Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-18T16:19:49.253Z Has data issue: false hasContentIssue false
  • English
  • Français

Epibiotic association between filamentous bacteria and the vent-associated galatheid crab, Shinkaia crosnieri (Decapoda: Anomura)

Published online by Cambridge University Press:  24 November 2010

Shinji Tsuchida ,
Yohey Suzuki ,
Yoshihiro Fujiwara ,
Masaru Kawato ,
Katsuyuki Uematsu ,
Toshiro Yamanaka ,
Chitoshi Mizota  and
Hiroyuki Yamamoto
Shinji Tsuchida*
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Yohey Suzuki
Affiliation:
National Institute of Advanced Industrial Science and Technology, 1-1, Higashi 1-chome, Tsukuba-shi, Ibaraki 305-8567, Japan
Yoshihiro Fujiwara
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Masaru Kawato
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Katsuyuki Uematsu
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Toshiro Yamanaka
Affiliation:
Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima-naka, Okayama 700-8530, Japan
Chitoshi Mizota
Affiliation:
Faculty of Agriculture, Iwate University, Ueda 3-18-8, Morioka, Iwate 020-8550, Japan
Hiroyuki Yamamoto
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
*
Correspondence should be addressed to: S. Tsuchida, Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The galatheid crab Shinkaia crosnieri, is the sole member of the subfamily Shinkaiinae. It is abundant and forms dense beds around active hydrothermal vents in the Okinawa Trough. Thousands of filamentous bacteria attached to the plumose setae on the ventral surface of this crab were observed using field-emission scanning electron microscopy and transmission electron microscopy. Nucleic acids were extracted from the filamentous bacteria, and the phylotypes of 16S rRNA genes were identified from 81 clones. These phylotypes were divided into three groups: Epsilonproteobacteria (74%); Gammaproteobacteria (20%); and Bacteroidetes (6%). Gamma- and major phylotypes of Epsilonproteobacteria were also detected using fluorescence in situ hybridization analysis. These Epsilon- and Gammaproteobacteria were closely related to cultured and uncultured bacteria from hydrothermal vent fields including episymbionts of vent-associated invertebrates such as Rimicaris exoculata, Alvinella pompejana, the scaly-foot snail, Kiwa hirsuta etc. The carbon isotopic compositions of the muscle of S. crosnieri and in filamentous bacteria were similar. The muscle of S. crosnieri contained monounsaturated C16 and C18 fatty acids, which are known to be characteristic of sulphur-oxidizing bacteria in H2S-rich marine habitats. Through the video images transmitted by a submersible and a remotely operated vehicle, S. crosnieri was observed to comb out its ventral setae using the third maxilliped and appeared to consume the contents. These evidences suggest the epibiotic association between S. crosnieri and the filamentous bacteria attached to the ventral setae of the crab, but the details of role and function are still unclear at the present study.

Keywords

Shinkaia crosnieriepibionthydrothermal ventOkinawa TroughHatoma KnollEpsilonproteobacteriaGammaproteobacteria
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 1 , February 2011 , pp. 23 - 32
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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

