Evolution of mitochondria reconstructed from the energy metabolism of living bacteria

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Esposti, Mauro Degli ^a   Chouaia, Bessem ^b   Comandatore, Francesco ^b   Crotti, Elena ^b   Sassera, Davide ^b,c   Lievens, Patricia Marie Jeanne ^a,d   Daffonchio, Daniele ^b   Bandi, Claudio ^b  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 3; PROSTAGLANDIN SYNTHASE;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOENERGY; CONTROLLED STUDY; COX GENE; ENERGY METABOLISM; EVOLUTION; GENETIC ANALYSIS; GENETIC VARIABILITY; METHYLOTROPH; METHYLOTROPHIC BACTERIUM; MITOCHONDRION; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYLOGENY;

EID: 84900560869     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096566     Document Type: Article

References (89)

1. Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4: a011403.
2. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467: 929-934.
3. Margulis L (1996) Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci U S A 93: 1071-1076.
4. Andersson SG, Karlberg O, Canbäck B, Kurland CG (2003) On the origin of mitochondria: a genomics perspective. Philos Trans R Soc Lond B Biol Sci 358: 165-177.
5. Williams KP, Sobral BW, Dickerman AW (2007) A robust species tree for the alphaproteobacteria. J Bacteriol 189: 4578-4586. (Pubitemid 47025569)
6. Abhishek A, Bavishi A, Bavishi A, Choudhary M (2011) Bacterial genome chimaerism and the origin of mitochondria. Can J Microbiol 57: 49-61.
7. Georgiades K, Raoult D (2011) The rhizome of Reclinomonas americana, Homo sapiens, Pediculus humanus and Saccharomyces cerevisiae mitochondria. Biol Direct 6: 55.
8. 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: 466-485.
9. Gribaldo S, Poole AM, Daubin V, Forterre P, Brochier-Armanet C (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 8: 743-752.
10. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76: 444-495.
11. Searcy DG (2003) Metabolic integration during the evolutionary origin of mitochondria. Cell Res 13: 229-238.
12. Gabaldón T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301: 609. (Pubitemid 36927938)
13. Brindefalk B, Ettema TJG, Viklund J, Thollesson M, Andersson SGE (2011) A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLOS ONE 6: e24457.
14. Georgiades K, Madoui M-A, Le P Robert C, Raoult D (2011) Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PLOS ONE 6: e24857.
15. Rodríguez-Ezpeleta N, Embley TM (2012) The SAR11 group of alpha-proteobacteria is not related to the origin of mitochondria. PLOS ONE 7: e30520.
16. Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, et al (2004) A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 21: 1643-1660. (Pubitemid 39096881)
17. Yip C, Harbour ME, Jayawardena K, Fearnley IM, Sazanov LA (2011) Evolution of respiratory complex I: 'supernumerary' subunits are present in the alpha-proteobacterial enzyme. J Biol Chem 286: 5023-5033.
18. Clements A, Bursac D, Gatsos X, Perry AJ, Civciristov S, et al (2009) The reducible complexity of a mitochondrial molecular machine. Proc Natl Acad Sci U S A 106: 15791-15795.
19. Davidov Y, Huchon D, Koval SF, Jurkevitch E (2006) A new alpha-proteobacterial clade of Bdellovibrio-like predators: implications for the mitochondrial endosymbiotic theory. Environ Microbiol 8: 2179-2188. (Pubitemid 44730248)
20. Atteia A, Adrait A, Brugière S, Tardif M, van Lis R, 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 alpha-proteobacterial mitochondrial ancestor. Mol Biol Evol 26: 1533-1548.
21. Sassera D, Lo N, Epis S, D'Auria G, Montagna M, et al (2011) Phylogenomic evidence for the presence of a flagellum and cbb(3) oxidase in the free-living mitochondrial ancestor. Mol Biol Evol 28: 3285-3296.
22. Chouaia B, Gaiarsa S, Crotti E, Comandatore F, Degli Esposti M, et al (2014) Acetic acid bacteria genomes reveal functional traits for adaptation to life in insect guts. Genome Biol Evol, in press.
23. Kim SW, Fushinobu S, Zhou S, Wakagi T, Shoun H (2009) Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the proto-mitochondrion? Appl Environ Microbiol 75: 2652-2658.
24. Johnston DT, Wolfe-Simon F, Pearson A, Knoll AH (2009). Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age. Proc Natl Acad Sci U S A 106: 16925-16929.
