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The adaptive evolution of the mammalian mitochondrial genome.

da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A - BMC Genomics (2008)

Bottom Line: ATP6, which has an essential role in rotor performance, showed a high adaptive variation in predicted loop areas.Our study provides insight into the adaptive evolution of the mtDNA genome in mammals and its implications for the molecular mechanism of oxidative phosphorylation.We present a framework for future experimental characterization of the impact of specific mutations in the function, physiology, and interactions of the mtDNA encoded proteins involved in oxidative phosphorylation.

View Article: PubMed Central - HTML - PubMed

Affiliation: REQUIMTE, Departamento de Química, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 687, 4169-007 Porto, Portugal. rute.r.da.fonseca@gmail.com

ABSTRACT

Background: The mitochondria produce up to 95% of a eukaryotic cell's energy through oxidative phosphorylation. The proteins involved in this vital process are under high functional constraints. However, metabolic requirements vary across species, potentially modifying selective pressures. We evaluate the adaptive evolution of 12 protein-coding mitochondrial genes in 41 placental mammalian species by assessing amino acid sequence variation and exploring the functional implications of observed variation in secondary and tertiary protein structures.

Results: Wide variation in the properties of amino acids were observed at functionally important regions of cytochrome b in species with more-specialized metabolic requirements (such as adaptation to low energy diet or large body size, such as in elephant, dugong, sloth, and pangolin, and adaptation to unusual oxygen requirements, for example diving in cetaceans, flying in bats, and living at high altitudes in alpacas). Signatures of adaptive variation in the NADH dehydrogenase complex were restricted to the loop regions of the transmembrane units which likely function as protons pumps. Evidence of adaptive variation in the cytochrome c oxidase complex was observed mostly at the interface between the mitochondrial and nuclear-encoded subunits, perhaps evidence of co-evolution. The ATP8 subunit, which has an important role in the assembly of F0, exhibited the highest signal of adaptive variation. ATP6, which has an essential role in rotor performance, showed a high adaptive variation in predicted loop areas.

Conclusion: Our study provides insight into the adaptive evolution of the mtDNA genome in mammals and its implications for the molecular mechanism of oxidative phosphorylation. We present a framework for future experimental characterization of the impact of specific mutations in the function, physiology, and interactions of the mtDNA encoded proteins involved in oxidative phosphorylation.

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Mammalian mitogenomic phylogenetic tree. Consensus phylogenetic tree (50 percent majority rule) constructed from the combined set of MCMC runs resulting topologies in MrBayes. Numbers give the percentage of posterior probability support for each clade averaged over the runs.
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Figure 2: Mammalian mitogenomic phylogenetic tree. Consensus phylogenetic tree (50 percent majority rule) constructed from the combined set of MCMC runs resulting topologies in MrBayes. Numbers give the percentage of posterior probability support for each clade averaged over the runs.

Mentions: The mitogenomic phylogenetic reconstruction (Figure 2) obtained with Bayesian inference methods [25,26] is mostly congruent with previous comprehensive analyses from nuclear and mtDNA genes [27] where mammalian species form four major groups: Laurasiatheria, Euarchontoglires, Xenarthra, and Afrotheria. The superordinal tree is resolved with posterior probabilities greater than 0.99. The relative positioning of the orders is in agreement with that obtained using Maximum Likelihood [see Additional file 1, Fig. S2], supporting the previous topology.


The adaptive evolution of the mammalian mitochondrial genome.

da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A - BMC Genomics (2008)

Mammalian mitogenomic phylogenetic tree. Consensus phylogenetic tree (50 percent majority rule) constructed from the combined set of MCMC runs resulting topologies in MrBayes. Numbers give the percentage of posterior probability support for each clade averaged over the runs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2375446&req=5

Figure 2: Mammalian mitogenomic phylogenetic tree. Consensus phylogenetic tree (50 percent majority rule) constructed from the combined set of MCMC runs resulting topologies in MrBayes. Numbers give the percentage of posterior probability support for each clade averaged over the runs.
Mentions: The mitogenomic phylogenetic reconstruction (Figure 2) obtained with Bayesian inference methods [25,26] is mostly congruent with previous comprehensive analyses from nuclear and mtDNA genes [27] where mammalian species form four major groups: Laurasiatheria, Euarchontoglires, Xenarthra, and Afrotheria. The superordinal tree is resolved with posterior probabilities greater than 0.99. The relative positioning of the orders is in agreement with that obtained using Maximum Likelihood [see Additional file 1, Fig. S2], supporting the previous topology.

Bottom Line: ATP6, which has an essential role in rotor performance, showed a high adaptive variation in predicted loop areas.Our study provides insight into the adaptive evolution of the mtDNA genome in mammals and its implications for the molecular mechanism of oxidative phosphorylation.We present a framework for future experimental characterization of the impact of specific mutations in the function, physiology, and interactions of the mtDNA encoded proteins involved in oxidative phosphorylation.

View Article: PubMed Central - HTML - PubMed

Affiliation: REQUIMTE, Departamento de Química, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 687, 4169-007 Porto, Portugal. rute.r.da.fonseca@gmail.com

ABSTRACT

Background: The mitochondria produce up to 95% of a eukaryotic cell's energy through oxidative phosphorylation. The proteins involved in this vital process are under high functional constraints. However, metabolic requirements vary across species, potentially modifying selective pressures. We evaluate the adaptive evolution of 12 protein-coding mitochondrial genes in 41 placental mammalian species by assessing amino acid sequence variation and exploring the functional implications of observed variation in secondary and tertiary protein structures.

Results: Wide variation in the properties of amino acids were observed at functionally important regions of cytochrome b in species with more-specialized metabolic requirements (such as adaptation to low energy diet or large body size, such as in elephant, dugong, sloth, and pangolin, and adaptation to unusual oxygen requirements, for example diving in cetaceans, flying in bats, and living at high altitudes in alpacas). Signatures of adaptive variation in the NADH dehydrogenase complex were restricted to the loop regions of the transmembrane units which likely function as protons pumps. Evidence of adaptive variation in the cytochrome c oxidase complex was observed mostly at the interface between the mitochondrial and nuclear-encoded subunits, perhaps evidence of co-evolution. The ATP8 subunit, which has an important role in the assembly of F0, exhibited the highest signal of adaptive variation. ATP6, which has an essential role in rotor performance, showed a high adaptive variation in predicted loop areas.

Conclusion: Our study provides insight into the adaptive evolution of the mtDNA genome in mammals and its implications for the molecular mechanism of oxidative phosphorylation. We present a framework for future experimental characterization of the impact of specific mutations in the function, physiology, and interactions of the mtDNA encoded proteins involved in oxidative phosphorylation.

Show MeSH
Related in: MedlinePlus