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Signals of positive selection in mitochondrial protein-coding genes of woolly mammoth: Adaptation to extreme environments?

ABSTRACT: The mammoths originated in warm and equatorial Africa and later colonized cold and high-latitude environments. Studies on nuclear genes suggest that woolly mammoth had evolved genetic variations involved in processes relevant to cold tolerance, including lipid metabolism and thermogenesis, and adaptation to extremely varied light and darkness cycles. The mitochondria is a major regulator of cellular energy metabolism, thus the mitogenome of mammoths may also exhibit adaptive evolution. However, little is yet known in this regard. In this study, we analyzed mitochondrial protein-coding genes (MPCGs) sequences of 75 broadly distributed woolly mammoths (Mammuthus primigenius) to test for signatures of positive selection. Results showed that a total of eleven amino acid sites in six genes, namely ND1, ND4, ND5, ND6, CYTB, and ATP6, displayed strong evidence of positive selection. Two sites were located in close proximity to proton-translocation channels in mitochondrial complex I. Biochemical and homology protein structure modeling analyses demonstrated that five amino acid substitutions in ND1, ND5, and ND6 might have influenced the performance of protein-protein interaction among subunits of complex I, and three substitutions in CYTB and ATP6 might have influenced the performance of metabolic regulatory chain. These findings suggest metabolic adaptations in the mitogenome of woolly mammoths in relation to extreme environments and provide a basis for further tests on the significance of the variations on other systems.

SUBMITTER: Ngatia JN

PROVIDER: S-EPMC6662336 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Signals of positive selection in mitochondrial protein-coding genes of woolly mammoth: Adaptation to extreme environments?

Ngatia Jacob Njaramba JN Lan Tian Ming TM Dinh Thi Dao TD Zhang Le L Ahmed Ahmed Khalid AK Xu Yan Chun YC

Ecology and evolution 20190509 12

The mammoths originated in warm and equatorial Africa and later colonized cold and high-latitude environments. Studies on nuclear genes suggest that woolly mammoth had evolved genetic variations involved in processes relevant to cold tolerance, including lipid metabolism and thermogenesis, and adaptation to extremely varied light and darkness cycles. The mitochondria is a major regulator of cellular energy metabolism, thus the mitogenome of mammoths may also exhibit adaptive evolution. However, ...[more]

PMID: 31380018

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Project description:BackgroundAnimal mitochondria play a central role in energy production in the cells through the oxidative phosphorylation (OXPHOS) pathway. Recent studies of selection on different mitochondrial OXPHOS genes have revealed the adaptive implications of amino acid changes in these subunits. In hares, climatic variation and/or introgression were suggested to be at the origin of such adaptation. Here we looked for evidence of positive selection in three mitochondrial OXPHOS genes, using tests of selection, protein structure modelling and effects of amino acid substitutions on the protein function and stability. We also used statistical models to test for climate and introgression effects on sites under positive selection.ResultsOur results revealed seven sites under positive selection in ND4 and three sites in Cytb. However, no sites under positive selection were observed in the COX1 gene. All three subunits presented a high number of codons under negative selection. Sites under positive selection were mapped on the tridimensional structure of the predicted models for the respective mitochondrial subunit. Of the ten amino acid replacements inferred to have evolved under positive selection for both subunits, six were located in the transmembrane domain. On the other hand, three codons were identified as sites lining proton translocation channels. Furthermore, four codons were identified as destabilizing with a significant variation of Δ vibrational entropy energy between wild and mutant type. Moreover, our PROVEAN analysis suggested that among all positively selected sites two fixed amino acid replacements altered the protein functioning. Our statistical models indicated significant effects of climate on the presence of ND4 and Cytb protein variants, but no effect by trans-specific mitochondrial DNA introgression, which is not uncommon in a number of hare species.ConclusionsPositive selection was observed in several codons in two OXPHOS genes. We found that substitutions in the positively selected codons have structural and functional impacts on the encoded proteins. Our results are concordantly suggesting that adaptations have strongly affected the evolution of mtDNA of hare species with potential effects on the protein function. Environmental/climatic changes appear to be a major trigger of this adaptation, whereas trans-specific introgressive hybridization seems to play no major role for the occurrence of protein variants.

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Signals of positive selection in mitochondrial protein-coding genes of woolly mammoth: Adaptation to extreme environments?

Publications

Signals of positive selection in mitochondrial protein-coding genes of woolly mammoth: Adaptation to extreme environments?

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