Ultrastructural and molecular evidence for potentially symbiotic bacteria within the byssal plaques of the deep-sea hydrothermal vent mussel Bathymodiolus azoricus
- 160 Downloads
This study reports on the presence of a putatively symbiotic bacterial flora within the byssus plaque of the deep sea hydrothermal mussel Bathymodiolus azoricus, contributing to metal sequestration/deposition and testing positive to methane oxidizing symbiont-specific fluorescent probes. Combining an array of approaches including histology, electron microscopy, X-ray microanalysis, analytical chemistry, and microbiology we provide evidence for the frequently assumed, but rarely shown influence of prokaryotes on the biogeochemical cycling of metals as well as inorganic C sources (i.e., methane) at deep sea hydrothermal vents. Our results indicate that in spite of its antibacterial protective sheath, the byssus plaque gives access to a whole range of prokaryotic organisms which may be responsible for the extremely high concentration of metallic elements (Fe, Cu, Zn, Mn, Co, Mo, Cd, Pb and Hg) measured in this attachment organ. The very high levels of metals in byssus, together with its frequent renewal rate due to the dynamic nature of the habitat, suggest that intra-byssal bacteria may have a major influence on biomineralisation/deposition of metals. The presence of a methanotroph morphotype within the byssus plaque was confirmed by FISH and TEM. The implications of the biogeochemical cycling of metals and methane at hydrothermal vents are discussed.
KeywordsHydrothermal vent Bathymodiolus azoricus Biomineralisation Byssus Endosymbiont Fe-oxidising bacteria
This study was undertaken under the framework of SEAHMA (PDCTM/P/MAR/15281/1999) and FISIOVENT-Physiological adaptations to extreme conditions at deep sea hydrothermal vents, project (POCTI/MAR/55547/2004) funded by FCT, Portugal. The Pluriannual and Programatic funding schemes of FCT-MCTES and DRCT-Azores to the R&D Unit #531 are acknowledged. Postdoctoral fellowship was awarded to Eniko Kadar (SFRH-BPD-19625/2004) and to Raul Bettencourt (SFRH/BPD/14896/2004) by FCT. We thank the crew of R/V Atalante, the ROV team and the crew of R/V Arquipelago for technical assistance during sample collection. Domitilia Rosa is acknowledged for her assistance in the histological preparations.
- Charlou JL, Donval JP, Douville E, Jean-Baptiste P, Radford-Knoery J, Fouquet Y, Dapoigny A, Stievenard M (2000) Compared geochemical signatures and the evolution of M. Gwen 37 degrees 50 ‘ N and Lucky Strike 37 degrees 17 ‘ N hydrothermal fluids, south of the Azores Triple Junction on the Mid-Atlantic Ridge. Chem Geol 171:49–75CrossRefGoogle Scholar
- Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Medioni A, Amann R, Dubilier N (2005) Dual symbiosis in a Bathymodiolus sp. Mussel from a methane seep on the Gaboncontinental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71:1694–1700PubMedCrossRefGoogle Scholar
- Fiala-Medioni A, Lepennec M (1987) Trophic structural adaptations in relation to the bacterial association of bivalve mollusks from hydrothermal vents and subduction zones. Symbiosis 4:63–74Google Scholar
- Fisher CR (1990) Chemoautotrophic and methanotrophicsymbioses in marine invertebrates. Rev Aquat Sci 2:399–613Google Scholar
- Kádár E, Costa V, Santos RS, Powell JJ (2006b) Tissue partitioning of micro-essential metals in the vent bivalve Bathymodiolus azoricus and associated organisms (endosymbiont bacteria and parasite polychaete) from geochemically distinct vents of the Mid-Atlantic Ridge. J Sea Res 56:45–52CrossRefGoogle Scholar
- Kádár E, Bettencourt R, Lobo-Da-Cunha A (2006f) Symbiotic gamma-proteobacteria in digestive gland of the vent mussel Bathymodiolus azoricus. Cah Biol Mar 47:429–434Google Scholar
- Kádár E, Davis SA, Lobo-da-Cunha A (in press) Cytoenzymatic investigation of intracellular digestion in the symbiont-bearing hydrothermal bivalve Bathymodiolus azoricus. doi: 10.1007/s00227-007-0827-0
- Langmuir C, Humphris S, Fornari D, Van-Dover C, Von-Damm K, Tivey MK, Colodner D, Charlou JL, Desonie D, Wilson C, Fouquet Y, Klinkhammer G, Bougault H (1997) Hydrothermal vents near a mantle hot spot: The Lucky Strike vent field at 37 degrees N on the Mid-Atlantic Ridge. Earth Planet Sci Lett 148:69–91CrossRefGoogle Scholar
- Von Cosel R, Comtet T, Krylova EM (1999) Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vents on the Azores Triple Junction and the Logatchev hydrothermal field, Mid-Atlantic Ridge. Veliger 42:218–248Google Scholar