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Phylogenomic Analysis of Type 1 NADH:Quinone Oxidoreductase

G. E. Novakovsky1, D. V. Dibrova2, and A. Y. Mulkidjanian1,2,3*

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

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

3Osnabrueck University, Department of Physics, 49069 Osnabrueck, Germany; E-mail: amulkid@uos.de, armen.mulkidjanian@uni-osnabrueck.de

* To whom correspondence should be addressed.

Received November 10, 2015; Revision received March 22, 2016
We performed phylogenomic analysis of the catalytic core of NADH:quinone oxidoreductases of type 1 (NDH-1). Analysis of phylogenetic trees, as constructed for the core subunits of NDH-1, revealed fundamental differences in their topologies. In the case of four putatively homologous ion-carrying membrane subunits, the trees for the NuoH and NuoN subunits contained separate archaeal clades, whereas subunits NuoL and NuoM were characterized by multiple archaeal clades spread among bacterial branches. Large, separate clades, which united sequences belonging to different archaeal subdomains, were also found for cytoplasmic subunits NuoD and NuoB, homologous to the large and small subunits of nickel-iron hydrogenases. A smaller such clade was also shown for subunit NuoC. Based on these data, we suggest that the ancestral NDH-1 complex could be present already at the stage of the Last Universal Cellular Ancestor (LUCA). Ancestral forms of membrane subunits NuoN and NuoH and cytoplasmic subunits NuoD, NuoB, and, perhaps NuoC, may have formed a membrane complex that operated as an ion-translocating membrane hydrogenase. After the complex attained the ability to reduce membrane quinones, gene duplications could yield the subunits NuoL and NuoM, which enabled translocation of additional ions.
KEY WORDS: proton bioenergetics, molecular evolution, respiration, protein complexes, quinone reduction, phylogenetic analysis

DOI: 10.1134/S0006297916070142