Adaptation of aerobic respiration to low O2 environments

Huazhi Han, James Hemp, Laura A. Pace, Hanlin Ouyang, Krithika Ganesan, Jung Hyeob Roh, Fevzi Daldal, Steven R. Blanke, Robert B. Gennis

Research output: Contribution to journalArticle

Abstract

Aerobic respiration in bacteria, Archaea, and mitochondria is performed by oxygen reductase members of the heme-copper oxidoreductase superfamily. These enzymes are redox-driven proton pumps which conserve part of the free energy released from oxygen reduction to generate a proton motive force. The oxygen reductases can be divided into three main families based on evolutionary and structural analyses (A-, B- and C-families), with the B- and C-families evolving after the A-family. The A-family utilizes two proton input channels to transfer protons for pumping and chemistry, whereas the B- and C-families require only one. Generally, the B- and C-families also have higher apparent oxygen affinities than the A-family. Here we use whole cell proton pumping measurements to demonstrate differential proton pumping efficiencies between representatives of the A-, B-, and C-oxygen reductase families. The A-family has a coupling stoichiometry of 1 H+/e-, whereas the B- and C-families have coupling stoichiometries of 0.5 H+?e-. The differential proton pumping stoichiometries, along with differences in the structures of the protonconducting channels, place critical constraints on models of the mechanism of proton pumping. Most significantly, it is proposed that the adaptation of aerobic respiration to low oxygen environments resulted in a concomitant reduction in energy conservation efficiency, with important physiological and ecological consequences.

Original languageEnglish (US)
Pages (from-to)14109-14114
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number34
DOIs
StatePublished - Aug 23 2011

Keywords

  • Cytochrome oxidase
  • Evolution

ASJC Scopus subject areas

  • General

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