Phylogeny and Evolutionary History of Respiratory Complex I Proteins in Melainabacteria.

Christen Grettenberger,Jonathan A Eisen,Tyler J Mackey,Dawn Y Sumner,Anne D Jungblut

doi:10.3390/genes12060929

Christen Grettenberger, Jonathan A Eisen + Show 3 more

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https://doi.org/10.3390/genes12060929

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Abstract

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.

Highlights

In Earth’s history, in the Archaean, organisms evolved the ability to perform oxygenic photosynthesis [1,2,3,4,5,6]
As they interact with O2, complexes III and IV likely emerged after the advent of oxygenic photosynthesis
We retrieved Melainabacteria and Sericytochromatia genomes by selecting all genomes available in the Genomes from Earth’s Microbiome Catalog (GEMs) [15]

Summary

Introduction

In Earth’s history, in the Archaean, organisms evolved the ability to perform oxygenic photosynthesis [1,2,3,4,5,6]. The byproduct of this metabolic innovation, O2, led to a second transformative innovation, aerobic respiration, the use of previously trace amounts of O2 to fuel metabolic activities. As they interact with O2, complexes III and IV likely emerged after the advent of oxygenic photosynthesis Phylogenetic studies of these complexes from across the bacterial tree of life support the hypothesis that they evolved after the great oxidation event (GOE) [8,9]. One terminal oxidase (A-O2Red) may have been present before the divergence of major bacterial and archaeal phyla and before the evolution of oxygenic photosynthesis [10]

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