25. Borisov VB, Gennis RB, Hemp J, Verkhovsky MI (2011) The cytochrome bd respiratory oxygen reductases. Biochim Biophys Acta 1807: 1398-1413
26. Sousa FL, Alves RJ, Ribeiro MA, Pereira-Leal JB, Teixeira M, et al (2012) The superfamily of heme-copper oxygen reductases: types and evolutionary considerations. Biochim Biophys Acta 1817: 629-637
27. Ducluzeau AL, Ouchane S, Nitschke W(2008) The cbb3 oxidases are an ancient innovation of the domain bacteria. Mol Biol Evol 25: 1158-1166.
28. McLeod MP, Qin X, Karpathy SE, Gioia J, Highlander SK, et al (2004) Complete genome sequence of Rickettsia typhi and comparison with sequences of other rickettsiae. J Bacteriol 186: 5842-5855. (Pubitemid 39128658)
29. Takaya N (2009) Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci Biotechnol Biochem 73: 1-8.
30. Vlaeminck SE, Hay AG, Maignien L, Verstraete W (2011) In quest of the nitrogen oxidizing prokaryotes of the early Earth. Environ Microbiol 13: 283-295.
31. Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4: 44.
32. Simon J, Klotz MG (2013) Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochim Biophys Acta 1827: 114-135.
33. Tamas I, Dedysh SN, Liesack W, Stott MB, Alam M, et al (2010) Complete genome sequence of Beijerinckia indica subsp. indica. J Bacteriol 192: 4532-4533.
34. Shih PM, Matzke NJ (2013) Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci U S A 110: 12355-12360.
35. Slot JC, Hibbett DS (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLOS ONE 2: e1097.
36. Lin JT, Goldman BS, Stewart V (1994) The nasFEDCBA operon for nitrate and nitrite assimilation in Klebsiella pneumoniae M5al. J Bacteriol 176: 2551-2559. (Pubitemid 24139033)
37. Lebrun E, Santini JM, Brugna M, Ducluzeau AL, Ouchane S et al (2006) The Rieske protein: a case study on the pitfalls of multiple sequence alignments and phylogenetic reconstruction. Mol Biol Evol 23: 1180-1191. (Pubitemid 43781593)
38. Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181: 6573-6584. (Pubitemid 29517969)
39. Mohan SB, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49: 433-443. (Pubitemid 39119600)
40. Zhang Y, Rump S, Gladyshev VN (2011) Comparative Genomics and Evolution of Molybdenum Utilization. Coord Chem Rev 255: 1206-1217.
41. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39 (Database issue): D225-9.
42. Lee SJ, McCormick MS, Lippard SJ, Cho US (2013) Control of substrate access to the active site in methane monooxygenase. Nature 494: 380-384.
43. Chistoserdova L, Kalyuzhnaya MG, Lidstrom ME (2009) The expanding world of methylotrophic metabolism. Annu Rev Microbiol 63: 477-499.
44. Stewart JJ, Coyne KJ (2011) Analysis of raphidophyte assimilatory nitrate reductase reveals unique domain architecture incorporating a 2/2 hemoglobin. Plant Mol Biol 77: 565-575.
45. Lau E, Fisher MC, Steudler PA, Cavanaugh CM (2013) The methanol dehydrogenase gene, mxaF, as a functional and phylogenetic marker for proteobacterial methanotrophs in natural environments. POS ONE 8: e56993.
46. Liu X, Taber HW (1998) Catabolite regulation of the Bacillus subtilis ctaBCDEF gene cluster. J Bacteriol 180: 6154-6163. (Pubitemid 28544245)
47. Radzi Noor M, Soulimane T (2012) Bioenergetics at extreme temperature: Thermus thermophilus ba(3)- and caa(3)-type cytochrome c oxidases. Biochim Biophys Acta 1817: 638-649.
48. Burger G, Gray MW, Forget L, Lang BF (2013) Strikingly Bacteria-Like and Gene-Rich Mitochondrial Genomes throughout jakobid protists. Genome Biol Evol 5: 418-438.
49. Hussain H, Grove J, Griffiths L, Busby S, Cole J (1994) A seven-gene operon essential for formate-dependent nitrite reduction to ammonia by enteric bacteria. Mol Microbiol 12: 153-163. (Pubitemid 24197453)
50. Refojo PN, Sousa FL, Teixeira M, Pereira MM (2010) The alternative complex III: a different architecture using known building systems. Biochim Biophys Acta 1797: 1869-1876.
51. Starkenburg SR, Larimer FW, Stein LY, Klotz MG, Chain PS, et al (2008) Complete genome sequence of Nitrobacter hamburgensis X14 and comparative genomic analysis of species within the genus Nitrobacter. Appl Environ Microbiol 74: 2852-2863. (Pubitemid 351632616)
52. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J (2012). The Pfam protein families database. Nucleic Acids Res 40 (Database issue): D290-301.
53. Svensson-Ek M, Abramson J, Larsson G, Törnroth S, Brzezinski P, et al (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J Mol Biol 321: 329-339.
