Cited by 110Microbial Community Ecology and PhysiologyMarine Biology and Ecology ResearchMethane Hydrates and Related Phenomena

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

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Ponsard, Julie, Cambon-Bonavita, Marie-Anne, Zbinden, Magali, Lepoint, Gilles, Joassin, André, Corbari, Laure, Shillito, Bruce, Durand, Lucile +2 more·2013·The ISME Journal

Abstract

The shrimp Rimicaris exoculata dominates several hydrothermal vent ecosystems of the Mid-Atlantic Ridge and is thought to be a primary consumer harbouring a chemoautotrophic bacterial community in its gill chamber. The aim of the present study was to test current hypotheses concerning the epibiont's chemoautotrophy, and the mutualistic character of this association. In-vivo experiments were carried out in a pressurised aquarium with isotope-labelled inorganic carbon (NaH(13)CO(3) and NaH(14)CO(3)) in the presence of two different electron donors (Na(2)S(2)O(3) and Fe(2+)) and with radiolabelled organic compounds ((14)C-acetate and (3)H-lysine) chosen as potential bacterial substrates and/or metabolic by-products in experiments mimicking transfer of small biomolecules from epibionts to host. The bacterial epibionts were found to assimilate inorganic carbon by chemoautotrophy, but many of them (thick filaments of epsilonproteobacteria) appeared versatile and able to switch between electron donors, including organic compounds (heterotrophic acetate and lysine uptake). At least some of them (thin filamentous gammaproteobacteria) also seem capable of internal energy storage that could supply chemosynthetic metabolism for hours under conditions of electron donor deprivation. As direct nutritional transfer from bacteria to host was detected, the association appears as true mutualism. Import of soluble bacterial products occurs by permeation across the gill chamber integument, rather than via the digestive tract. This first demonstration of such capabilities in a decapod crustacean supports the previously discarded hypothesis of transtegumental absorption of dissolved organic matter or carbon as a common nutritional pathway.

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  1. Compe `re P, Jeuniaux C, Goffinet G. (2004). The integu- ment: morphology and biochemistry. In: Forest J, Van Vaupel Klein JC (eds). Treatise on Zoology, 1. Anatomy, Taxonomy and Biology, The Crustacea. vol. 1: Brill, Leiden, pp 59-144.

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Authors
Ponsard, J., Cambon-Bonavita, M.-A., Zbinden, M., Lepoint, G., Joassin, A., Corbari, L., Shillito, B., Durand, L., Cueff-Gauchard, V., & Compère, P.
Affiliations
  • University of Liège (BE)
  • Laboratoire de Microbiologie des Environnements Extrêmes UMR 6197 Ifremer-CNRS-UBO, BP70 , Plouzané, France
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Compère, Philippe
Venue
The ISME Journal
Published
2012-08-23
Volume
7
Issue
1
Pages
96-109
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
OpenAlex
W2030347912
Cited by
110
References
79
Citations by year
2026: 4 · 2024: 3 · 2023: 5 · 2022: 10 · 2021: 23 · 2020: 4 · 2019: 12 · 2018: 9 · 2017: 11 · 2016: 5 · 2015: 11 · 2014: 7 · 2013: 5
FWCI
6.50
Type
journal article
Language
en
Open access
Locations
  • The ISME Journal (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion)
  • Flanders Marine Institute (Flanders Marine Institute) (submittedVersion)
  • ORBi (University of Liège) (submittedVersion, other-oa)
Funders
  • Fonds De La Recherche Scientifique - FNRS
  • Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture
Topics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
  • Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
Keywords
Rimicaris exoculata, chemosynthetic bacteria, inorganic carbon fixation, hydrothermal vent shrimp, host-symbiont mutualism, Epsilonproteobacteria, Gammaproteobacteria, heterotrophic metabolism, energy storage, gill chamber, Decapoda, isotopic labeling
MeSH terms
Animals, Gills, Symbiosis, Gammaproteobacteria, Epsilonproteobacteria, Decapoda, Chemoautotrophic Growth, Carbon Cycle, Hydrothermal Vents

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