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Phylogenetic Analysis of Proteins Associated in the Four Major Energy Metabolism Systems: Photosynthesis, Aerobic Respiration, Denitrification, and Sulfur Respiration

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Abstract

The four electron transfer energy metabolism systems, photosynthesis, aerobic respiration, denitrification, and sulfur respiration, are thought to be evolutionarily related because of the similarity of electron transfer patterns and the existence of some homologous proteins. How these systems have evolved is elusive. We therefore conducted a comprehensive homology search using PSI-BLAST, and phylogenetic analyses were conducted for the three homologous groups (groups 1–3) based on multiple alignments of domains defined in the Pfam database. There are five electron transfer types important for catalytic reaction in group 1, and many proteins bind molybdenum. Deletions of two domains led to loss of the function of binding molybdenum and ferredoxin, and these deletions seem to be critical for the electron transfer pattern changes in group 1. Two types of electron transfer were found in group 2, and all its member proteins bind siroheme and ferredoxin. Insertion of the pyridine nucleotide disulfide oxidoreductase domain seemed to be the critical point for the electron transfer pattern change in this group. The proteins belonging to group 3 are all flavin enzymes, and they bind flavin adenine dinucleotide (FAD) or flavin mononucleotide (FMN). Types of electron transfer in this group are divergent, but there are two common characteristics. NAD(P)H works as an electron donor or acceptor, and FAD or FMN transfers electrons from/to NAD(P)H. Electron transfer functions might be added to these common characteristics by the addition of functional domains through the evolution of group 3 proteins. Based on the phylogenetic analyses in this study and previous studies, we inferred the phylogeny of the energy metabolism systems as follows: photosynthesis (and possibly aerobic respiration) and the sulfur/nitrogen assimilation system first diverged, then the sulfur/nitrogen dissimilation system was produced from the latter system.

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Acknowledgments

We are grateful to Dr. Hiromi Suzuki of Meiji University for helping us in the initial part of this study. We appreciate Dr. Takeshi Kawabata of NAIST for advising us of the PSI-BLAST homology search method and helping us to conduct it. Color version of all figures is available at http://sayer.lab.nig.ac.jp/∼tomiki/JME_metabolism/.

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Correspondence to Naruya Saitou.

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Tomiki, T., Saitou, N. Phylogenetic Analysis of Proteins Associated in the Four Major Energy Metabolism Systems: Photosynthesis, Aerobic Respiration, Denitrification, and Sulfur Respiration. J Mol Evol 59, 158–176 (2004). https://doi.org/10.1007/s00239-004-2610-2

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