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Adaptive evolution and functional redesign of core metabolic proteins in snakes.

Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD - PLoS ONE (2008)

Bottom Line: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure.It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution.The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America.

ABSTRACT

Background: Adaptive evolutionary episodes in core metabolic proteins are uncommon, and are even more rarely linked to major macroevolutionary shifts.

Methodology/principal findings: We conducted extensive molecular evolutionary analyses on snake mitochondrial proteins and discovered multiple lines of evidence suggesting that the proteins at the core of aerobic metabolism in snakes have undergone remarkably large episodic bursts of adaptive change. We show that snake mitochondrial proteins experienced unprecedented levels of positive selection, coevolution, convergence, and reversion at functionally critical residues. We examined Cytochrome C oxidase subunit I (COI) in detail, and show that it experienced extensive modification of normally conserved residues involved in proton transport and delivery of electrons and oxygen. Thus, adaptive changes likely altered the flow of protons and other aspects of function in CO, thereby influencing fundamental characteristics of aerobic metabolism. We refer to these processes as "evolutionary redesign" because of the magnitude of the episodic bursts and the degree to which they affected core functional residues.

Conclusions/significance: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure. It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution. The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

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Amino acid replacements at residues within and directly adjacent to the three proton transport channels (D, H, and K) within cytochrome C oxidase subunit 1 (COI) have substantially altered COI structure and presumably function in snakes.On the small snake phylogenetic trees shown, amino acid replacements that occur in snakes at sites comprising the channel are indicated with ovals, and changes at sites adjacent to each channel are indicated with rectangles. Deep colors (dark red and dark blue) indicate replacements at unique sites (see text) whereas lighter colors (light red and light blue) are not unique sites. Sites that were inferred to be under significant positive selection along the Alethinophidian snake branch (by PAML branch-site analyses) are indicated with a plus sign. The relative order of replacements along each single branch has no meaning. These same sites are shown as spacefill representations in the structure, and are labeled and shaded with the same color code as the mark on the tree. One channel is shown per subfigure (A = channel D, B = channel H, and C = channel K). The three proton channels D, H, and K are shown in transparent purple, green, or magenta volumetric representation, respectively. The entire CO1 structure is shown as a transparent grey ribbon structure, heme groups are shown as spacefill representations colored by element, and the magnesium and copper atoms are colored magenta and green, respectively.
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pone-0002201-g003: Amino acid replacements at residues within and directly adjacent to the three proton transport channels (D, H, and K) within cytochrome C oxidase subunit 1 (COI) have substantially altered COI structure and presumably function in snakes.On the small snake phylogenetic trees shown, amino acid replacements that occur in snakes at sites comprising the channel are indicated with ovals, and changes at sites adjacent to each channel are indicated with rectangles. Deep colors (dark red and dark blue) indicate replacements at unique sites (see text) whereas lighter colors (light red and light blue) are not unique sites. Sites that were inferred to be under significant positive selection along the Alethinophidian snake branch (by PAML branch-site analyses) are indicated with a plus sign. The relative order of replacements along each single branch has no meaning. These same sites are shown as spacefill representations in the structure, and are labeled and shaded with the same color code as the mark on the tree. One channel is shown per subfigure (A = channel D, B = channel H, and C = channel K). The three proton channels D, H, and K are shown in transparent purple, green, or magenta volumetric representation, respectively. The entire CO1 structure is shown as a transparent grey ribbon structure, heme groups are shown as spacefill representations colored by element, and the magnesium and copper atoms are colored magenta and green, respectively.

Mentions: To further investigate the functional ramifications of evolutionary change in snake COI, we dissected the details of evolutionary modifications in each channel individually (Figure 3) and inferred the impact of replacements based on existing hypotheses concerning CO function. Proton channel D is thought to be the only channel that is capable of both delivering protons to the reaction center for the reduction of oxygen and pumping protons across the membrane to drive ATP synthesis [18], [22], [23]. Of the 14 residues that comprise the D channel, all but one are completely conserved outside of squamate reptiles (Table S5). Nevertheless, replacements in channel D at the base of snake evolution seem likely to have reduced (or eliminated) its proton transport capacity, based on the functional models of the bovine CO [18], [22], [23]. Replacements S108A and T146A exchanged conserved polar residues with alanine, interrupting an integrated chain of hydrogen bonds critical to proton transfer (Figure 3A; Tables S5–S6). Tsukihara et al. [18] suggested that individual substitutions in the proton channels might be tolerated due to contributions from water molecules, but the combined effect of these two replacements alone would be substantial, creating a large polarity gap in the network around intervening residue S149.


