Journal of Molecular Evolution

, Volume 62, Issue 3, pp 319–331

Molecular Evolution of Cytochrome c Oxidase in High-Performance Fish (Teleostei: Scombroidei)

  • Anne C. Dalziel
  • Christopher D. Moyes
  • Emma Fredriksson
  • Stephen C. Lougheed
Article

Abstract

The 13 peptides encoded by vertebrate mitochondrial DNA (mtDNA) are essential subunits of oxidative phosphorylation (OXPHOS) enzymes. These genes normally experience purifying selection and also coevolve with nuclear-encoded subunits of OXPHOS complexes. However, the role of positive selection on mtDNA evolution is still unclear, as most examples of intergenomic coevolution appear to be the result of compensation by nuclear-encoded genes for mildly deleterious mtDNA mutations, and not simultaneous positive selection in both genomes. Organisms that have experienced strong selective pressures to increase aerobic capacity or adapt to changes in thermal environment may be better candidates in which to examine the impact of positively selected changes on mtDNA evolution. The tuna (suborder Scombroidei, family Scombridae) and billfish (suborder Scombroidei, families Xiphiidae and Istiophoridae) are highly aerobic fish with multiple specializations in muscle energetics, including a high mitochondrial content and regional endothermy. We examined the role of positively selected mtDNA substitutions in the production of these unique phenotypes. Focusing on a catalytic subunit of cytochrome c oxidase (COX II), we found that the rate ratio of nonsynonymous (dN; amino acid changing)-to-synonymous (dS; silent) substitutions was not increased in lineages leading to the tuna but was significantly increased in the lineage preceding the billfish. Furthermore, there are a number of individual positively selected sites that, when mapped onto the COX crystal structure, appear to interact with other COX subunits and may affect OXPHOS function and regulation in billfish.

Keywords

Mitochondrial DNA evolution Positive selection Cytochrome c oxidase Aerobic energy metabolism Endothermy Tuna Billfish 

