Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T06:53:27.019Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular investigations of the stalked barnacle Vulcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand

Published online by Cambridge University Press:  15 May 2009

Yohey Suzuki ,
Masae Suzuki ,
Shinji Tsuchida ,
Ken Takai ,
Koki Horikoshi ,
Alan J. Southward ,
William A. Newman  and
Toshiyuki Yamaguchi
Yohey Suzuki*
Affiliation:
Research Institute for Geo-resources & Environment, National Institute of Advanced Industrial Science & Technology (AIST), 1-1-1 Higashi, Tsukuba 305-8567, Japan
Masae Suzuki
Affiliation:
Extremobiosphere Research Center, Japan Agency for Marine-Earth Science & Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Shinji Tsuchida
Affiliation:
Extremobiosphere Research Center, Japan Agency for Marine-Earth Science & Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Ken Takai
Affiliation:
Extremobiosphere Research Center, Japan Agency for Marine-Earth Science & Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Koki Horikoshi
Affiliation:
Extremobiosphere Research Center, Japan Agency for Marine-Earth Science & Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Alan J. Southward
Affiliation:
Marine Biological Association of the United Kingdom, Citadel Hill, Plymouth, PLI 2PB Devon, UK
William A. Newman
Affiliation:
Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093-0202, USA
Toshiyuki Yamaguchi
Affiliation:
Marine Biosystems Research Center, Chiba University, 1-33, Yayogi-cho, Inage, Chiba 263-8522, Japan
*
Correspondence should be addressed to: Y. Suzuki, Research Institute for Geo-resources & Environment, National Institute of Advanced Industrial Science & Technology (AIST), 1-1-1 Higashi, Tsukuba 305-8567, Japan email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The hydrothermal-vent barnacle Vulcanolepas osheai of the subfamily Neolepadinae is one of the most conspicuous organisms at the Brothers Caldera, south Kermadec Arc, New Zealand. Like a neolepad species found in the Lau Basin, V. osheai harbours filamentous bacteria on its elongated cirral setae. To define the phylogenetic affiliation of the epibiotic bacteria and the nutrition of the barnacle host, we conducted molecular phylogenetic and isotopic analyses. Analysis of 16S rRNA gene sequences of microbial communities on the cirral setae showed that among 91 bacterial sequences investigated, 28 sequences were related to the ɛ-proteobacterial endosymbiont of Alviniconcha aff. hessleri; 11 sequences were related to the epibiont of the bresiliid shrimp Rimicaris exoculata. Fluorescence in situ hybridization showed that in contrary to results from the 16S rRNA gene-sequence library, approximately 80% of the filamentous bacteria hybridized with a probe targeting the sequences related to the epibiont of the bresiliid shrimp R. exoculata. The fatty-acid profiles of the filamentous bacteria and the host barnacle both contained high levels of monounsaturated C16 and C18 fatty acids, and the carbon isotopic compositions of the biomass and monounsaturated C16 and C18 fatty acids of both the bacteria and barnacle were nearly identical. This would suggest that the nutrition of the barnacle is highly dependent on bacteria thriving around the barnacle, including the epibiotic bacteria.

Keywords

molecular investigationsVulcanolepas osheaiepibiotic bacteriaBrothers Calderasouth Kermadec ArcNew Zealand
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 4 , June 2009 , pp. 727 - 733
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ackman, R.G. and Hooper, S.N. (1973) Non-methylene-interrupted fatty acids in lipids of shallow-water marine invertebrates: a comparison of two molluscs (Littorina littorea and Lunatia triseriata) with the sand shrimp (Crangon septemspinosus). Comparative Biochemstry and Physiology 46B, 153–165.Google Scholar
Campbell, B.J., Stein, J.L. and Cary, S.C. (2003) Evidence of chemolithoautotrophy in the bacterial community associated with Allvinella pompejana, a hydrothermal vent polychaete. Applied and Environmental Microbiology 69, 5070–5078.Google Scholar
Conway, N. and Capuzzo, J.M. (1991) Incorporation and utilization of bacterial lipids in the Solemya velum symbiosis. Marine Biology 108, 277–291.CrossRefGoogle Scholar
Conway, N.M., Howes, B.L., McDowell Capuzzo, J.E., Turner, R.D. and Cavanaugh, C.M. (1992) Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve–bacteria symbiosis. Marine Biology 112, 610–613.Google Scholar
