Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen.

Abstract

Cytochrome oxidase is a key enzyme in aerobic metabolism. All the recorded eubacterial (domain Bacteria) and archaebacterial (Archaea) sequences of subunits 1 and 2 of this protein complex have been used for a comprehensive evolutionary analysis. The phylogenetic trees reveal several processes of gene duplication. Some of these are ancient, having occurred in the common ancestor of Bacteria and Archaea, whereas others have occurred in specific lines of Bacteria. We show that eubacterial quinol oxidase was derived from cytochrome c oxidase in Gram‐positive bacteria and that archaebacterial quinol oxidase has an independent origin. A considerable amount of evidence suggests that Proteobacteria (Purple bacteria) acquired quinol oxidase through a lateral gene transfer from Gram‐positive bacteria. The prevalent hypothesis that aerobic metabolism arose several times in evolution after oxygenic photosynthesis, is not sustained by two aspects of the molecular data. First, cytochrome oxidase was present in the common ancestor of Archaea and Bacteria whereas oxygenic photosynthesis appeared in Bacteria. Second, an extant cytochrome oxidase in nitrogen‐fixing bacteria shows that aerobic metabolism is possible in an environment with a very low level of oxygen, such as the root nodules of leguminous plants. Therefore, we propose that aerobic metabolism in organisms with cytochrome oxidase has a monophyletic and ancient origin, prior to the appearance of eubacterial oxygenic photosynthetic organisms.

Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense

“…The position of branches of both types of haem-copper oxidase of Pyrobaculum is consistent with the proposed idea that the SoxB-type branch and the SoxM-type branch of haem-copper oxidases evolved from an early gene duplication preceding the divergence of archaea and bacteria (Fig. 7) (Castresana et al, 1994). The phylogenetic analysis of cytochrome b showed that thermophilic archaea are clearly divided from the bacterial branch.…”

“…Most terminal oxidases belong to the haem-copper oxidase family; a few of them belong to the cyanide-insensitive alternative oxidase group (Garcia-Horsman et al, 1994). Phylogenetic and biochemical analysis of haem-copper oxidases indicates that the haem-copper oxidase family can be divided into three groups: FixN-, SoxB-and SoxM-type (Castresana et al, 1994;Garcia-Horsman et al, 1994). Mitochondria have one SoxM-type terminal oxidase but a number of bacteria and archaea have multiple terminal oxidases and the regulation of multiple oxidases is the important factor in their adaptation to changes in oxygen tension in their habitat.…”

“…In general, FixN-type haem-copper oxidase is utilized for low oxygen tension (Castresana et al, 1994) and SoxM-type haem-copper oxidase for atmospheric oxygen tension. SoxB-type haem-copper oxidases are observed in extremely thermophilic or hyperthermophilic bacteria and archaea, and in halophilic archaea, but their general character is still in question.…”

Aerobic growth at nanomolar oxygen concentrations

“…Independent of these geological arguments, the history of oxidase enzymes places other constraints on the origins of aerobiosis (30,43,44). Although there is active debate on the phylogenetic history of oxidase enzymes, recent models (30,43,44) support an ancient origin, even before the evolution of oxygen-producing cyanobacteria (45). Without a cyanobacterial source, oxygen could have come from abiotic sources, such as the rainout and disproportionation (by catalase enzymes) of atmospherically produced H 2 O 2 at the Earth's surface.…”

Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes

“…Recent taxonomic study on COXs and NORs showed the congruence of A-type COX and 16S rRNA tree at the Archaea/Bacteria domain and suggested the presence of A-type COX in common ancestor (22). On the other hand, based on the assumption that NO was present in the atmosphere prior to O 2 , Castresana et al (23) suggested that NORs were the first respiratory enzymes to appear, and C-type COXs was evolved from NORs. Our structural data on NORs cannot clarify the order of the appearance of the respiratory enzymes.…”