Amann, R. and Fuchs, B.M. (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Reviews Microbiology 6, 339–348.CrossRefGoogle ScholarPubMed
Baba, K. and Williams, A.B. (1998) New galatheoidea (Crustacea, Decapoda, Anomura) from hydrothermal systems in the West Pacific Ocean: Bismarck Archipelago and Okinawa Trough. Zoosystema 20, 143–156.Google Scholar
Brazelton, W.J., Schrenk, M.O., Kelley, D.S. and Baross, J.A. (2006) Methane- and sulfur-metabolizing microbial communities dominate the Lost City hydrothermal field ecosystem. Applied and Environmental Microbiology 72, 6257–6270.CrossRefGoogle ScholarPubMed
Campbell, B.J., Jeanthon, C., Kostka, J.E., Luther, G.W.III and Cary, S.C. (2001) Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Applied and Environmental Microbiology 67, 4566–4572.CrossRefGoogle Scholar
Cary, S.C., Cottrell, M.T., Stein, J.L., Camacho, F. and Desbruyères, D. (1997) Molecular identification and localization of filamentous symbiotic bacteria associated with the hydrothermal vent annelid Alvinella pompejana. Applied and Environmental Microbiology 63, 1124–1130.CrossRefGoogle ScholarPubMed
Chan, T.-Y., Lee, D.-A., and Lee, C.-S. (2000) The first deep-sea hydrothermal animal reported from Taiwan: Shinkaia crosnieri Baba and Williams, 1998 (Crustacea: Decapoda: Galatheidae). Bulletin of Marine Science 67, 799–804.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 (Bivalvvia; Solemyidae), another bivalve–bacteria symbiosis. Marine Biology 112, 601–613.CrossRefGoogle Scholar
Conway, N.M., Kennicutt, M.C.II and Van Dover, C.L. (1994) Stable isotopes in the study of marine chemosynthetic-based ecosystems. In Lajtha, K. and Michener, R.H. (eds) Stable isotopes in ecology and environmental science. Oxford: Blackwell Scientific Publications, pp. 158–186.Google Scholar
Cubelio, S.S., Tsuchida, S. and Watanabe, S. (2007) New species of Munidopsis (Decapoda: Anomura Galatheidae) from hydrothermal vent in Okinawa Trough and cold seep in Sagami Bay. Crustacean Research 36, 1–14.CrossRefGoogle Scholar
Dhillon, A., Teske, A., Dillon, J., Stahl, D.A. and Sogin, M.L. (2003) Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Applied and Environmental Microbiology 69, 2765–2772.CrossRefGoogle ScholarPubMed
Drazen, J.C., Phleger, C.F., Guest, M.A. and Nichols, P.D. (2008) Lipid, sterols and fatty acids of abyssal polychaetes, crustaceans, and a cnidarian from the northeast Pacific Ocean: food web implications. Marine Ecology Progress Series 372, 157–167.CrossRefGoogle Scholar
Fujiwara, Y., Takai, T., Uematsu, K., Tsuchida, S., Hunt, J.C. and Hashimoto, J. (2000) Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels: influence on host distributions. Marine Ecology Progress Series 208, 147–155.CrossRefGoogle Scholar
Gaill, F. and Hunt, S. (1991) The biology of annelid worms from high-temperature hydrothermal vent regions. Reviews in Aquatic Sciences 4, 107–137.Google Scholar
Goffredi, S.K., Warèn, 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.CrossRefGoogle Scholar
Goffredi, S.K., Jones, W.J., Erhlich, H., Springer, A. and Vrijenhoek, R.C. (2008) Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environmental Microbiology 10, 2623–2634.CrossRefGoogle ScholarPubMed
Guindon, S., Lethiec, F., Duroux, P. and Gascuel, O. (2005) Phyml Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research 33, W557–W559.CrossRefGoogle ScholarPubMed
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
Inagaki, F., Takai, K., Nealson, K.H. and Horikoshi, K. (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ɛ-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. International Journal of Systematic and Evolutionary Microbiology 54, 1477–1482.CrossRefGoogle Scholar
Johnson, P.W., Sieburth, J.M., Sastry, A., Arnold, C.R. and Doty, M.S. (1971) Leucothrix mucor infection on benthic crustacea, fish eggs, and tropical algae. Limnology and Oceanography 16, 962–969.CrossRefGoogle Scholar
Komagata, K. and Suzuki, K. (1987) Lipid and cell wall analysis in bacterial systematics. Methods in Microbiology 19, 161–207.CrossRefGoogle Scholar
Kormas, K.A., Tivey, M.K., Von Damm, K. and Teske, A. (2006) Bacterial and archaeal phylotypes associated with distinct mineralogical layers of a white smoker spire from a deep-sea hydrothermal vent site (9°N, East Pacific Rise). Environmental Microbiology 8, 909–920.CrossRefGoogle Scholar
Lane, D.J. (1991) 16S/23S sequencing. In Stackebrandt, E. and Goodfellow, M. (eds) Nucleic acid techniques in bacterial systematics. Chichester: John Wiley & 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.CrossRefGoogle ScholarPubMed