Desbruyères, D., Chevaldonne, P., Alayse, A.-M., Jollivet, D., Lallier, F.H., Jouin-Toulmond, C., Zal, F., Sarradin, P.M., Cosson, R., Caprais, J.C., Arndt, C., O'Brien, J., Guezennec, J., Hourdez, S., Riso, R., Gaill, F., Laubier, L. and Toulmond, A. (1998) Biology and ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal dweller of an extreme deep-sea environment: a synthesis of current knowledge and recent developments. Deep-Sea Research II 45, 383–422.CrossRefGoogle Scholar
Distel, D.L. (1998) Evolution of chemoautotrophic endosymbioses in bivalves. BioScience 48, 277–286.CrossRefGoogle Scholar
Enright, J.T., Newman, W.A., Hessler, R.R. and McGowan, J.A. (1981) Deep-ocean hydrothermal vent communities. Nature 289, 219–220.CrossRefGoogle Scholar
Fullarton, J.G., Southward, A.J., Dando, P.R., Sargent, J. and Southward, E.C. (1995) Fatty acids of hydrothermal vent Ridgeia piscesae and inshore bivalves containing symbiotic bacteria. Journal of the Marine Biological Association of the United Kingdom 75, 455–468.CrossRefGoogle Scholar
Gail, F., Desbruyères, D. and Prieur, D. (1987) Bacterial communities associated with “Pompei worms” from the East Pacific Rise hydrothermal vents: SEM, TEM observations. Microbial Ecology 13, 129–139.CrossRefGoogle Scholar
Gardner, D. and Riley, J.P. (1972) The component fatty acids of the lipids of some species of marine and freshwater molluscs. Journal of the Marine Biological Association of the United Kingdom 52, 827–838.Google Scholar
Gebruk, A.V., Pimenov, A.V. and Savvichev, A.S. (1993) Feeding specialization of bresiliid shrimps in the TAG site hydrothermal community. Marine Ecology Progress Series 98, 247–253.CrossRefGoogle Scholar
Giovannoni, S.J., DeLong, E.F., Olsen, G.J. and Pace, N.R. (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. Journal of Bacteriology 170, 720–726.Google Scholar
Goffredi, S.K., Waren, A., Orphan, V.J., Van Dover, C.L. and Vrijenhoek, R.C. (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Applied and Environmental Microbiology 70, 3082–3090.Google Scholar
Haddad, A., Camacho, F., Durand, P. and Cary, S.C. (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Applied and Environmental Microbiology 61, 1679–1687.CrossRefGoogle ScholarPubMed
Hurlbelt, S.H. (1971) The non-concept of species diversity: a critique and alternative parameters. Ecology 52, 577–586.CrossRefGoogle Scholar
Jones, D.S. (1993) A new Neolepas (Cirripedia: Thoacica: Scalpellidae) from an abyssal hydrothermal vent, Southeast Pacific. Bulletin of Marine Science 52, 37–948.Google Scholar
Komagata, K. and Suzuki, K. (1987) Lipid and cell-wall analysis in bacterial systematics. Methods in Microbiology 19, 161–207.CrossRefGoogle Scholar
Lane, D.J. (1991) 16S/23S rRNA sequencing. In Stackebrandt, E. and Goodfellow, M. (eds) Nucleic acid techniques in bacterial systematics. New York: John Wiley and Sons, pp. 115–175.Google Scholar
Lathe, R. (1985) Synthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. Journal of Molecular Biology 183, 1–12.Google Scholar
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lüßmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A. and Schleifer, K.-H. (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32, 1363–1371.Google Scholar
Manz, W., Amann, R., Ludwig, W., Wagner, M. and Schleifer, K.-H. (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Systematic and Applied Microbiology 15, 593–600.Google Scholar
Manz, W., Amann, R., Ludwig, W., Vancanneyt, M. and Schleifer, K.-H. (1996) Application of a suit of 16S rRNA-specific oligonucleotide probes designed to bacteria of the phylum Cytophaga–Flavobacterium–Bacteroides in the natural environment. Microbiology 142, 1097–1106.Google Scholar
Newman, W.A. (1979) A new scalpellid (Cirripedia); a Mesozoic relic living near an abyssal hydrothermal spring. Transactions of the San Diego Society of Natural History 19, 53–167.Google Scholar
Newman, W.A. and Yamaguchi, T. (1995) A new sessile barnacle (Cirripedia, Brachylopadomorpha) from the Lau-Arc Basin, Tonga; first record of a living representative since the Miocene. Bulletin du Muséum National d'Historie Naturelle, Paris, serie 4 17A, 221–243.Google Scholar
Nichols, P.D., Guckert, J.B. and White, D.C. (1986) Determination of monounsaturated fatty acid double-bond position and geometry for microbial monocultures and complex consortia by capillary GC-MS of their dimethyl disulphide adducts. Journal of Microbiological Methods 5, 49–55.Google Scholar
Polz, M.F. and Cavanaugh, C.M. (1995) Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proceedings of the National Academy of Science of the United States of America 92, 7232–7236.Google Scholar
