Something old, something new, something borrowed, something blue: the anaerobic microbial ancestry of aerobic respiration.

Abstract

Aerobic respiration evolved by bricolage, with modules cobbled together as microbial biochemistry coevolved with Earth's geochemistry. The mitochondrial electron transport chain represents a patchwork of respiratory modules inherited from microbial methanogenesis, iron oxidation, anoxygenic photosynthesis, and denitrification pathways, and preserves a biochemical record of Earth's redox environment over its four-billion-year history. Imprints of the anoxic early Earth are recognizable in Complex I's numerous iron-sulfur cofactors and vestigial binding sites for ferredoxin, nickel-iron, and molybdopterin, whereas the more recent advent of oxygen as a terminal electron acceptor necessitated use of heme and copper cofactors by Complex IV. Bricolage of respiratory complexes resulted in supercomplexes for improved electron transfer efficiency in some bacteria and archaea, and in many eukaryotes. Accessory subunits evolved to wrap mitochondrial supercomplexes for improved assembly and stability. Environmental microbes with 'fossil' proteins that are similar to ancestral forms of the respiratory complexes deserve further scrutiny and may reveal new insights on the evolution of aerobic respiration.