Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Formate-driven growth coupled with H2 production

Nature volume 467, pages 352–355 (2010)Cite this article

Subjects

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° = +1.3 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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Growth of T. onnurineus NA1 on formate.
Figure 2: Gene expression analysis in T. onnurineus NA1.
Figure 3: Quantitative RT–PCR analysis and gene disruption in T. onnurineus NA1.
Figure 4: Proposed mechanism.

Similar content being viewed by others

References

  1. Dolfing, J., Jiang, B., Henstra, A. M., Stams, A. J. M. & Plugge, C. M. Syntrophic growth on formate: a new microbial niche in anoxic environments. Appl. Environ. Microbiol. 74, 6126–6131 (2008)

    Article  CAS  Google Scholar 

  2. Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Rev. Microbiol. 7, 568–577 (2009)

    Article  CAS  Google Scholar 

  3. Andrews, S. C. et al. A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 143, 3633–3647 (1997)

    Article  CAS  Google Scholar 

  4. Böhm, R., Sauter, M. & Böck, A. Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol. Microbiol. 4, 231–243 (1990)

    Article  Google Scholar 

  5. Sauter, M., Bohm, R. & Böck, A. Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol. Microbiol. 6, 1523–1532 (1992)

    Article  CAS  Google Scholar 

  6. Bagramyan, K., Mnatsakanyan, N., Poladian, A., Vassilian, A. & Trchounian, A. The roles of hydrogenases 3 and 4, and the F0F1-ATPase, in H2 production by Escherichia coli at alkaline and acidic pH. FEBS Lett. 516, 172–178 (2002)

    Article  CAS  Google Scholar 

  7. Takács, M. et al. Formate hydrogenlyase in the hyperthermophilic archaeon, Thermococcus litoralis. BMC Microbiol. 8, 88 (2008)

    Article  Google Scholar 

  8. Schauer, N. L. & Ferry, J. G. Metabolism of formate in Methanobacterium formicicum. J. Bacteriol. 142, 800–807 (1980)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Baron, S. F. & Ferry, J. G. Reconstitution and properties of a coenzyme F420-mediated formate hydrogenlyase system in Methanobacterium formicicum. J. Bacteriol. 171, 3854–3859 (1989)

    Article  CAS  Google Scholar 

  10. Wood, G. E., Haydock, A. K. & Leigh, J. A. Function and regulation of the formate dehydrogenase genes of the methanogenic archaeon Methanococcus maripaludis. J. Bacteriol. 185, 2548–2554 (2003)

    Article  CAS  Google Scholar 

  11. Lupa, B., Hendrickson, E. L., Leigh, J. A. & Whitman, W. B. Formate-dependent H2 production by the mesophilic methanogen Methanococcus maripaludis. Appl. Environ. Microbiol. 74, 6584–6590 (2008)

    Article  CAS  Google Scholar 

  12. Lee, H. S. et al. The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J. Bacteriol. 190, 7491–7499 (2008)

    Article  CAS  Google Scholar 

  13. Thauer, R. K. & Morris, J. G. in The Microbes 1984 Part II, Prokaryotes and Eukaryotes (eds Kelly, D. P. & Carr, N. G.) 123–168 (Cambridge Univ. Press, 1984)

    Google Scholar 

  14. Schink, B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Zivanovic, Y. et al. Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol. 10, R70 (2009)

    Article  Google Scholar 

  16. Möller, S., Croning, M. D. R. & Apweiler, R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17, 646–653 (2001)

    Article  Google Scholar 

  17. Gardy, J. L. et al. PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21, 617–623 (2005)

    Article  CAS  Google Scholar 

  18. Sapra, R., Verhagen, M. F. & Adams, M. W. Purification and characterization of a membrane-bound hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 182, 3423–3428 (2000)

    Article  CAS  Google Scholar 

  19. Hedderich, R. & Forzi, L. Energy-converting [NiFe] hydrogenases: more than just H2 activation. J. Mol. Microbiol. Biotechnol. 10, 92–104 (2005)

    Article  CAS  Google Scholar 

  20. Jenney, F. E., Jr & Adams, M. W. Hydrogenases of the model hyperthermophiles. Ann. NY Acad. Sci. 1125, 252–266 (2008)

