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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Acknowledgements
The authors thank Christophe Brandily, Françoise Lesongeur and Nadège Quintin for technical support, and Yves Fouquet, Karine Alain, Mohamed Jebbar, Jordan Hartunians and Jean-Pierre Donval for useful discussions. We are much indebted to anonymous referees for their helpful comments. We also thank Cécile Cathalot for providing hydrothermal fluid samples and Marie-Anne Cambon-Bonavita, chief scientist of BICOSE 1 and 2 cruises. All crew members and the Scientific Party were crucial in this effort, especially the ROV ‘Victor 6000’ and DSV ‘Nautile’ crews for the sampling efforts. Sébastien Le Guellec was supported by the ‘Laboratoire d’Excellence’ LabexMER (ANR-10-LABX-19) and co-funded by a grant from Ifremer and the Regional Council of Brittany. Elodie Leroy was supported by a grant from Ifremer.
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Le Guellec, S., Leroy, E., Courtine, D. et al. H2-dependent formate production by hyperthermophilic Thermococcales: an alternative to sulfur reduction for reducing-equivalents disposal. ISME J 15, 3423–3436 (2021). https://doi.org/10.1038/s41396-021-01020-x
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DOI: https://doi.org/10.1038/s41396-021-01020-x