Lemaitre, R. (2004) Discovery of the first hermit crab (Crustacea: Decapoda: Parapaguridae) associated with hydrothermal vents. Cahiers de Biologie Marine 5, 325–334.Google Scholar
Liu, C.-S., Morita, S., Liao, Y.-H., Ku, C.-K., Machiyama, H., Lin, S. and Soh, W. (2008) High-resolution seismic images of the Formosa Ridge off southwestern Taiwan where ‘Hydrothermal’ chemosynthetic community is present at a cold seep site. Proceedings of the 6th International Conference on Gas Hydrates (ICGH 2008), Vancouver, British Columbia, Canada, July 6–10, 2008.Google Scholar
López-García, P., Gaill, F. and Moreira, D. (2002) Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environmental Microbiology 4, 204–215.CrossRefGoogle ScholarPubMed
López-García, P., Duperron, S., Philippot, P., Foriel, J., Susini, J. and Moreira, J. (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environmental Microbiology 5, 961–976.CrossRefGoogle ScholarPubMed
Macpherson, E., Jones, W. and Segonzac, M. (2005) A new squat lobster family of Galatheoidea (Crustacea, Decapoda, Anomura) from the hydrothermal vents of the Pacific–Antarctic Ridge. Zoosystema 27, 709–723.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. Systematics and Applied Microbiology 15, 593–600.CrossRefGoogle Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between d15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.CrossRefGoogle Scholar
Miyake, H., Kitada, M., Tsuchida, S., Okuyama, Y. and Nakamura, K. (2007) Ecological aspects of hydrothermal vent animals in captivity at atmospheric pressure. Marine Ecology 28, 86–92.CrossRefGoogle Scholar
Mizota, C., Shimoyama, S. and Yamanaka, T. (1999) An isotopic characterization of sulfur uptake by benthic animals from Tsuyazaki inlet, northern Kyushu, Japan. Benthos Research 54, 81–85.CrossRefGoogle Scholar
Ohta, S. and Kim, D. (2001) Submersible observations of the hydrothermal vent communities on the Iheya Ridge, Mid Okinawa Trough, Japan. Journal of Oceanography 57, 663–677.CrossRefGoogle 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 Sciences of the United States of America 92, 7232–7236.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.CrossRefGoogle Scholar
Pranal, V., Fiala-Médioni, 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., Fiala-Médioni, 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
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 Microbiology Letters 249, 105–112.CrossRefGoogle ScholarPubMed
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 Proteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Applied and Environmental Microbiology 71, 5440–5450.CrossRefGoogle ScholarPubMed
Suzuki, Y., Suzuki, M., Tsuchida, S., Takai, K., Horikoshi, K., Southward, A.J., Newman, W.A. and Yamaguchi, T. (2009) Molecular investigations of the stalked barnacle Vulcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand. Journal of the Marine Biological Association of the United Kingdom 89, 727–733.CrossRefGoogle Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Tokuda, G., Yamada, A., Nakano, K., Arita, N.O. and Yamasaki, H. (2008) Colonization of Sulfurovum sp. on the gill surfaces of Alvinocaris longirostris, a deep-sea hydrothermal vent shrimp. Marine Ecology 29, 106–114.CrossRefGoogle Scholar
Tsuchida, S., Fujiwara, Y. and Fujikura, K. (2003) Distribution and population structure of the galatheid crab, Shinkaia crosnieri, in the southern Okinawa Trough. Japanese Journal of Benthology 58, 69–76.CrossRefGoogle Scholar
Van Dover, C.L. (2000) The ecology of deep-sea hydrothermal vents. Princeton: Princeton University Press.CrossRefGoogle Scholar
Warèn, A., Bengtson, S., Goffredi, S.K. and Van Dover, C.L. (2003) A hot-vent gastropod with iron sulfide dermal sclerites. Science 302, 107.CrossRefGoogle ScholarPubMed
Yamanaka, T., Mizota, C., Maki, Y., Fujikura, K. and Chiba, H. (2000) Sulfur isotope composition of soft tissues of deep-sea mussels, Bathymodiolus spp., in Japanese waters. Benthos Research 55, 63–68.CrossRefGoogle Scholar
Yamanaka, T., Mizota, C., Ishibashi, J., Nakayama, N., Morimoto, Y., Okamoto, K., Kosaka, A., Maki, Y., Tsunogai, U., Fujikura, K., Tsuchida, S. and Fujiwara, Y. (2002) Carbon, nitrogen and sulfur isotopic characterization of biological samples from chemo-synthetic communities in southern Okinawa, Japan. AGU fall meeting, Moscone Center, San Francisco, CA, USA.Google Scholar
Yanagisawa, F. and Sakai, H. (1983) Thermal decomposition of barium sulfate–vanadium pentaoxide–silica glass mixtures for preparation of sulfur dioxide in sulfur isotope ratio measurements. Analytical Chemistry 55, 985–987.CrossRefGoogle Scholar
Zhang, C.I., 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.CrossRefGoogle ScholarPubMed