Formate-driven growth coupled with H2 production

Yun Jae Kim, Hyun Sook Lee, Eun Sook Kim, Seung Seob Bae, Jae Kyu Lim, Rie Matsumi, Alexander V. Lebedinsky, Tatyana G. Sokolova, Darya A. Kozhevnikova, Sun Shin Cha, Sang Jin Kim, Kae Kyoung Kwon, Tadayuki Imanaka, Haruyuki Atomi, Elizaveta A. Bonch-Osmolovskaya, Jung Hyun Lee, Sung Gyun Kang

Research output: Contribution to journalArticle

139 Citations (Scopus)

Abstract

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° = +1.3kJmol-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 H 2 partial pressure, thus making the pathway exergonic. 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, H 2 -producing growth. The actual δG values for the formate metabolism are calculated to range between -8 and -20kJmol-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.

Original languageEnglish
Pages (from-to)352-355
Number of pages4
JournalNature
Volume467
Issue number7313
DOIs
Publication statusPublished - Sep 2010

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formic acid
Growth
Thermococcus
Bicarbonates
Moorella
Protons
Methanobrevibacter
Methanobacteriaceae
Desulfovibrio
Antiporters

All Science Journal Classification (ASJC) codes

  • General

Cite this

Kim, Y. J., Lee, H. S., Kim, E. S., Bae, S. S., Lim, J. K., Matsumi, R., ... Kang, S. G. (2010). Formate-driven growth coupled with H2 production. Nature, 467(7313), 352-355. https://doi.org/10.1038/nature09375

Formate-driven growth coupled with H2 production. / Kim, Yun Jae; Lee, Hyun Sook; Kim, Eun Sook; Bae, Seung Seob; Lim, Jae Kyu; Matsumi, Rie; Lebedinsky, Alexander V.; Sokolova, Tatyana G.; Kozhevnikova, Darya A.; Cha, Sun Shin; Kim, Sang Jin; Kwon, Kae Kyoung; Imanaka, Tadayuki; Atomi, Haruyuki; Bonch-Osmolovskaya, Elizaveta A.; Lee, Jung Hyun; Kang, Sung Gyun.

In: Nature, Vol. 467, No. 7313, 09.2010, p. 352-355.

Research output: Contribution to journalArticle

Kim, YJ, Lee, HS, Kim, ES, Bae, SS, Lim, JK, Matsumi, R, Lebedinsky, AV, Sokolova, TG, Kozhevnikova, DA, Cha, SS, Kim, SJ, Kwon, KK, Imanaka, T, Atomi, H, Bonch-Osmolovskaya, EA, Lee, JH & Kang, SG 2010, 'Formate-driven growth coupled with H2 production', Nature, vol. 467, no. 7313, pp. 352-355. https://doi.org/10.1038/nature09375
Kim YJ, Lee HS, Kim ES, Bae SS, Lim JK, Matsumi R et al. Formate-driven growth coupled with H2 production. Nature. 2010 Sep;467(7313):352-355. https://doi.org/10.1038/nature09375
Kim, Yun Jae ; Lee, Hyun Sook ; Kim, Eun Sook ; Bae, Seung Seob ; Lim, Jae Kyu ; Matsumi, Rie ; Lebedinsky, Alexander V. ; Sokolova, Tatyana G. ; Kozhevnikova, Darya A. ; Cha, Sun Shin ; Kim, Sang Jin ; Kwon, Kae Kyoung ; Imanaka, Tadayuki ; Atomi, Haruyuki ; Bonch-Osmolovskaya, Elizaveta A. ; Lee, Jung Hyun ; Kang, Sung Gyun. / Formate-driven growth coupled with H2 production. In: Nature. 2010 ; Vol. 467, No. 7313. pp. 352-355.
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