Mosaic nature of the mitochondrial proteome: Implications for the origin and evolution of mitochondria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10133-10138

  Gray, Michael W ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Endosymbiont; Mitochondria; Phagotrophy; Proteome; Syntrophy

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PROTEOME;

ARTICLE; ELECTRON TRANSPORT; ENDOSYMBIONT; MITOCHONDRIAL GENOME; MITOCHONDRION; MOSAICISM; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHAGOTROPH; PRIORITY JOURNAL; PROTEOBACTERIA; RECLINOMONAS AMERICANA; ALPHAPROTEOBACTERIA; ANIMAL; EVOLUTION; GENE TRANSFER; HUMAN; MOLECULAR EVOLUTION; MOUSE; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS; YEAST;

EUKARYOTA; PROKARYOTA; PROTEOBACTERIA;

ALPHAPROTEOBACTERIA; ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENE TRANSFER TECHNIQUES; GENOME, MITOCHONDRIAL; HUMANS; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PHYLOGENY; PROTEOME; SYMBIOSIS; YEASTS;

EID: 84939863150     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421379112     Document Type: Article

References (75)

1. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14(3):255-274.
2. Margulis L (1970) Origin of Eukaryotic Cells (Yale Univ Press, New Haven, CT).
3. O'Malley MA (2010) The first eukaryote cell: An unfinished history of contestation. Stud Hist Philos Biol Biomed Sci 41(3):212-224.
4. Poole AM, Gribaldo S (2014) Eukaryotic origins: How and when was the mitochondrion acquired? Cold Spring Harb Perspect Biol 6(12):a015990.
5. Gray MW (2014) The pre-endosymbiont hypothesis: A new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6(3):a016097.
6. Kannan S, Rogozin IB, Koonin EV (2014) MitoCOGs: Clusters of orthologous genes from mitochondria and implications for the evolution of eukaryotes. BMC Evol Biol 14(1):237.
7. Degli Esposti M, et al. (2014) Evolution of mitochondria reconstructed from the energy metabolism of living bacteria. PLoS ONE 9(5):e96566.
8. Wang Z, Wu M (2014) Phylogenomic reconstruction indicates mitochondrial ancestor was an energy parasite. PLoS ONE 9(10):e110685.
9. Lane N (2014) Bioenergetic constraints on the evolution of complex life. Cold Spring Harb Perspect Biol 6(5):a015982.
10. Wang Z, Wu M (2015) An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Sci Rep 5:7949.
11. Cavalier-Smith T (2014) The neomuran revolution and phagotrophic origin of eukaryotes and cilia in the light of intracellular coevolution and a revised tree of life. Cold Spring Harb Perspect Biol 6(9):a016006.
12. McInerney JO, O'Connell MJ, Pisani D (2014) The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat Rev Microbiol 12(6):449-455.
13. Baum DA, Baum B (2014) An inside-out origin for the eukaryotic cell. BMC Biol 12(1):76.
14. Lang BF (2014) Mitochondria and the origin of eukaryotes. Endosymbiosis, ed Löffelhardt W (Springer, Vienna), pp 3-18.
15. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283(5407):1476-1481.
16. Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4(9):a011403.
17. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46(1):1-42.
18. Gray MW (1992) The endosymbiont hypothesis revisited. Int Rev Cytol 141:233-357.
19. Raff RA, Mahler HR (1972) The non symbiotic origin of mitochondria. Science 177(4049):575-582.
20. Mahler HR, Raff RA (1975) The evolutionary origin of the mitochondrion: A nonsymbiotic model. Int Rev Cytol 43:1-124.
21. Uzzell T, Spolsky C (1974) Mitochondria and plastids as endosymbionts: A revival of special creation? Am Sci 62(3):334-343.
22. Lang BF, et al. (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387(6632):493-497.
23. Burger G, Gray MW, Forget L, Lang BF (2013) Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol 5(2):418-438.
24. Gawryluk RMR, Chisholm KA, Pinto DM, Gray MW (2014) Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. J Proteomics 109(0):400-416.
25. Taylor SW, Fahy E, Ghosh SS (2003) Global organellar proteomics. Trends Biotechnol 21(2):82-88.
26. Warnock DE, Fahy E, Taylor SW (2004) Identification of protein associations in organelles, using mass spectrometry-based proteomics. Mass Spectrom Rev 23(4):259-280.
27. Richly E, Chinnery PF, Leister D (2003) Evolutionary diversification of mitochondrial proteomes: Implications for human disease. Trends Genet 19(7):356-362.
28. Smith DGS, et al. (2007) Exploring the mitochondrial proteome of the ciliate protozoon Tetrahymena thermophila: Direct analysis by tandem mass spectrometry. J Mol Biol 374(3):837-863.
29. Atteia A, et al. (2009) A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the α-proteobacterial mitochondrial ancestor. Mol Biol Evol 26(7):1533-1548.
30. Panigrahi AK, et al. (2009) A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9(2):434-450.
31. Gabaldón T, Huynen MA (2004) Shaping the mitochondrial proteome. Biochim Biophys Acta 1659(2-3):212-220.
32. Gabaldón T, Huynen MA (2007) From endosymbiont to host-controlled organelle: The hijacking of mitochondrial protein synthesis and metabolism. PLOS Comput Biol 3(11):e219.
33. Yip CY, Harbour ME, Jayawardena K, Fearnley IM, Sazanov LA (2011) Evolution of respiratory complex I: "Supernumerary" subunits are present in the α-proteobacterial enzyme. J Biol Chem 286(7):5023-5033.
34. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69-92.
35. Gabaldón T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I). J Mol Biol 348(4):857-870.
