On the origin of respiration: electron transport proteins from archaea to man.

Abstract

All aerobic organisms use the exergonic reduction of molecular oxygen to water as primary source of metabolic energy. This reaction is catalyzed by membrane residing terminal heme/Cu-oxidases which belong to a superfamily of widely varying structural complexity between mitochondrial and bacterial members of this family. Over the last few years, considerable information from this and other laboratories accumulated also on archaeal respiratory chains and their terminal oxidases. In the following, the molecular and catalytic properties of the latter are discussed and compared to those from bacteria and eucarya under the aspect of their energy conserving capabilities and their phylogenetic relations. The Rieske iron-sulfur proteins being important functional constituents of energy transducing respiratory complexes are included in this study. A number of essential conclusions can be drawn. (1) Like bacteria, archaea can also contain split respiratory chains with parallel expression of separate terminal oxidases. (2) The functional core of all oxidases is the highly conserved topological motif of subunit I consisting of at least 12 membrane spanning helices with the 6 histidine residues of the heme/Cu-binding centers in identical locations. (3) Some archaeal oxidases are organized in unusual supercomplexes with other cytochromes and Rieske [2Fe2S] proteins. These complexes are likely to function as proton pumps, whereas on a structural basis several subunit I equivalents alone are postulated to be unable to pump protons. (4) The genes of two archaeal Rieske proteins have been cloned from Sulfolobus; phylogenetically they are forming a separate archaeal branch and suggest the existence of an evolutionary ancestor preceding the split into the three urkingdoms. (5) Archaeal oxidase complexes may combine features of electron transport systems occurring exclusively as separate respiratory complexes in bacteria and eucarya. (6) As far back as the deepest branches of the phylogentic tree, terminal oxidases reveal a degree of complexity comparable to that found in higher organisms. (7) Sequence analysis suggests a monophyletic origin of terminal oxidases with an early split into two types found in archaea as well as bacteria. This view implies an origin of terminal oxidases prior to oxygenic photosynthesis in contrast to the widely accepted inverse hypothesis.