The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: Evolutionary implications

Alessandro Giuffrè, Gottfried Stubauer, Paolo Sarti, Maurizio Brunori, Walter G. Zumft, Gerhard Buse, Tewfik Soulimane

Research output: Contribution to journalArticlepeer-review

Abstract

We show that the heme-copper terminal oxidases of Thermus thermophilus (called ba3 and caa3) are able to catalyze the reduction of nitric oxide (NO) to nitrous oxide (N2O) under reducing anaerobic conditions. The rate of NO consumption and N2O production were found to be linearly dependent on enzyme concentration, and activity was abolished by enzyme denaturation. Thus, contrary to the eukaryotic enzyme, both T. thermophilus oxidases display a NO reductase activity (3.0 ± 0.7 mol NO/mol ba3 x min and 32 ± 8 mol NO/mol caa3 x min at [NO] ≃ 50 μM and 20°C) that, though considerably lower than that of bona fide NO reductases (300-4,500 mol NO/mol enzyme x min), is definitely significant. We also show that for ba3 oxidase, NO reduction is associated to oxidation of cytochrome b at a rate compatible with turnover, suggesting a mechanism consistent with the stoichiometry of the overall reaction. We propose that the NO reductase activity of T. thermophilus oxidases may depend on a peculiar Cu(B)/+ coordination, which may be revealed by the forthcoming three-dimensional structure. These findings support the hypothesis of a common phylogeny of aerobic respiration and bacterial denitrification, which was proposed on the basis of structural similarities between the Pseudomonas stutzeri NO reductase and the cbb3 terminal oxidases. Our findings represent functional evidence in support of this hypothesis.

Original languageEnglish
Pages (from-to)14718-14723
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume96
Issue number26
DOIs
Publication statusPublished - 21 Dec 1999
Externally publishedYes

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