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Phylogenomic Analysis Identifies a Sodium-Translocating Decarboxylating Oxidoreductase in Thermotogae

O. I. Klimchuk1, D. V. Dibrova2, and A. Y. Mulkidjanian1,2,3*

1School of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119991 Moscow, Russia

2Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991 Moscow, Russia

3School of Physics, Osnabrueck University, 49069 Osnabrueck, Germany; E-mail: amulkid@uos.de

* To whom correspondence should be addressed.

Received November 11, 2015; Revision received January 27, 2016
Bacterial sodium-dependent decarboxylases were the first enzymes exemplifying sodium-dependent bioenergetics. These enzyme complexes couple decarboxylation of organic acids with the export of sodium ions via a special membrane subunit. In 711 representative prokaryotic genomes, we have analyzed genomic neighborhoods of the genes that code the membrane subunit of sodium decarboxylases. In representatives of Thermotogae, the operons with the gene of this subunit lack the genes of subunits that perform non-oxidative decarboxylation. Instead, these operons contain the genes of alpha- and delta-subunits of decarboxylating oxidoreductases of alpha-ketoacids. The genes of beta- and gamma-subunits of the decarboxylating oxidoreductases were found within the genomes of respective Thermotogae species as separate, two-gene operons. We suggest that the described two operons code together for sodium-translocating decarboxylating oxidoreductases capable of coupling oxidative decarboxylation of alpha-ketoacids with the export of sodium ions, which is a novel type of bioenergetic coupling.
KEY WORDS: sodium transport, membrane bioenergetics, comparative genomics, phylogenetic analysis, ferredoxin, molecular evolution, anaerobic bacteria

DOI: 10.1134/S0006297916050059