Abstract
Thyasiridae are one of the less studied groups of chemosymbiotic bivalves. Here, we investigated symbioses in three different thyasirid species collected at three cold seeps from the Atlantic and Mediterranean. Phylogenetic analysis of bacterial 16S ribosomal RNA gene sequences demonstrated that each thyasirid species harbours a single phylotype of symbiont that belongs to a distinct lineage of putative sulphur-oxidizing Gammaproteobacteria. This result is confirmed by other marker genes (encoding 23S rRNA and APS reductase) and fluorescence in situ hybridization. This work highlights the diversity of bacteria involved in symbiosis with thyasirids and underlines the relevance of this group as a target for future symbiosis studies.
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References
Amann R, Blinder BJ, Olson RJ, Crisholm SW, Devereux R, Stahl DA (1990) Combination of 16s rRNA-target oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925
Brissac T, Rodrigues CF, Gros O, Duperron S (2010) Characterization of bacterial symbioses in Myrtea sp. (Bivalvia: Lucinidae) and Thyasira sp. (Bivalvia: Thyasiridae) from a cold seep in the eastern Mediterranean. Mar Ecol. doi:10.1111/j.1439-0485.2010.00413.x
Carlier A, Ritt B, Rodrigues CF, Olu K, Sarrazin J, Grall J, Clavier J (2010) Heterogeneous energetic pathway and carbon sources for deep eastern Mediterranean cold-seep communities. Mar Biol 157(11):2545–2565
Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci 90:5695–5699
Dando P, Spiro B (1993) Varying nutritional dependence of the thyasirid bivalves Thyasira sarsi and T. equalis on chemoautotrophic symbiotic bacteria, demonstrated by isotope ratios of tissue carbon and shell carbonate. Mar Ecol Prog Ser 92:151–158
Distel DL, Wood AP (1992) Characterization of the gill symbiont of Thyasira flexuosa (Thyasiridae: Bivalvia) by use of polymerase chain reaction and 16S rRNA sequence analysis. J Bacteriol 174:6317–6320
Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 5:725–740
Dufour SC (2005) Gill anatomy and the evolution of symbiosis in the bivalve family Thyasiridae. Biol Bull 208:200–212
Dufour SC, Felbeck H (2006) Symbiont abundance in thyasirids (Bivalvia) is related to particulate food and sulphide availability. Mar Ecol Pro Ser 320:185–194
Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Médioni A, Amann R, Dubilier N (2005) Dual symbiosis in Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71:1694–1700
Duperron S, Fiala-Medioni A, Caprais JC, Olu K, Sibuet M (2007) Evidence for chemoautotrophic symbiosis in a Mediterranean cold seep clam (Bivalvia: Lucinidae): comparative sequence analysis of bacterial 16S rRNA, APS reductase and RubisCO genes. FEMS Microbiol Ecol 59:64–70
Felsenstein J (1993) PHYLIP (phylogeny inference package) version 3.5c. Department of Genetics, University of Washington, Seattle
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
Fujiwara Y, Kato C, Masui N, Fujikura K, Kojima S (2001) Dual symbiosis in the cold-seep thyasirid clam Maorithyas hadalis from the hadal zone in the Japan Trench, western Pacific. Mar Ecol Prog Ser 214:151–159
Imhoff JF, Sahling H, Suling J, Kath T (2003) 16S rDNA-based phylogeny of sulphur-oxidizing bacterial endosymbionts in marine bivalves from cold-seeps environments. Mar Ecol Prog Ser 249:39–51
Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M, Matsuyama K, Takishita K, Kawato M, Uematsu K, Fujiwara Y, Sato T, Kato C, Kitagawa M, Kato I, Maruyama T (2007) Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol 17:881–886
MacAvoy SE, Carney RS, Fisher CR, Macko SA (2002) Use of chemosynthetic biomass by large, mobile, benthic predators in the Gulf of Mexico. Mar Ecol Prog Ser 225:65–78
Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM (2007) The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315:998–1000
Oliver PG, Rodrigues CF, Cunha MR (2011) Chemosymbiotic bivalves from the mud volcanoes of the Gulf of Cadiz, with descriptions of new Solemyidae, Lucinidae and Vesicomyidae. Zookeys (in press)
Olu-Le Roy K, Sibuet M, Fiala-Médioni A, Gofas S, Salas C, Mariotti A, Foucher JP, Woodside J (2004) Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes. Deep Sea Res I 51:1915–1936
Rodrigues CF, Webster G, Cunha MR, Duperron S, Weightman A (2010) Chemosynthetic bacteria found in bivalve species from mud volcanoes of the Gulf of Cadiz. FEMS Microbiol Ecol 73(3):486–499
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Stewart FJ, Young CR, Cavanaugh CM (2008) Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol Biol Evol 25(4):673–687
Taylor JD, Glover EA (2009) New lucinid bivalves from hydrocarbon seeps of the Western Atlantic (Mollusca: Bivalvia: Lucinidae). Steenstrupa 32(2):127–140
Taylor JD, Glover EA (2010) Chemosymbiotic bivalves. In: Kiel S (ed) The vent and seep biota, topics in geobiology, vol 33. Springer, Germany, pp 107–135
Taylor JD, Williams ST, Glover EA (2007) Evolutionary relationships of the bivalve family Thyasiridae (Mollusca: Bivalvia), monophyly and superfamily status. J Mar Biol Ass UK 87:565–574
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X–Windows interface: flexible strategies for multiple sequence alignments aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Won YJ, Jones WJ, Vrijenhoek RC (2008) Absence of cospeciation between deep-sea mytilids and their thiotrophic endosymbionts. J Shell Res 27(1):129–138
Acknowledgements
This research was supported by the European Commission Seventh Framework Programme (FP7/2007-2013) under the HERMIONE project number 226354, as well as ANR DEEP-OASES (ANRO6BDV005). Thanks are due to the chief scientists for the invitation to participate in the several cruises that allowed the collection of species here studied: Dr. Catherine Pierre, Dr. Antje Boetius and Dr. Michael Ivanov and a special thanks to Dr. Marina R. Cunha for providing the material from the Gulf of Cadiz. We are indebted to Dr. Graham Oliver from the National Museum of Wales (Cardiff, UK) for the taxonomic identifications. We thank Dr. Magali Zbinden (UMR 7138, UPMC) and IFR83 Biologie Intégrative for their help with electron microscopy.
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Rodrigues, C.F., Duperron, S. Distinct symbiont lineages in three thyasirid species (Bivalvia: Thyasiridae) from the eastern Atlantic and Mediterranean Sea. Naturwissenschaften 98, 281–287 (2011). https://doi.org/10.1007/s00114-011-0766-3
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DOI: https://doi.org/10.1007/s00114-011-0766-3