H2-dependent formate production by hyperthermophilic Thermococcales: an alternative to sulfur reduction for reducing-equivalents disposal

Type Article
Acceptance Date 2021 IN PRESS
Language English
Author(s) Le Guellec SebastienORCID1, Leroy Elodie1, Courtine DamienORCID1, Godfroy Anne1, Roussel ErwanORCID1
Affiliation(s) 1 : Ifremer, Univ Brest, CNRS, Laboratoire de Microbiologie des Environnements Extrêmes, Plouzané, France
Source The ISME Journal (1751-7362) (Springer Science and Business Media LLC) In Press
DOI 10.1038/s41396-021-01020-x
Keyword(s) Archaeal physiology, Environmental microbiology
Abstract

Removal of reducing equivalents is an essential catabolic process for all microorganisms to maintain their internal redox balance. The electron disposal by chemoorganotrophic Thermococcales generates H2 by proton reduction or H2S in presence of S0. Although in the absence of S0 growth of these (hyper)thermopiles was previously described to be H2-limited, it remains unclear how Thermococcales could be present in H2-rich S0-depleted habitats. Here, we report that 12 of the 47 strains tested, distributed among all three orders of Thermococcales, could grow without S0 at 0.8 mM dissolved H2 and that tolerance to H2 was always associated with formate production. Two conserved gene clusters coding for a formate hydrogenlyase (FHL) and a putative formate dehydrogenase-NAD(P)H-oxidoreductase were only present in H2-dependent formate producers, and were both systematically associated with a formate dehydrogenase and a formate transporter. As the reaction involved in this alternative pathway for disposal of reducing equivalents was close to thermodynamic equilibrium, it was strongly controlled by the substrates–products concentration ratio even in the presence of S0. Moreover, experimental data and thermodynamic modelling also demonstrated that H2-dependent CO2 reduction to formate could occur within a large temperature range in contrasted hydrothermal systems, suggesting it could also provide an adaptive advantage.

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Publisher's official version IN PRESS 14 1 MB Open access
Supplementary Information 13 19 MB Open access
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