TY - JOUR
T1 - Adaptation of aerobic respiration to low O2 environments
AU - Han, Huazhi
AU - Hemp, James
AU - Pace, Laura A.
AU - Ouyang, Hanlin
AU - Ganesan, Krithika
AU - Roh, Jung Hyeob
AU - Daldal, Fevzi
AU - Blanke, Steven R.
AU - Gennis, Robert B.
PY - 2011/8/23
Y1 - 2011/8/23
N2 - 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.
AB - 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.
KW - Cytochrome oxidase
KW - Evolution
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U2 - 10.1073/pnas.1018958108
DO - 10.1073/pnas.1018958108
M3 - Article
C2 - 21844375
AN - SCOPUS:79960581689
SN - 0027-8424
VL - 108
SP - 14109
EP - 14114
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 34
ER -