophyll A analysis and also by zooxanthellae isolation and cell counting. The bleached and unbleached colonies were found to contain similar concentrations of eremophilene as the major terpene, and both exhibited similar biosynthetic capability as evaluated by the transformation of [C1-3H]-farnesyl diphosphate to the sesquiterpenes. Differences in bacterial communities between the bleached and unbleached colonies were analyzed using molecular techniques, and preliminary indications are that unbleached and bleached corals are dominated by low G + C firmicutes and gammaproteobacteria, respectively. It therefore appears that terpene biosynthesis can proceed independently of the zooxanthellae in P. fusifera, suggesting that the coral or a bacterium is the biosynthetic source.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Bayer FM (1961) The shallow-water Octocorallia of the West Indian region: a manual for marine biologists. Martinus Nijhoff, The Hague, Netherlands
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:129–138
Brown BE, Dunne RP, Chansang H (1996) Coral bleaching relative to elevated seawater temperature in the Andaman Sea (Indian Ocean) over the last 50 years. Coral Reefs 15:151–152
Brueck TB, Brueck WM, Santiago-Vazquez LZ, McCarthy PJ, Kerr RG (2007) Diversity of the bacterial communities associated with the azooxanthellate deep water octocorals Leptogorgia minimata, Iciligorgia schrammi, and Swiftia exertia. Mar Biotechnol 9:561–576 DOI 10.1007/s10126-007-9009-1
Ciereszko LS (1989) Sterol and diterpenoid production by zooxanthellae in coral reefs: a review. Biol Oceanogr 6:363–374
Faulkner DJ, He H, Unson MD, Bewley CA, Garson MJ (1993) New metabolites from marine sponges: are symbionts important. Gazz Chim Ital 123:301–307
Gleeson MW, Strong AE (1995) Applying MCSST to coral reef bleaching. Adv Space Res 16:151–154
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509
Goiran C, Allemand D, Galgani I (1997) Transient Na[+] stress in symbiotic dinoflagellates after isolation from coral-host cells and subsequent immersion in seawater. Mar Biol 129:581–589
Goreau TJ, Hayes RL (1994) Coral bleaching and ocean “hot spots”. Ambio 23:176–180
Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472
Harder T, Lau SCK, Dobretsov S, Fang TK, Qian P-Y (2003) A distinctive epibiotic bacterial community on the soft coral Dendronephthya sp. and antibacterial activity of coral tissue extracts suggest a chemical mechanism against bacterial epibiosis. FEMS Microbiol Ecol 43:337–347
Hochmannova J, Novotny L, Herout V (1962a) Sesquiterpenic hydrocarbons from rhizomes of Petasites officinalis. Collect Czechoslov Chem Commun 27:1870–1876
Hochmannova J, Novotny L, Herout V (1962b) Hydrocarbons from Petasites albus (L.) Gaerth. Rhizomes. Collect Czechoslov Chem Commun 27:2711–2714
Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Mar Ecol Prog Ser 121:181–190
Hoegh-Guldberg O, Smith GJ (1989) Periodic mass-bleaching and elevated sea temperatures bleaching of outer reef slope communities in Moorea, French Polynesia. J Exp Mar Biol Ecol 129:279–303
Hoegh-Guldberg O, Berkelmans R, Oliver J (1997) Proceedings of the Cooperative Research Centre Conference on Research and Reef Management Meeting. The Great Barrier Reef: Science, Use and Management, CRC Conference, pp 21–43
Jeffrey SW, Mantoura RFC, Bjørnland T (1997) Part IV—data for the identification of47 key phytoplankton pigments. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Part IV Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris
Jones RJ, Berkelmans R, Oliver J (1997) Recurrent bleaching of corals at Magnetic Island (Australia) relative to air and seawater temperature. Mar Ecol Prog Ser 158:289–292
Kleppel GS, Dodge RE, Reese CJ (1989) Changes in pigmentation associated with the bleaching of stony corals. Limnol Oceanogr 34:1331–1335
Kobayashi J, Ishibashi M (1993) Bioactive metabolites of symbiotic marine organisms. Chem Rev 93:1753–1770
Kokke WCMC, Epstein S, Look SA, Rau GH, Fenical W, Djerrasi C (1984) On the origin of terpenes in symbiotic associations between marine invertebrates and algae (Zooxanthellae). J Biol Chem 259:8168–8173
Krepinsky J, Motl O, Dolejs L, Novotny L, Herout V, Bates RB (1968) The structure of eremophilene, the sesquiterpenic hydrocarbon from Petasites genus. Tetrahedron Lett 29:3315–3318
Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Systematic and Evol Micro 51:1383–1388
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, UK, pp 115–175
Look SA, Fenical W, Jacobs RS, Clardy J (1986) The Pseudopterosins: anti-inflammatory and analgesic natural products from the sea whip Pseudopterogorgia elisabethae. Proc Natl Acad Sci 83:6238–6240
Michalek-Wagner K, Bourne DJ, Bowden BF (2001) The effects of different strains of zooxanthellae on the secondary-metabolite chemistry and development of the soft-coral host Lobophytum compactum. Mar Biol 138:753–760
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient poor environments. Bioscience 27:454–460
Mydlarz LD, Jacobs RS, Boehnlein J, Kerr RG (2003) Pseudopterosin biosynthesis in Symbiodinium sp., the dinoflagellate symbiont of Pseudopterogorgia elisabethae. Chem Biol 10:1–20
Papastephanou C, Anderson DG (1982) Crassin acetate biosynthesis in a cell-free homogenate of zooxanthellae from Pseudoplexaura porosa (Houttyun): implication to the symbiotic process. Comp Biochem Physiol 73B:617–624
Penn K, Wu D, Eisen JA, Ward N (2006) Characterization of bacterial communities associated with deep-sea corals on Gulf of Alaska seamounts. Appl Environ Microb 72:1680–1683
Rodriguez A (1995) The natural products chemistry of West Indian gorgonian octocorals. Tetrahedron 51:4571–4618
Rowher F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91
Schmidt E (2005) From chemical structure to environmental biosynthetic pathways: navigating marine invertebrate–bacteria associations. Trends Biotech 23:437–440
Schmitz K, Kremer BP (1977) Carbon fixation and analysis of assimilates in a coral–dinoflagellate symbiosis. Mar Biol 42:305–313
Webster NS, Bourne D (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94
Yonge DM, Nicholls AG (1973) Studies on the physiology of corals. IV. The structure, distribution and physiology of the zooxanthellae. Scientific Report of the Great Barrier Reef Expedition 1928–29, pp 135–176
Acknowledgments
We would like to acknowledge funding for a Florida Center of Excellence in Biomedical and Marine Biotechnology, support from the National Science Foundation (UCB-0119011), the Canada Research Chair program, and the US Environmental Protection Agency’s Science to Achieve Results (STAR) Program (U-91618401-0; JFR). We would also like to thank R. Ritson-Williams (Smithsonian Marine Station) for performing spicule analysis, S. Gunasekera (Harbor Branch Oceanographic Institute) for optical rotation measurement, and the crew of the Easy Goin’ for assistance in the collection of specimens.
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Frenz-Ross, J.L., Enticknap, J.J. & Kerr, R.G. The Effect of Bleaching on the Terpene Chemistry of Plexaurella fusifera: Evidence that Zooxanthellae Are Not Responsible for Sesquiterpene Production. Mar Biotechnol 10, 572–578 (2008). https://doi.org/10.1007/s10126-008-9095-8
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DOI: https://doi.org/10.1007/s10126-008-9095-8