Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen

• Published in: The EMBO journal 1994-06, Vol.13 (11), p.2516-2525
• Main Authors: Castresana, J., Lübben, M., Saraste, M., Higgins, D.G.
• Format: Article
• Language: English
• Subjects: Aerobiosis; Amino Acid Sequence; Archaea; Aspergillus nidulans - enzymology; Bacteria - enzymology; Bacteriology; Biological and medical sciences; Biological Evolution; Conserved Sequence - genetics; Databases, Factual; Electron Transport Complex IV - classification; Electron Transport Complex IV - genetics; Fundamental and applied biological sciences. Psychology; Genetics; Humans; Microbiology; Models, Biological; Oxidoreductases; Sequence Alignment; Zea mays - enzymology
• ISSN: 0261-4189; 1460-2075
• DOI: 10.1002/j.1460-2075.1994.tb06541.x

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.