A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea
Takunari Kono, Sandhya Mehrotra, Chikako Endo, Natsuko Kizu, Mami Matusda, Hiroyuki Kimura, Eiichi Mizohata, Tsuyoshi Inoue, Tomohisa Hasunuma, Akiho Yokota, Hiroyoshi Matsumura & Hiroki Ashida
Nature Communications 8, Article number: 14007 (2017)
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Archaeal biology Enzymes Metabolic pathways X-ray crystallography
Received: 06 April 2016 Accepted: 18 November 2016 Published online: 13 January 2017
Figure 4: Proposed RHP pathway and related metabolic processes in Archaea.
Abstract
Two enzymes are considered to be unique to the photosynthetic Calvin–Benson cycle: ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), responsible for CO2 fixation, and phosphoribulokinase (PRK). Some archaea possess bona fide RuBisCOs, despite not being photosynthetic organisms, but are thought to lack PRK. Here we demonstrate the existence in methanogenic archaea of a carbon metabolic pathway involving RuBisCO and PRK, which we term ‘reductive hexulose-phosphate’ (RHP) pathway. These archaea possess both RuBisCO and a catalytically active PRK whose crystal structure resembles that of photosynthetic bacterial PRK. Capillary electrophoresis-mass spectrometric analysis of metabolites reveals that the RHP pathway, which differs from the Calvin–Benson cycle only in a few steps, is active in vivo. Our work highlights evolutionary and functional links between RuBisCO-mediated carbon metabolic pathways in methanogenic archaea and photosynthetic organisms. Whether the RHP pathway allows for autotrophy (that is, growth exclusively with CO2 as carbon source) remains unknown.
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Author notes
Hiroyoshi Matsumura & Hiroki Ashida
These authors jointly supervised this work
Affiliations
Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama-cho, Ikoma, Nara 630-0192, Japan
Takunari Kono, Chikako Endo & Akiho Yokota
Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-Ku, Kobe 657-8501, Japan
Takunari Kono & Hiroki Ashida
Department of Biological Sciences, Birla Institute of Technology and Science, Pilani, Rajasthan 333031, India
Sandhya Mehrotra
Department of Applied Chemistry, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan
Natsuko Kizu, Eiichi Mizohata & Tsuyoshi Inoue
Department of Chemical Science and Engineering, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501, Japan
Mami Matusda & Tomohisa Hasunuma
Department of Geosciences, Faculty of Science, Shizuoka University, Shizuoka 422-8529, Japan
Hiroyuki Kimura
Research Institute of Green Science and Technology, Shizuoka University, Shizuoka 422-8529, Japan
Hiroyuki Kimura
Department of Biotechnology, College of Life Sciences, Ritsumeikan University, 1-1-1 Noji-higashi, Kusatsu, Shiga 525-8577, Japan
Hiroyoshi Matsumura
Contributions
T.K. designed experiments, performed enzymatic analyses for M. hungatei PRK and RuBisCO together with S.M., and performed enzyme assays of PHI and HPS. T.K. and C.E. performed activity assays of other archaeal RuBisCOs. N.K., E.M. and H.M. crystallized M. hungatei PRK and determined its structure. M.M. and T.H. performed the metabolomic analysis with 13C labelling of M. hungatei. T.I. supervised the structural analysis. H.K. cultured M. hungatei. A.Y. and H.A. designed experiments and supervised the study. T.K., H.M. and H.A. wrote the manuscript.
Competing interests
The authors declare no competing financial interests.
Corresponding authors
Correspondence to Hiroyoshi Matsumura or Hiroki Ashida.
