Recurrent erosion of COA1/MITRAC15 exemplifies conditional gene dispensability in oxidative phosphorylation

Sagar Sharad Shinde,Nagarjun Vijay,Ashutosh Sharma,Sandhya Sharma,Lokdeep Teekas

doi:10.1038/s41598-021-04077-y

Sagar Sharad Shinde, Nagarjun Vijay + Show 3 more

Open Access

https://doi.org/10.1038/s41598-021-04077-y

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Abstract

Skeletal muscle fibers rely upon either oxidative phosphorylation or the glycolytic pathway with much less reliance on oxidative phosphorylation to achieve muscular contractions that power mechanical movements. Species with energy-intensive adaptive traits that require sudden bursts of energy have a greater dependency on glycolytic fibers. Glycolytic fibers have decreased reliance on OXPHOS and lower mitochondrial content compared to oxidative fibers. Hence, we hypothesized that gene loss might have occurred within the OXPHOS pathway in lineages that largely depend on glycolytic fibers. The protein encoded by the COA1/MITRAC15 gene with conserved orthologs found in budding yeast to humans promotes mitochondrial translation. We show that gene disrupting mutations have accumulated within the COA1 gene in the cheetah, several species of galliform birds, and rodents. The genomic region containing COA1 is a well-established evolutionary breakpoint region in mammals. Careful inspection of genome assemblies of closely related species of rodents and marsupials suggests two independent COA1 gene loss events co-occurring with chromosomal rearrangements. Besides recurrent gene loss events, we document changes in COA1 exon structure in primates and felids. The detailed evolutionary history presented in this study reveals the intricate link between skeletal muscle fiber composition and the occasional dispensability of the chaperone-like role of the COA1 gene.

Highlights

Skeletal muscles control numerous locomotor functions in v ertebrates[1]
Our study evaluates whether the protein encoded by the COA1 gene, a mitochondrial complex I translation factor with a chaperone-like role, is dispensable when the oxidative phosphorylation (OXPHOS) pathway is under relaxed selective constraints
We hypothesized that the OXPHOS pathway might have experienced reduced purifying selection in felids, rodents, marsupials, and galliform birds based on an increased proportion of glycolytic fibers

Summary

Introduction

Skeletal muscles control numerous locomotor functions in v ertebrates[1]. The hundreds of different muscles in the body consist of highly organized heterogeneous bundles of fibers. The special locomotory needs of galliform birds, rodents, marsupials, and felids lead to a greater reliance on anaerobic fast fibers for sudden bursts of energy[11,12,13]. The OXPHOS pathway is under stronger selective constraint in non-galliform bird species than galliform birds due to the functional specialization of mitochondria to different muscle fibers[25]. The higher proportion of fast glycolytic fibers in felids, rodents, and marsupials results in relaxed selection on the OXPHOS pathway genes in these species. Our study evaluates whether the protein encoded by the COA1 gene, a mitochondrial complex I translation factor with a chaperone-like role, is dispensable when the OXPHOS pathway is under relaxed selective constraints. We hypothesized that the OXPHOS pathway might have experienced reduced purifying selection in felids, rodents, marsupials, and galliform birds based on an increased proportion of glycolytic fibers. We extensively screened publicly available genomes and transcriptomes of more than 365 vertebrate species to establish recurrent loss of the widely conserved COA1 gene

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