45
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: not found

      Adaptive Evolution and Functional Redesign of Core Metabolic Proteins in Snakes

      research-article

      Read this article at

      ScienceOpenPublisherPMC
      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          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.

          Related collections

          Most cited references38

          • Record: found
          • Abstract: found
          • Article: not found

          Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.

          Q. Z. Yang (2000)
          Approximate methods for estimating the numbers of synonymous and nonsynonymous substitutions between two DNA sequences involve three steps: counting of synonymous and nonsynonymous sites in the two sequences, counting of synonymous and nonsynonymous differences between the two sequences, and correcting for multiple substitutions at the same site. We examine complexities involved in those steps and propose a new approximate method that takes into account two major features of DNA sequence evolution: transition/transversion rate bias and base/codon frequency bias. We compare the new method with maximum likelihood, as well as several other approximate methods, by examining infinitely long sequences, performing computer simulations, and analyzing a real data set. The results suggest that when there are transition/transversion rate biases and base/codon frequency biases, previously described approximate methods for estimating the nonsynonymous/synonymous rate ratio may involve serious biases, and the bias can be both positive and negative. The new method is, in general, superior to earlier approximate methods and may be useful for analyzing large data sets, although maximum likelihood appears to always be the method of choice.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome.

            A model of DNA sequence evolution applicable to coding regions is presented. This represents the first evolutionary model that accounts for dependencies among nucleotides within a codon. The model uses the codon, as opposed to the nucleotide, as the unit of evolution, and is parameterized in terms of synonymous and nonsynonymous nucleotide substitution rates. One of the model's advantages over those used in methods for estimating synonymous and nonsynonymous substitution rates is that it completely corrects for multiple hits at a codon, rather than taking a parsimony approach and considering only pathways of minimum change between homologous codons. Likelihood-ratio versions of the relative-rate test are constructed and applied to data from the complete chloroplast DNA sequences of Oryza sativa, Nicotiana tabacum, and Marchantia polymorpha. Results of these tests confirm previous findings that substitution rates in the chloroplast genome are subject to both lineage-specific and locus-specific effects. Additionally, the new tests suggest tha the rate heterogeneity is due primarily to differences in nonsynonymous substitution rates. Simulations help confirm previous suggestions that silent sites are saturated, leaving no evidence of heterogeneity in synonymous substitution rates.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A.

              The crystal structure of bovine heart cytochrome c oxidase at 2.8 A resolution with an R value of 19.9 percent reveals 13 subunits, each different from the other, five phosphatidyl ethanolamines, three phosphatidyl glycerols and two cholates, two hemes A, and three copper, one magnesium, and one zinc. Of 3606 amino acid residues in the dimer, 3560 have been converged to a reasonable structure by refinement. A hydrogen-bonded system, including a propionate of a heme A (heme a), part of peptide backbone, and an imidazole ligand of CuA, could provide an electron transfer pathway between CuA and heme a. Two possible proton pathways for pumping, each spanning from the matrix to the cytosolic surfaces, were identified, including hydrogen bonds, internal cavities likely to contain water molecules, and structures that could form hydrogen bonds with small possible conformational change of amino acid side chains. Possible channels for chemical protons to produce H2O, for removing the produced water, and for O2, respectively, were identified.
                Bookmark

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                21 May 2008
                : 3
                : 5
                : e2201
                Affiliations
                [1 ]Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America
                [2 ]Department of Biological Sciences, Biological Computation and Visualization Center, Louisiana State University, Baton Rouge, Louisiana, United States of America
                University of California, Berkeley, United States of America
                Author notes

                Conceived and designed the experiments: DP. Performed the experiments: TC ZJ. Analyzed the data: DP TC ZJ WG ZW. Contributed reagents/materials/analysis tools: DP WG. Wrote the paper: DP TC ZJ.

                [¤a]

                Current address: Computational Biology, Scripps Florida, Jupiter, Florida, United States of America

                [¤b]

                Current address: Genome Sequencing Center, Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, United States of America

                Article
                07-PONE-RA-03016R1
                10.1371/journal.pone.0002201
                2376058
                18493604
                9c49c6c1-370c-483d-9f9b-9293dfe6712b
                Castoe et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 12 December 2007
                : 1 April 2008
                Page count
                Pages: 14
                Categories
                Research Article
                Biochemistry/Bioinformatics
                Biochemistry/Molecular Evolution
                Computational Biology/Evolutionary Modeling
                Computational Biology/Molecular Genetics
                Evolutionary Biology/Animal Genetics
                Evolutionary Biology/Bioinformatics
                Evolutionary Biology/Evolutionary and Comparative Genetics
                Evolutionary Biology/Genomics
                Genetics and Genomics/Comparative Genomics
                Genetics and Genomics/Comparative Genomics
                Molecular Biology/Molecular Evolution
                Physiology/Genomics
                Physiology/Respiratory Physiology

                Uncategorized
                Uncategorized

                Comments

                Comment on this article