References

  1. Adkins RM, Honeycutt RL (1994) Evolution of the primate cytochrome-c-oxidase subunit-II gene. J Mol Evol 38:215–231CrossRefPubMedGoogle Scholar
  2. Adkins RM, Honeycutt RL, Disotell TR (1996) Evolution of eutherian cytochrome c oxidase subunit II: Heterogeneous rates of protein evolution and altered interaction with cytochrome c. Mol Biol Evol 13:1393–1404PubMedGoogle Scholar
  3. Arnold S, Goglia F, Kadenbach B (1998) 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur J Biochem 252:325–330CrossRefPubMedGoogle Scholar
  4. Arnold S, Lee I, Kim M, Song E, Linder D, Lottspeich F, Kadenbach B (1997) The subunit structure of cytochrome-c oxidase from tuna heart and liver. Eur J Biochem 248:99–103CrossRefPubMedGoogle Scholar
  5. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman (1997) Short protocols in molecular biology, 3rd ed. John Wiley & Sons, New YorkGoogle Scholar
  6. Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744CrossRefPubMedGoogle Scholar
  7. Blier PU, Dufresne F, Burton RS (2001) Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet 17:400–406CrossRefPubMedGoogle Scholar
  8. Block BA (1986) Structure of the brain and eye heater tissue in marlins, sailfish, and spearfish. J Morphol 190:169–189CrossRefPubMedGoogle Scholar
  9. Block BA (1987) Billfish brain and eye heater: A new look at nonshivering heat production. News Physiol Sci 2:208–213Google Scholar
  10. Block BA (1994) Thermogenesis in muscle. Annu Rev Physiol 56:535–577CrossRefPubMedGoogle Scholar
  11. Block BA, Finnerty JR (1994) Endothermy in fish: A phylogenetic analysis of constraints, predispositions, and selection pressures. Environ Biol Fish 40:283–302CrossRefGoogle Scholar
  12. Block BA, Finnerty JR, Stewart AF, Kidd J (1993) Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260:210–214PubMedGoogle Scholar
  13. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275:81–86PubMedGoogle Scholar
  14. Brill RW (1996) Selective advantages conferred by the high performance physiology of tuna, billfish, and dolphin fish. Comp Biochem Physiol A Physiol 113:3–15Google Scholar
  15. Carey FG (1982) A brain heater in the swordfish. Science 216:1327–1329PubMedGoogle Scholar
  16. Chen WJ, Bonillo C, Lecointre G (2003) Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol Phylogenet Evol 26:262–288PubMedGoogle Scholar
  17. Collette BB, Reeb C, Block BA (2001) Systematics of the tuna and mackerels (scombridae). In: Block BA, Stevens ED (eds) Tuna: Physiology, ecology, and evolution. Academic Press, San Diego, CA, pp 1–30Google Scholar
  18. Dalziel AC, Moore SE, Moyes CD (2005) Mitochondrial enzyme content in the muscles of high-performance fish: evolution and variation among fiber types. Am J Physiol Regul Integr Comp Physiol 288:R163–R172PubMedGoogle Scholar
  19. Das J, Miller ST, Stern DL (2004) Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome C oxidase suggests conservation of structure underlies evolving functional sites. Mol Biol Evol 21:1572–1582PubMedGoogle Scholar
  20. Dickson KA (1996) Locomotor muscle of high-performance fish: What do comparisons of tuna with ectothermic sister taxa reveal? Comp Biochem Physiol 113:39–49CrossRefGoogle Scholar
  21. Dickson KA, Graham JB (2004) Evolution and consequences of endothermy in fish. Physiol Biochem Zool 77:998–1018CrossRefPubMedGoogle Scholar
  22. Finnerty JR, Block BA (1995) Evolution of cytochrome-b in the scombroidei (Teleostei)— Molecular insights into billfish (Istiophoridae and Xiphiidae) relationships. Fish Bull 93:78–96Google Scholar
  23. Goglia F, Moreno M, Lanni A (1999) Action of thyroid hormones at the cellular level: the mitochondrial target. FEBS Lett 452:115–120CrossRefPubMedGoogle Scholar
  24. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–36PubMedGoogle Scholar
  25. Graham JB, Dickson KA (2001) Anatomical and physiological specializations for endothermy. In: Block BA, Stevens ED (eds) Tuna: Physiology, ecology, and evolution. Academic Press, San Diego, CAGoogle Scholar
  26. Grossman LI, Wildman DE, Schmidt TR, Goodman M (2004) Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet 20:578–585CrossRefPubMedGoogle Scholar
  27. Hofacker I, Schulten K (1998) Oxygen and proton pathways in cytochrome c oxidase. Proteins 30:100–107CrossRefPubMedGoogle Scholar
  28. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  29. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688PubMedGoogle Scholar
  30. Huttemann M, Frank V, Kadenbach B (1999) The possible role of isoforms of cytochrome c oxidase subunit VIa in mammalian thermogenesis. Cell Mol Life Sci 55:1482–1490PubMedGoogle Scholar
  31. Inoue JG, Miya M, Tsukamoto K, Nishida M (2001) A mitogenomic perspective on the basal teleostean phylogeny: resolving higher-level relationships with longer DNA sequences. Mol Phylogenet Evol 20:275–285PubMedGoogle Scholar
  32. Jobson RW, Nielsen R, Laakkonen L, Wikstrom M, Albert VA (2004) Adaptive evolution of cytochrome c oxidase: Infrastructure for a carnivorous plant radiation. Proc Natl Acad Sci USA 101:18064–18068CrossRefPubMedGoogle Scholar
  33. Kadenbach B (2003) Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta 1604:77–94PubMedGoogle Scholar
  34. Korsmeyer KE, Dewar H (2001) Tuna metabolism and energetics. In: Block BA, Stevens ED (eds) Tuna: Physiology, ecology, and evolution. Academic Press, San Diego, CA, pp 36–78Google Scholar
  35. Lanni A, Moreno M, Lombardi A, Goglia F (1998) 3,5-Diiodo-L-thyronine and 3,5,3′-triiodo-L-thyronine both improve the cold tolerance of hypothyroid rats, but possibly via different mechanisms. Pflugers Arch 436:407–14CrossRefPubMedGoogle Scholar
  36. Marcinek DJ, Bonaventura J, Wittenberg JB, Block BA (2001) Oxygen affinity and amino acid sequence of myoglobins from endothermic and ectothermic fish. Am J Physiol Regul Integr Comp Physiol 280:R1123–R1133PubMedGoogle Scholar