36. Cardol P (2011) Mitochondrial NADH:ubiquinone oxidoreductase (complex I) in eukaryotes: A highly conserved subunit composition highlighted by mining of protein databases. Biochim Biophys Acta 1807(11):1390-1397.
37. Gawryluk RMR, Chisholm KA, Pinto DM, Gray MW (2012) Composition of the mitochondrial electron transport chain in acanthamoeba castellanii: Structural and evolutionary insights. Biochim Biophys Acta 1817(11):2027-2037.
38. Zíková A, Schnaufer A, Dalley RA, Panigrahi AK, Stuart KD (2009) The F(0) F(1)-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathog 5(5):e1000436.
39. Balabaskaran Nina P, et al. (2010) Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol 8(7):e1000418.
40. Lapaille M, et al. (2010) Atypical subunit composition of the chlorophycean mitochondrial F1FO-ATP synthase and role of Asa7 protein in stability and oligomycin resistance of the enzyme. Mol Biol Evol 27(7):1630-1644.
41. Smits P, Smeitink JAM, van den Heuvel LP, Huynen MA, Ettema TJG (2007) Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res 35(14):4686-4703.
42. Desmond E, Brochier-Armanet C, Forterre P, Gribaldo S (2011) On the last common ancestor and early evolution of eukaryotes: Reconstructing the history of mitochondrial ribosomes. Res Microbiol 162(1):53-70.
43. Zíková A, et al. (2008) Trypanosoma brucei mitochondrial ribosomes: Affinity purification and component identification by mass spectrometry. Mol Cell Proteomics 7(7):1286-1296.
44. Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK (2009) Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci USA 106(24):9637-9642.
45. Dolezal P, Likic V, Tachezy J, Lithgow T (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313(5785):314-318.
46. Koumandou VL, et al. (2013) Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit Rev Biochem Mol Biol 48(4):373-396.
47. Gabaldón T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301(5633):609.
48. Karlberg O, Canbäck B, Kurland CG, Andersson SGE (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17(3):170-187.
49. Kurland CG, Andersson SGE (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64(4):786-820.
50. Martin W, Hoffmeister M, Rotte C, Henze K (2001) An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem 382(11):1521-1539.
51. Sommer MS, Schleiff E (2014) Protein targeting and transport as a necessary consequence of increased cellular complexity. Cold Spring Harb Perspect Biol 6(8):a016055.
52. Lang BF, Burger G (2012) Mitochondrial and eukaryotic origins: A critical review. Mitochondrial Genome Evolution, Advances in Botanical Research, ed Maréchal-Drouard L (Elsevier, Amsterdam), Vol 63, pp 1-20.
53. Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392(6671):37-41.
54. Cavalier-Smith T (1983) Endosymbiotic origin of the mitochondrial envelope. Endocytobiology II, eds Schwemmler W, Schenk HEA (de Gruyter, Berlin), pp 265-279.
55. Cavalier-Smith T (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci 503(1):55-71.
56. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52(Pt 2):297-354.
57. Cavalier-Smith T (2006) Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc Biol Sci 273(1596):1943-1952.
58. Esser C, Martin W, Dagan T (2007) The origin of mitochondria in light of a fluid prokaryotic chromosome model. Biol Lett 3(2):180-184.
59. Thiergart T, Landan G, Schenk M, Dagan T, Martin WF (2012) An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol Evol 4(4):466-485.
60. Gabaldón T, et al. (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 1(1):8.
61. Lester L, Meade A, Pagel M (2006) The slow road to the eukaryotic genome. BioEssays 28(1):57-64.
62. Brindefalk B, Viklund J, Larsson D, Thollesson M, Andersson SGE (2007) Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases. Mol Biol Evol 24(3):743-756.
63. Gabaldón T (2014) Evolutionary considerations on the origin of peroxisomes from the endoplasmic reticulum, and their relationships with mitochondria. Cell Mol Life Sci 71(13):2379-2382.
64. de Duve C (2007) The origin of eukaryotes: A reappraisal. Nat Rev Genet 8(5):395-403.
65. Titorenko VI, Rachubinski RA (2001) The life cycle of the peroxisome. Nat Rev Mol Cell Biol 2(5):357-368.
66. Pan R, Hu J (2011) The conserved fission complex on peroxisomes and mitochondria. Plant Signal Behav 6(6):870-872.
67. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA 105(51):20356-20361.
68. Foster PG, Cox CJ, Embley TM (2009) The primary divisions of life: A phylogenomic approach employing composition-heterogeneous methods. Philos Trans R Soc Lond B Biol Sci 364(1527):2197-2207.
69. Guy L, Ettema TJG (2011) The archaeal 'TACK' superphylum and the origin of eukaryotes. Trends Microbiol 19(12):580-587.
70. Kelly S, Wickstead B, Gull K (2011) Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc Biol Sci 278(1708):1009-1018.
71. Williams TA, Foster PG, Nye TMW, Cox CJ, Embley TM (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Soc 279(1749):4870-4879.
72. Williams TA, Embley TM (2014) Archaeal "dark matter" and the origin of eukaryotes. Genome Biol Evol 6(3):474-481.
73. Guy L, Saw JH, Ettema TJG (2014) The archaeal legacy of eukaryotes: A phylogenomic perspective. Cold Spring Harb Perspect Biol 6(10):a016022.
74. Martijn J, Ettema TJ (2013) From archaeon to eukaryote: The evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans 41(1):451-457.
75. Shutt TE, Gray MW (2006) Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet 22(2):90-95.