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

Type Article
Date 2013-01
Language English
Author(s) Ponsard Julie1, Cambon-Bonavita Marie-AnneORCID2, Zbinden Magali3, Lepoint Gilles4, Joassin Andre5, Corbari Laure6, Shillito Bruce3, Durand Lucile2, Cueff-Gauchard ValerieORCID2, Compere Philippe1
Affiliation(s) 1 : Univ Liege, Lab Morphol Fonct & Evolut, Dept Biol Ecol & Evolut, Ctr MARE, B-4000 Liege, Belgium.
2 : UBO, Lab Microbiol Environm Extremes, IFREMER, CNRS,UMR 6197, Plouzane, France.
3 : Univ Paris 06, Equipe Adaptat Milieux Extremes, CNRS, UMR 7138, Paris 05, France.
4 : Univ Liege, Lab Oceanol, Dept Biol Ecol & Evolut, Ctr MARE, B-4000 Liege, Belgium.
5 : Univ Liege, Lab Chim Coordinat & Radiochim, Dept Chim, B-4000 Liege, Belgium.
6 : Museum Natl Hist Nat, Equipe Especes & Speciat, CNRS, UMR 7138, Paris 05, France.
Source Isme Journal (1751-7362) (Nature Publishing Group), 2013-01 , Vol. 7 , N. 1 , P. 96-109
DOI 10.1038/ismej.2012.87
WOS© Times Cited 71
Keyword(s) autoradiography, chemosynthetic ectosymbiosis, Crustacea, isotopes, Rimicaris exoculata, transtegumental transfer
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. Invivo experiments were carried out in a pressurised aquarium with isotope-labelled inorganic carbon (NaH13CO3 and NaH14CO3) in the presence of two different electron donors (Na2S2O3 and Fe2þ) and with radiolabelled organic compounds (14C-acetate and 3H-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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Ponsard Julie, Cambon-Bonavita Marie-Anne, Zbinden Magali, Lepoint Gilles, Joassin Andre, Corbari Laure, Shillito Bruce, Durand Lucile, Cueff-Gauchard Valerie, Compere Philippe (2013). Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. Isme Journal, 7(1), 96-109. Publisher's official version : https://doi.org/10.1038/ismej.2012.87 , Open Access version : https://archimer.ifremer.fr/doc/00114/22507/