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Genomic Analysis Reveals Multiple [FeFe] Hydrogenases and Hydrogen Sensors Encoded by Treponemes from the H2-Rich Termite Gut

Microbial Ecology volume 63, pages 282–294 (2012)Cite this article

Abstract

We have completed a bioinformatic analysis of the hydrogenases encoded in the genomes of three termite gut treponeme isolates: hydrogenotrophic, homoacetogenic Treponema primitia strains ZAS-1 and ZAS-2, and the hydrogen-producing, sugar-fermenting Treponema azotonutricium ZAS-9. H2 is an important free intermediate in the breakdown of wood by termite gut microbial communities, reaching concentrations in some species exceeding those measured for any other biological system. The spirochetes encoded 4, 8, and 5 [FeFe] hydrogenase-like proteins, identified by their H domains, respectively, but no other recognizable hydrogenases. The [FeFe] hydrogenases represented many sequence families previously proposed in an analysis of termite gut metagenomic data. Each strain encoded both putative [FeFe] hydrogenase enzymes and evolutionarily related hydrogen sensor/transducer proteins likely involved in phosphorelay or methylation pathways, and possibly even chemotaxis. A new family of [FeFe] hydrogenases (FDH-Linked) is proposed that may form a multimeric complex with formate dehydrogenase to provide reducing equivalents for reductive acetogenesis in T. primitia. The many and diverse [FeFe] hydrogenase-like proteins encoded within the sequenced genomes of the termite gut treponemes has enabled the discovery of a putative new class of [FeFe] hydrogenase proteins potentially involved in acetogenesis and furthered present understanding of many families, including sensory, of H domain proteins beyond what was possible through the use of fragmentary termite gut metagenome sequence data alone, from which they were initially defined.

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Acknowledgements

This research was supported by a grant from the NSF (MCB-0523267) and an NSF Graduate Student Research Fellowship (to NRB). The draft shotgun genome sequencing of T. primitia ZAS-1 was performed by Richard White and Stephen Quake at Stanford University, for which we are extremely grateful. We would like to thank our laboratory colleagues for their insightful comments during the preparation of this manuscript.

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Authors and Affiliations

  1. Biochemistry & Molecular Biophysics, Mailcode 138-78, California Institute of Technology, Pasadena, CA, 91125, USA

    Nicholas R. Ballor & Jared R. Leadbetter

  2. The Ronald & Maxine Linde Center for Global Environmental Science, Mailcode 138-78, California Institute of Technology, Pasadena, CA, 91125, USA

    Jared R. Leadbetter

  3. Department of Chemistry & Biomolecular Sciences, Macquarie University Sydney, Sydney, Australia

    Ian Paulsen

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  1. Nicholas R. Ballor
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Correspondence to Jared R. Leadbetter.

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Table S1

Primer sequences used in this study (PDF 288 KB)

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Ballor, N.R., Paulsen, I. & Leadbetter, J.R. Genomic Analysis Reveals Multiple [FeFe] Hydrogenases and Hydrogen Sensors Encoded by Treponemes from the H2-Rich Termite Gut. Microb Ecol 63, 282–294 (2012). https://doi.org/10.1007/s00248-011-9922-8

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Keywords

  • FeFe
  • Formate Dehydrogenase
  • Hydrogen Sensor
  • Hydrogenase Gene
  • Gene Cluster Analysis