Although a common reaction in anaerobic environments, the conversion of formate and water to bicarbonate and H2 (with a change in Gibbs free energy of ΔG° = +1.3 kJ mol−1) has not been considered energetic enough to support growth of microorganisms. Recently, experimental evidence for growth on formate was reported for syntrophic communities of Moorella sp. strain AMP and a hydrogen-consuming Methanothermobacter species and of Desulfovibrio sp. strain G11 and Methanobrevibacter arboriphilus strain AZ1. The basis of the sustainable growth of the formate-users is explained by H2 consumption by the methanogens, which lowers the H2 partial pressure, thus making the pathway exergonic2. However, it has not been shown that a single strain can grow on formate by catalysing its conversion to bicarbonate and H2. Here we report that several hyperthermophilic archaea belonging to the Thermococcus genus are capable of formate-oxidizing, H2-producing growth. The actual ΔG values for the formate metabolism are calculated to range between −8 and −20 kJ mol−1 under the physiological conditions where Thermococcus onnurineus strain NA1 are grown. Furthermore, we detected ATP synthesis in the presence of formate as a sole energy source. Gene expression profiling and disruption identified the gene cluster encoding formate hydrogen lyase, cation/proton antiporter and formate transporter, which were responsible for the growth of T. onnurineus NA1 on formate. This work shows formate-driven growth by a single microorganism with protons as the electron acceptor, and reports the biochemical basis of this ability.
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This work was supported by the KORDI in-house programme (PE98513), the Marine and Extreme Genome Research Center programme and the Development of Biohydrogen Production Technology using Hyperthermophilic Archaea programme of the Ministry of Land, Transport, and Maritime Affairs, Korea, as well as by the Molecular and Cell Biology programme of RAS and the Russian Foundation of Basic Research (grant no. 10-04-01180). We thank J. Querellou and the crew of the French scientific vessel Pourquoi pas?, and A.-L. Reysenbach and the crew of the American scientific vessel Thomas G. Thompson for opportunities to obtain deep-sea samples. We thank W. B. Whitman and R. K. Thauer for comments on the manuscript, and S. G. Jeon, K.-B. Yi and J.-G. Na for discussions.
The authors declare no competing financial interests.
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