Photosystem II and terminal respiratory oxidases molecular machines operating in opposite directions

Abstract

In the thylakoid membrane of green plants, cyanobacteria and algae, photosystem II (PSII) uses light energy to split water and generate molecular oxygen. In the opposite process of the biochemical transformation of dioxygen, in heterotrophs, the terminal respiratory oxidases (TRO) are at the end of the respiratory chain in mitochondria and in plasma membrane of many aerobic bacteria reducing dioxygen back to water. Despite the different sources of free energy (light or oxidation of the substrates), energy conversion by these enzymes is based on the spatial organization of enzymatic reactions in which the conversion of water to dioxygen (and vice versa) involves the transfer of protons and electrons in opposite directions across the membrane, which is accompanied by generation of proton-motive force. Similar and distinctive features in structure and function of these important energy-converting molecular machines are described. Information about many fascinating parallels between the mechanisms of TRO and PSII could be used in the artificial light-driven water-splitting process and elucidation of energy conversion mechanism in protein pumps.

ROS Defense Systems and Terminal Oxidases in Bacteria

“…Each of the single-electron steps in the catalytic cycle of COX during the O 2 reduction in the BNC (heme a 3 /Cu B ) is associated with the transfer of ~1 pumped proton through the membrane. The catalytic cycle of heme-copper oxidases is a highly coordinated system of individual electrogenic stages of electron transfer from cytochrome c on the P-side of the membrane and substrate protons on the N-side through the protein matrix to the BNC, as well as the transfer of pumped protons from the N-side of the membrane through temporary loading proton sites to the external water phase [ 32 ].…”

“…The membrane-embedded terminal oxidases include the superfamily of heme-copper oxidases [ 13 , 14 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 ] and the family of copper-lacking bd -type oxidases (cytochrome bd ) [ 11 , 25 , 26 , 27 , 28 , 29 ]. All these oxidases couple the catalytic redox reaction to the generation of a proton motive force [ 30 , 31 , 32 ]. Unlike cytochrome bd [ 33 , 34 , 35 ], the heme-copper oxidases create the proton motive force not only due to the transfer of protons and electrons to the catalytic site from different sides of the membrane but also due to a unique mechanism of the proton pumping [ 36 , 37 ].…”

Proton Pumping and Non-Pumping Terminal Respiratory Oxidases: Active Sites Intermediates of These Molecular Machines and Their Derivatives

“…HCOs catalyze the transfer of electrons from quinols or cytochromes to oxygen with the formation of water coupled to the generation of proton motive force [ 2 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 ]. In contrast to bd -type oxidases, HCOs generate the proton motive force not only by the transfer of electrons and protons to the catalytic center from different sides of the membrane but also due to the unique ability for redox-coupled directed proton pumping through the membrane [ 23 ].…”

In Escherichia coli Ammonia Inhibits Cytochrome bo3 But Activates Cytochrome bd-I

“…Each one is composed of four different subunits, however the cytochromes are structurally and evolutionarily unrelated. Cytochrome bo 3 is a member of type A-1 of the heme-copper oxidase superfamily [11][12][13][14][15][16]. It carries the ubiquinol binding site, two hemes, b and o 3 , and a copper ion [17].…”