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A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile

Present address: Faculty of Environmental Engineering, The University of Kitakyushu, Japan.

Present address: Faculty of Life Sciences, Tokyo University of Agriculture, Japan.

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02 Feb 2018: Vol. 359, Issue 6375, pp. 559-563 DOI: 10.1126/science.aao3407
Takuro Nunoura
Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Yoshito Chikaraishi
Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Institute of Low Temperature Science, Hokkaido University, Kita-19, Nishi-8, Kita-ku, Sapporo 060-0819, Japan.
Rikihisa Izaki
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Nishikyo-ku, Kyoto 615-8510, Japan.
Takashi Suwa
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Nishikyo-ku, Kyoto 615-8510, Japan.
Takaaki Sato
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Nishikyo-ku, Kyoto 615-8510, Japan.
Takeshi Harada
NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation (NITE), 2-49-10 Nishihara, Shibuya-ku, Tokyo 151-0066, Japan.
Koji Mori
NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation (NITE), 2-49-10 Nishihara, Shibuya-ku, Tokyo 151-0066, Japan.
Yumiko Kato
NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation (NITE), 2-49-10 Nishihara, Shibuya-ku, Tokyo 151-0066, Japan.
Masayuki Miyazaki
Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Shigeru Shimamura
Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Katsunori Yanagawa
Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Aya Shuto
Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Naohiko Ohkouchi
Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Nobuyuki Fujita
NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation (NITE), 2-49-10 Nishihara, Shibuya-ku, Tokyo 151-0066, Japan.
Yoshihiro Takaki
Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
Haruyuki Atomi
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Katsura, Nishikyo-ku, Kyoto 615-8510, Japan. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), 7 Goban-cho, Chiyoda-ku, Tokyo 102-0076, Japan.
Ken Takai
Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.

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About-face for citrate synthase

Classically, it is thought that citrate synthase only works in one direction: to catalyze the production of citrate from acetyl coenzyme A and oxaloacetate in the tricarboxylic acid (TCA) cycle. The TCA cycle can run in reverse to cleave citrate and fix carbon dioxide autotrophically, but this was thought to occur only with alternative enzymes, such as citrate lyase. Now Nunoura and Mall have discovered thermophilic bacteria with highly efficient and reversible citrate synthase that requires reduced ferredoxin (see the Perspective by Ragsdale). This function is undetectable by metagenomics, but classical biochemistry filled in the gaps seen between the genome sequences and the phenotypes of the organisms. The direction of catalysis depends on the availability of organic versus inorganic carbon and reflects a flexible bet-hedging strategy for survival in fluctuating environments. In evolutionary terms, this capacity might predate the classical TCA cycle and is likely to occur in a wide range of anaerobic microorganisms.

, this issue p. , p. 563 ; see also p.

Abstract

Inorganic carbon fixation is essential to sustain life on Earth, and the reductive tricarboxylic acid (rTCA) cycle is one of the most ancient carbon fixation metabolisms. A combination of genomic, enzymatic, and metabolomic analyses of a deeply branching chemolithotrophic ABI70S6 revealed a previously unknown reversible TCA cycle whose direction was controlled by the available carbon source(s). Under a chemolithoautotrophic condition, a rTCA cycle occurred with the reverse reaction of citrate synthase (CS) and not with the adenosine 5′-triphosphate–dependent citrate cleavage reactions that had been regarded as essential for the conventional rTCA cycle. Phylometabolic evaluation suggests that the TCA cycle with reversible CS may represent an ancestral mode of the rTCA cycle and raises the possibility of a facultatively chemolithomixotrophic origin of life.

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Science

Vol 359, Issue 637502 February 2018

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A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile

By Takuro Nunoura , Yoshito Chikaraishi , Rikihisa Izaki , Takashi Suwa , Takaaki Sato , Takeshi Harada , Koji Mori , Yumiko Kato , Masayuki Miyazaki , Shigeru Shimamura , Katsunori Yanagawa , Aya Shuto , Naohiko Ohkouchi , Nobuyuki Fujita , Yoshihiro Takaki , Haruyuki Atomi , Ken Takai

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