  37. Meunier B, Rich PR (1998) Second-site reversion analysis is not a reliable method to determine distances in membrane proteins: an assessment using mutations in yeast cytochrome c oxidase subunits I and II. J Mol Biol 283:727–730CrossRefPubMedGoogle Scholar
  38. Mishmar D, Ruiz-Pesini E, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, Easley K, Chen E, Brown MD, Sukernik RI, Olckers A, Wallace DC (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci USA 100:171–176CrossRefPubMedGoogle Scholar
  39. Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138PubMedGoogle Scholar
  40. Morrissette JM, Franck JP, Block BA (2003) Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans). J Exp Biol 206:805–812CrossRefPubMedGoogle Scholar
  41. Moyes CD, Mathieu-Costello OA, Brill RW, Hochachka PW (1992) Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish. Can J Zool 70:1246–1253Google Scholar
  42. Nakamura I (1983) Systematics of the billfish (Xiphiidae and Istiophoridae). Publ Set Mar Biol Lab 28:255–396Google Scholar
  43. Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936PubMedGoogle Scholar
  44. Overholtzer MH, Yakowec PS, Cameron V (1996) The effect of amino acid substitutions in the conserved aromatic region of subunit II of cytochrome c oxidase in Saccharomyces cerevisiae. J Biol Chem 271:7719–7724PubMedGoogle Scholar
  45. Posada D, Crandall KA (1998) MODELTEST: Testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  46. Potthoff T, Kelley S, Javech JC (1986) Cartilage and bone development in scombroid fish. Fish Bull 84:647–678Google Scholar
  47. Rahman S, Taanman JW, Cooper JM, Nelson I, Hargreaves I, Meunier B, Hanna MG, Garcia JJ, Capaldi RA, Lake BD, Leonard JV, Schapira AH (1999) A missense mutation of cytochrome oxidase subunit II causes defective assembly and myopathy. Am J Hum Genet 65:1030–1039CrossRefPubMedGoogle Scholar
  48. Rambaut A, Drummond AJ (2004) Tracer. Version 1.2.1. University of Oxford, OxfordGoogle Scholar
  49. Rand DM (2001) The units of selection on mitochondrial DNA. Annu Rev Ecol Syst 32:415–448CrossRefGoogle Scholar
  50. Rand DM, Haney RA, Fry AJ (2004) Cytonuclear coevolution: The genomics of cooperation. Trends Ecol Evol 19:645–653CrossRefGoogle Scholar
  51. Rawson PD, Burton RS (2002) Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc Natl Acad Sci USA 99:12955–12958CrossRefPubMedGoogle Scholar
  52. Richter OM, Ludwig B (2003) Cytochrome c oxidase––structure, function, and physiology of a redox-driven molecular machine. Rev Physiol Biochem Pharmacol 147:47–74PubMedGoogle Scholar
  53. Roberts VA, Pique ME (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete, systematic search. J Biol Chem 274:38051–38060PubMedGoogle Scholar
  54. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223–226CrossRefPubMedGoogle Scholar
  55. Schmidt B, McCracken J, Ferguson-Miller S (2003) A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc Natl Acad Sci USA 100:15539–15542PubMedGoogle Scholar
  56. Schmidt TR, Wu W, Goodman M, Grossman LI (2001) Evolution of nuclear- and mitochondrial-encoded subunit interaction in cytochrome c oxidase. Mol Biol Evol 18:563–569PubMedGoogle Scholar
  57. Simmons MP, Miya M (2004) Efficiently resolving the basal clades of a phylogenetic tree using Bayesian and parsimony approaches: a case study using mitogenomic data from 100 higher teleost fish. Mol Phylogenet Evol 31:351–362PubMedGoogle Scholar
  58. Smeitink J, van den Heuvel L, DiMauro S (2001) The genetics and pathology of oxidative phosphorylation. Nat Rev Genet 2:342–352CrossRefPubMedGoogle Scholar
  59. Srere PA (1985) Organization of proteins within the mitochondrion. In: Welch GR (ed) Organized multienzyme systems. Catalytic properties. Academic Press, New York, London, pp 1–61Google Scholar
  60. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland, MAGoogle Scholar
  61. Szuplewski S, Terracol R (2001) The cyclope gene of Drosophila encodes a cytochrome c oxidase subunit VIc homolog. Genetics 158:1629–1643PubMedGoogle Scholar
  62. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedGoogle Scholar
  63. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272:1136–1144PubMedGoogle Scholar
  64. Tullis A, Block BA, Sidell BD (1991) Activities of key metabolic enzymes in the heater organs of scombroid fish. J Exp Biol 161:383–403PubMedGoogle Scholar
  65. White FC, Kelly R, Kemper S, Schumacker PT, Gallagher KR, Laurs RM (1988) Organ blood flow haemodynamics and metabolism of the albacore tuna Thunnus alalunga (Bonnaterre). Exp Biol 47:161–9PubMedGoogle Scholar
  66. Willett CS, Burton RS (2003) Environmental influences on epistatic interactions: Viabilities of cytochrome c genotypes in interpopulation crosses. Evolution 57:2286–2292PubMedGoogle Scholar
  67. Willett CS, Burton RS (2004) Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol Biol Evol 21:443–453PubMedGoogle Scholar
  68. Yang Z (1993) Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol Biol Evol 10:1396–1401PubMedGoogle Scholar
  69. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556PubMedGoogle Scholar
  70. Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15:568–573PubMedGoogle Scholar
  71. Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917PubMedGoogle Scholar
  72. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedGoogle Scholar
  73. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723–1729CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Anne C. Dalziel
    • 1
    • 2
  • Christopher D. Moyes
    • 1
  • Emma Fredriksson
    • 1
  • Stephen C. Lougheed
    • 1
  1. 1.Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Department of Zoology6270 University Boulevard, University of British ColumbiaVancouverCanada

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