Phylogeny and Evolutionary History of Respiratory Complex I Proteins in Melainabacteria

The evolution of oxygenic photosynthesis was one of the most transformative evolutionary events in Earth's history, leading eventually to the oxygenation of Earth's atmosphere and, consequently, the evolution of aerobic respiration. Previous work has shown that the terminal electron acceptors (complex IV) of aerobic respiration likely evolved after the evolution of oxygenic photosynthesis. However, complex I of the respiratory complex chain can be involved in anaerobic processes and, therefore, may have pre-dated the evolution of oxygenic photosynthesis. If so, aerobic respiration may have built upon respiratory chains that pre-date the rise of oxygen in Earth's atmosphere. The Melainabacteria provide a unique opportunity to examine this hypothesis because they contain genes for aerobic respiration but likely diverged from the Cyanobacteria before the evolution of oxygenic photosynthesis. Here, we examine the phylogenies of translated complex I sequences from 44 recently published Melainabacteria metagenome assembled genomes and genomes from other Melainabacteria, Cyanobacteria, and other bacterial groups to examine the evolutionary history of complex I. We find that complex I appears to have been present in the common ancestor of Melainabacteria and Cyanobacteria, supporting the idea that aerobic respiration built upon respiratory chains that pre-date the evolution of oxygenic photosynthesis and the rise of oxygen.

Automated summary

The evolution of oxygenic photosynthesis led to the oxygenation of Earth's atmosphere and the evolution of aerobic respiration. Previous research suggests that complex IV of aerobic respiration evolved after oxygenic photosynthesis, but complex I may have pre-dated it. Melainabacteria, which diverged before oxygenic photosynthesis, may provide insight into the evolution of aerobic respiration.