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

Journal

TRENDS IN MICROBIOLOGY
Volume 31, Issue 2, Pages 135-141

Publisher

CELL PRESS
DOI: 10.1016/j.tim.2022.08.006

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Aerobic respiration evolved through bricolage, combining modules from microbial biochemistry and Earth's geochemistry. The mitochondrial electron transport chain has a patchwork of modules inherited from various pathways, reflecting Earth's redox environment over its history. The anoxic early Earth can be seen in Complex I's iron-sulfur cofactors, while the advent of oxygen as an electron acceptor led to the use of heme and copper cofactors. Supercomplexes formed for improved electron transfer efficiency in some organisms, and accessory subunits evolved for better assembly and stability. Environmental microbes with "fossil" proteins similar to ancestral forms of respiratory complexes could provide insights on aerobic respiration evolution.
Aerobic respiration evolved by bricolage, with modules cobbled together as mi-crobial 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. Environ-mental microbes with 'fossil' proteins that are similar to ancestral forms of the respi-ratory complexes deserve further scrutiny and may reveal new insights on the evolution of aerobic respiration.

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