    Article  ADS  CAS  Google Scholar 

  21. Sokolova, T. G. et al. The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8, 317–323 (2004)

    Article  CAS  Google Scholar 

  22. Amend, J. P. & Shock, E. L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 175–243 (2001)

    Article  CAS  Google Scholar 

  23. Matsumi, R., Manabe, K., Fukui, T., Atomi, H. & Imanaka, T. Disruption of a sugar transporter gene cluster in a hyperthermophilic archaeon using a host-marker system based on antibiotic resistance. J. Bacteriol. 189, 2683–2691 (2007)

    Article  CAS  Google Scholar 

  24. Bae, S. S. et al. Thermoccoccus onnurineus sp. nov., a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area at the PACMANUS field. J. Microbiol. Biotechnol. 16, 1826–1831 (2006)

    CAS  Google Scholar 

  25. Holden, J. F. et al. Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the Northeastern Pacific Ocean. FEMS Microbiol. Ecol. 36, 51–60 (2001)

    Article  CAS  Google Scholar 

  26. Amaratunga, D. & Cabrera, J. Analysis of data from viral DNA microchips. J. Am. Stat. Assoc. 96, 1161–1170 (2001)

    Article  MathSciNet  Google Scholar 

  27. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264 (2003)

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Author notes

  1. Yun Jae Kim, Hyun Sook Lee, Eun Sook Kim and Seung Seob Bae: These authors contributed equally to this work.

Authors and Affiliations

  1. Korea Ocean Research & Development Institute, PO Box 29, Ansan 425-600, Korea,

    Yun Jae Kim, Hyun Sook Lee, Eun Sook Kim, Seung Seob Bae, Jae Kyu Lim, Sun-Shin Cha, Sang-Jin Kim, Kae Kyoung Kwon, Jung-Hyun Lee & Sung Gyun Kang

  2. Department of Marine Biotechnology, University of Science and Technology, Daejeon, 305-333, Korea

    Hyun Sook Lee, Seung Seob Bae, Jae Kyu Lim, Sun-Shin Cha, Sang-Jin Kim, Kae Kyoung Kwon, Jung-Hyun Lee & Sung Gyun Kang

  3. Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Nishikyo-ku, Kyoto 615-8510, Japan,

    Rie Matsumi, Tadayuki Imanaka & Haruyuki Atomi

  4. Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60-Letiya Oktyabrya 7/2, 117312, Moscow, Russia,

    Alexander V. Lebedinsky, Tatyana G. Sokolova, Darya A. Kozhevnikova & Elizaveta A. Bonch-Osmolovskaya

Authors
  1. Yun Jae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyun Sook Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun Sook Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seung Seob Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jae Kyu Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rie Matsumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexander V. Lebedinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tatyana G. Sokolova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Darya A. Kozhevnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sun-Shin Cha
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sang-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Kae Kyoung Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tadayuki Imanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Haruyuki Atomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Elizaveta A. Bonch-Osmolovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jung-Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Sung Gyun Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H.S.L., S.G.K. and J.-H.L. conceptualized and designed the experiments; Y.J.K., E.S.K. and S.S.B. performed most of the experiments with T. onurineus NA1 and analysed the data; J.K.L. contributed to the microarray and quantitative RT–PCR measurements; and K.K.K. performed gas analysis and analysed the data. T.G.S and D.A.K. performed growth experiments with Thermococcus strains other than T. onurineus NA1, and A.V.L. planned and analysed them. R.M., T.I. and H.A. contributed to developing a gene knockout system for T. onnurineus NA1. S.-S.C., E.A.B.-O. and S.-J.K. contributed critical comments on the manuscript. Y.J.K., H.S.L. and S.G.K. wrote the paper with input from the co-authors.

Corresponding authors

Correspondence to Jung-Hyun Lee or Sung Gyun Kang.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Tables 1-3 and Supplementary Figures 1-2 with legends. (PDF 304 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, Y., Lee, H., Kim, E. et al. Formate-driven growth coupled with H2 production. Nature 467, 352–355 (2010). https://doi.org/10.1038/nature09375

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09375

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology