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Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10224-30. doi: 10.1073/pnas.1423979112. Epub 2015 May 15.

Acetogenesis from H2 plus CO2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist.

Author information

1
Japan Collection of Microorganisms/Microbe Division, RIKEN BioResource Center, and Biomass Research Platform Team, RIKEN Biomass Engineering Program Cooperation Division, RIKEN Center for Sustainable Resource Science, Ibaraki 305-0074, Japan; mohkuma@riken.jp.
2
Japan Collection of Microorganisms/Microbe Division, RIKEN BioResource Center, and Interdisciplinary Graduate School of Medicine and Engineering, University of Yamanashi, Yamanashi 400-8511, Japan;
3
Department of Food, Life, and Environmental Sciences, Yamagata University, Yamagata 997-8555, Japan;
4
Japan Collection of Microorganisms/Microbe Division, RIKEN BioResource Center, and.
5
Biomass Research Platform Team, RIKEN Biomass Engineering Program Cooperation Division, RIKEN Center for Sustainable Resource Science, Ibaraki 305-0074, Japan;
6
Japan Collection of Microorganisms/Microbe Division, RIKEN BioResource Center, and Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, United Kingdom; and.
7
Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, United Kingdom; and.
8
Japan Collection of Microorganisms/Microbe Division, RIKEN BioResource Center, and Department of Biological Sciences, Tokyo Institute of Technology, Tokyo 152-8550, Japan.

Abstract

Symbiotic associations of cellulolytic eukaryotic protists and diverse bacteria are common in the gut microbial communities of termites. Besides cellulose degradation by the gut protists, reductive acetogenesis from H2 plus CO2 and nitrogen fixation by gut bacteria play crucial roles in the host termites' nutrition by contributing to the energy demand of termites and supplying nitrogen poor in their diet, respectively. Fractionation of these activities and the identification of key genes from the gut community of the wood-feeding termite Hodotermopsis sjoestedti revealed that substantial activities in the gut--nearly 60% of reductive acetogenesis and almost exclusively for nitrogen fixation--were uniquely attributed to the endosymbiotic bacteria of the cellulolytic protist in the genus Eucomonympha. The rod-shaped endosymbionts were surprisingly identified as a spirochete species in the genus Treponema, which usually exhibits a characteristic spiral morphology. The endosymbionts likely use H2 produced by the protist for these dual functions. Although H2 is known to inhibit nitrogen fixation in some bacteria, it seemed to rather stimulate this important mutualistic process. In addition, the single-cell genome analyses revealed the endosymbiont's potentials of the utilization of sugars for its energy requirement, and of the biosynthesis of valuable nutrients such as amino acids from the fixed nitrogen. These metabolic interactions are suitable for the dual functions of the endosymbiont and reconcile its substantial contributions in the gut.

KEYWORDS:

adaptive evolution; endosymbiosis; metabolic interaction; single-cell genomics; spirochetes

PMID:
25979941
PMCID:
PMC4547241
DOI:
10.1073/pnas.1423979112
[Indexed for MEDLINE]
Free PMC Article

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