Polz, M.F., Robinson, J. and Cavanaugh, C.M. (1998) Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnology and Oceanography 43, 1631–1638.CrossRefGoogle Scholar
Pond, D.W., Bell, M.V., Dixon, D.R., Fallick, A.E., Segonzac, M. and Sargent, J.R. (1998) Stable-carbon-isotope composition of fatty acids in hydrothermal vent mussels containing methanotrophic and thiotrophic bacterial endosymbionts. Applied and Environmental Microbiology 64, 370–375.CrossRefGoogle ScholarPubMed
Pond, D.W., Gebruk, A., Southward, E.C., Southward, A.J., Fallick, A.E., Bell, M.V. and Sargent, J.R. (2000) Unusual fatty acid composition of storage lipids in the bresilioid shrimp Rimicaris exoculata couples the photic zone with MAR hydrothermal vent sites. Marine Ecology Progress Series 198, 171–179.Google Scholar
Pranal, V., FialaMedioni, A. and Guezennec, J. (1996) Fatty acid characteristics in two symbiotic gastropods from a deep hydrothermal vent of the west Pacific. Marine Ecology Progress Series 142, 175–184.CrossRefGoogle Scholar
Pranal, V., FialaMedioni, A. and Guezennec, J. (1997) Fatty acid characteristics in two symbiont-bearing mussels from deep-sea hydrothermal vents of the south-western Pacific. Journal of the Marine Biological Association of the United Kingdom 77, 473–492.CrossRefGoogle Scholar
Segonzac, M., de Saint Laurent, M. and Casanova, B. (1993) L'énigme du comportement trophique des crevettes Alvinocaridae des sites hydrothermaux de la dorsale médio-atlantique. Cahier de Biologie Marine 34, 535–571.Google Scholar
Southward, A.J. and Newman, W.A. (1998) Ectosymbiosis between filamentous sulphur bacteria and a stalked barnacle (Scalpellomorpha, Neolepadinae) from the Lau Back Arc Basin, Tonga. Cahier de Biologie Marine 39, 259–262.Google Scholar
Southward, A.J., Newman, W.A., Schiere, D. and Tunnicliffe, V. (1997) Biological indicators confirm hydrothermal venting on the Southeast Indian Ridge. BRIDGE Newsletter 12, 35–39.Google Scholar
Suzuki, Y., Sasaki, T., Suzuki, M., Nealson, K.H. and Horikoshi, K. (2005a) Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: the genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiological Letter 249, 105–112.Google Scholar
Suzuki, Y., Sasaki, T., Suzuki, M., Nogi, Y., Miwa, T., Takai, K., Nealson, K.H. and Horikoshi, K. (2005b) Novel chemoautotrophic endosymbiosis between a member of the ɛ-Proteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Applied and Environmental Microbiology 71, 5440–5450.Google Scholar
Suzuki, Y., Kojima, S., Sasaki, T., Suzuki, M., Utsumi, T., Watanabe, H., Urakawa, H., Tsuchida, S., Nunoura, T., Hirayama, H., Takai, K., Nealson, K.H. and Horikoshi, K. (2005c) Host–symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the South West Pacific. Applied and Environmental Microbiology 72, 1388–1393.CrossRefGoogle Scholar
Suzuki, Y., Kojima, S., Watanabe, H., Suzuki, M., Tsuchida, S., Nunoura, T., Hirayama, H., Takai, K., Nealson, K.H. and Horikoshi, K. (2006) Single host and symbiont lineages of hydrothermal-vent gastropods, Ifremeria nautilei (Provannidae): biogeography and evolution. Marine Ecology Progress Series 315, 167–175.Google Scholar
Swofford, D.L. (1999) PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4.02 ed. Sunderland, MA: Sinauer Associates.Google Scholar
Takai, K. and Horikoshi, K. (2000) Rapid detection and quantification of members of the archaeal communities by quantitative PCR using fluorogenic probes. Applied and Environmental Microbiology 66, 5066–5072.Google Scholar
Takai, K., Oida, H., Suzuki, Y., Hirayama, H., Nakagawa, S., Nunoura, T., Inagaki, I., Nealson, K.H. and Horikoshi, K. (2004) Spatial distribution of marine Crenarchaeota group I in the vicinity of deep-sea hydrothermal systems. Applied and Environmental Microbiology 70, 2404–2413.CrossRefGoogle Scholar
Van Dover, C.L., Fry, B., Grassle, J.F., Humphris, S. and Rona, P.A. (1988) Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Marine Biology 98, 209–216.Google Scholar
Yamaguchi, T. and Newman, W.A. (1997) Eochionelasmus paquensis new species (Cirripedia, Balanomorpha) from 17°25′S, north of Easter Island: first record of a sessile hydrothermal barnacle from the East Pacific Rise. Journal of Crustacean Biology 17, 488–496.CrossRefGoogle Scholar
Zhang, C.L., Huang, Z., Cantu, J., Pancost, R.D., Brigmon, R.L., Lyons, T.W. and Sassen, R. (2005) Lipid biomarkers and carbon isotope signatures of a microbial (Beggiatoa) mat associated with gas hydrates in the Gulf of Mexico. Applied and Environmental Microbiology 71, 2106–2112.Google Scholar