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Fragmentation in mitochondrial genomes in relation to elevated sequence divergence and extreme rearrangements
Journal article   Open access   Peer reviewed

Fragmentation in mitochondrial genomes in relation to elevated sequence divergence and extreme rearrangements

Shiqian Feng, Andrea Pozzi, Vaclav Stejskal, George Opit, Qianqian Yang, Renfu Shao, Damian K Dowling and Zhihong Li
BMC Biology, Vol.20(1), pp.7-7
2022
DOI: https://doi.org/10.1186/s12915-021-01218-7
PMCID: PMC8742463
PMID: 34996453
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Fragmentation in mitochondrial genomes in relation to elevated sequence divergence and extreme rearrangements2.94 MBDownloadView
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https://doi.org/10.1186/s12915-021-01218-7View
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Abstract

Booklice Evolution Recombination Mitochondrial genome Fragmentation Rearrangement
A single circular mitochondrial (mt) genome is a common feature across most metazoans. The mt-genome includes protein-coding genes involved in oxidative phosphorylation, as well as RNAs necessary for translation of mt-RNAs, whose order and number are highly conserved across animal clades, with few known exceptions of alternative mt-gene order or mt-genome architectures. One such exception consists of the fragmented mitochondrial genome, a type of genome architecture where mt-genes are split across two or more mt-chromosomes. However, the origins of mt-genome fragmentation and its effects on mt-genome evolution are unknown. Here, we investigate these origin and potential mechanisms underlying mt-genome fragmentation, focusing on a genus of booklice, Liposcelis, which exhibits elevated sequence divergence, frequent rearrangement of mt-gene order, and fragmentation of the mt genome, and compare them to other Metazoan clades. We found this genus Liposcelis exhibits very low conservation of mt-gene order across species, relative to other metazoans. Levels of gene order rearrangement were, however, unrelated to whether or not mt-genomes were fragmented or intact, suggesting mitochondrial genome fragmentation is not affecting mt-gene order directly. We further investigated possible mechanisms underpinning these patterns and revealed very high conservation of non-coding sequences at the edges of multiple recombination regions across populations of one particular Liposcelis species, supportive of a hypothesis that mt-fragmentation arises from recombination errors between mt-genome copies. We propose these errors may arise as a consequence of a heightened mutation rate in clades exhibiting mt-fragmentation. Consistent with this, we observed a striking pattern across three Metazoan phyla (Arthropoda, Nematoda, Cnidaria) characterised by members exhibiting high levels of mt-gene order rearrangement and cases of mt-fragmentation, whereby the mt-genomes of species more closely related to species with fragmented mt-genomes diverge more rapidly despite experiencing strong purifying selection. We showed that contrary to expectations, mt-genome fragmentation is not correlated with the increase in mt-genome rearrangements. Furthermore, we present evidence that fragmentation of the mt-genome may be part of a general relaxation of a natural selection on the mt-genome, thus providing new insights into the origins of mt-genome fragmentation and evolution.

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