Adaptive evolution and functional redesign of core metabolic proteins in snakes.

Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD - PLoS ONE (2008)

Amino acid replacements at residues within and directly adjacent to the three proton transport channels (D, H, and K) within cytochrome C oxidase subunit 1 (COI) have substantially altered COI structure and presumably function in snakes.On the small snake phylogenetic trees shown, amino acid replacements that occur in snakes at sites comprising the channel are indicated with ovals, and changes at sites adjacent to each channel are indicated with rectangles. Deep colors (dark red and dark blue) indicate replacements at unique sites (see text) whereas lighter colors (light red and light blue) are not unique sites. Sites that were inferred to be under significant positive selection along the Alethinophidian snake branch (by PAML branch-site analyses) are indicated with a plus sign. The relative order of replacements along each single branch has no meaning. These same sites are shown as spacefill representations in the structure, and are labeled and shaded with the same color code as the mark on the tree. One channel is shown per subfigure (A = channel D, B = channel H, and C = channel K). The three proton channels D, H, and K are shown in transparent purple, green, or magenta volumetric representation, respectively. The entire CO1 structure is shown as a transparent grey ribbon structure, heme groups are shown as spacefill representations colored by element, and the magnesium and copper atoms are colored magenta and green, respectively.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2376058&req=5

pone-0002201-g003: Amino acid replacements at residues within and directly adjacent to the three proton transport channels (D, H, and K) within cytochrome C oxidase subunit 1 (COI) have substantially altered COI structure and presumably function in snakes.On the small snake phylogenetic trees shown, amino acid replacements that occur in snakes at sites comprising the channel are indicated with ovals, and changes at sites adjacent to each channel are indicated with rectangles. Deep colors (dark red and dark blue) indicate replacements at unique sites (see text) whereas lighter colors (light red and light blue) are not unique sites. Sites that were inferred to be under significant positive selection along the Alethinophidian snake branch (by PAML branch-site analyses) are indicated with a plus sign. The relative order of replacements along each single branch has no meaning. These same sites are shown as spacefill representations in the structure, and are labeled and shaded with the same color code as the mark on the tree. One channel is shown per subfigure (A = channel D, B = channel H, and C = channel K). The three proton channels D, H, and K are shown in transparent purple, green, or magenta volumetric representation, respectively. The entire CO1 structure is shown as a transparent grey ribbon structure, heme groups are shown as spacefill representations colored by element, and the magnesium and copper atoms are colored magenta and green, respectively.
Mentions: To further investigate the functional ramifications of evolutionary change in snake COI, we dissected the details of evolutionary modifications in each channel individually (Figure 3) and inferred the impact of replacements based on existing hypotheses concerning CO function. Proton channel D is thought to be the only channel that is capable of both delivering protons to the reaction center for the reduction of oxygen and pumping protons across the membrane to drive ATP synthesis [18], [22], [23]. Of the 14 residues that comprise the D channel, all but one are completely conserved outside of squamate reptiles (Table S5). Nevertheless, replacements in channel D at the base of snake evolution seem likely to have reduced (or eliminated) its proton transport capacity, based on the functional models of the bovine CO [18], [22], [23]. Replacements S108A and T146A exchanged conserved polar residues with alanine, interrupting an integrated chain of hydrogen bonds critical to proton transfer (Figure 3A; Tables S5–S6). Tsukihara et al. [18] suggested that individual substitutions in the proton channels might be tolerated due to contributions from water molecules, but the combined effect of these two replacements alone would be substantial, creating a large polarity gap in the network around intervening residue S149.

Bottom Line: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure.It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution.The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America.

ABSTRACT

Background: Adaptive evolutionary episodes in core metabolic proteins are uncommon, and are even more rarely linked to major macroevolutionary shifts.

Methodology/principal findings: We conducted extensive molecular evolutionary analyses on snake mitochondrial proteins and discovered multiple lines of evidence suggesting that the proteins at the core of aerobic metabolism in snakes have undergone remarkably large episodic bursts of adaptive change. We show that snake mitochondrial proteins experienced unprecedented levels of positive selection, coevolution, convergence, and reversion at functionally critical residues. We examined Cytochrome C oxidase subunit I (COI) in detail, and show that it experienced extensive modification of normally conserved residues involved in proton transport and delivery of electrons and oxygen. Thus, adaptive changes likely altered the flow of protons and other aspects of function in CO, thereby influencing fundamental characteristics of aerobic metabolism. We refer to these processes as "evolutionary redesign" because of the magnitude of the episodic bursts and the degree to which they affected core functional residues.

Conclusions/significance: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure. It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution. The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

Show MeSH