54. Lyons JA, Aragão D, Slattery O, Pisliakov AV, Soulimane T, et al (2012). Structural insights into electron transfer in caa3-type cytochrome oxidase. Nature 487: 514-518.
55. Torriani SF, Goodwin SB, Kema GH, Pangilinan JL, McDonald BA (2008) Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 45: 628-637.
56. Swart EC, Bracht JR, Magrini V, Minx P, Chen X, et al (2013) The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol 11: e1001473.
57. Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, et al (2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19: 3347-3368.
58. de Graaf RM, van Alen TA, Dutilh BE, Kuiper JW, van Zoggel HJ, et al (2009) The mitochondrial genomes of the ciliates Euplotes minuta and Euplotes crassus. BMC Genomics 10: 514.
59. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, et al (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272: 1136-1144.
60. Shinzawa-Itoh K, Aoyama H, Muramoto K, Terada H, Kurauchi T, et al (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26: 1713-1725. (Pubitemid 46480942)
61. Harrenga A, Michel H (1999) The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction. J Biol Chem 274: 33296-33299. (Pubitemid 129511629)
62. Qin L, Hiser C, Mulichak A, Garavito RM, Ferguson-Miller S (2006) Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc Natl Acad Sci U S A 103: 16117-16122. (Pubitemid 44715161)
63. Yanyushin MF, del Rosario MC, Brune DC, Blankenship RE (2005) New class of bacterial membrane oxidoreductases. Biochemistry 44: 10037-10045. (Pubitemid 41076799)
64. Brochier-Armanet C, Talla E, Gribaldo S (2009) The multiple evolutionary histories of dioxygen reductases: Implications for the origin and evolution of aerobic respiration. Mol Biol Evol 26: 285-297.
65. Thöny-Meyer L (1997) Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61: 337-376.
66. Kartal B, de Almeida NM, Maalcke WJ, Op den Camp HJ, Jetten MS, et al (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37: 428-461.
67. Budd A, Devos DP (2012) Evaluating the Evolutionary Origins of Unexpected Character Distributions within the Bacterial Planctomycetes-Verrucomicrobia- Chlamydiae Superphylum. Front Microbiol 3: 401.
68. Berry EA, Huang LS, Saechao LK, Pon NG, Valkova-Valchanova M, et al (2004) X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc (1): Comparison with its Mitochondrial and Chloroplast Counterparts. Photosynth Res 81: 251-275. (Pubitemid 39059689)
69. Esser L, Elberry M, Zhou F, Yu CA, Yu L, et al (2008) Inhibitor-complexed structures of the cytochrome bc1 from the photosynthetic bacterium Rhodobacter sphaeroides. J Biol Chem 283: 2846-2857.
70. Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, et al (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392: 677-684. (Pubitemid 28207780)
71. Kolling DJ, Brunzelle JS, Lhee S, Crofts AR, Nair SK (2007) Atomic resolution structures of rieske iron-sulfur protein: role of hydrogen bonds in tuning the redox potential of iron-sulfur clusters. Structure 15: 29-38. (Pubitemid 46091746)
72. Degli Esposti M, De Vries S, Crimi M, Ghelli A, Patarnello T, et al (1993). Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta 1143: 243-271. (Pubitemid 23216735)
73. Valas RE, Bourne PE (2009) Structural analysis of polarizing indels: an emerging consensus on the root of the tree of life. Biol Direct 4: 30.
74. Ouchane S, Nitschke W, Bianco P, Vermeglio A, Astier C (2005) Multiple Rieske genes in prokaryotes: exchangeable Rieske subunits in the cytochrome bc-complex of Rubrivivax gelatinosus. Mol Microbiol 57: 261-275. (Pubitemid 40896613)
75. Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, et al (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci U S A 107: 13479-13484.
76. Schübbe S, Williams TJ, Xie G, Kiss HE, Brettin TS, et al (2009) Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 75: 4835-4852.
77. Simmons SS, Isokpehi RD, Brown SD, McAllister DL, Hall CC, et al (2011) Functional Annotation Analytics of Rhodopseudomonas palustris Genomes. Bioinform Biol Insights 5: 115-129.
78. Bratton MR, Pressler MA, Hosler JP (1999) Suicide inactivation of cytochrome c oxidase: catalytic turnover in the absence of subunit III alters the active site. Biochemistry 38: 16236-16245. (Pubitemid 129520544)
79. Cunningham L, Pitt M, Williams HD (1997) The cioAB genes from Pseudomonas aeruginosa code for a novel cyanide-insensitive terminal oxidase related to the cytochrome bd quinol oxidases. Mol Microbiol 24: 579-591. (Pubitemid 27241705)
80. Boratyn GM, Schäffer AA, Agarwala R, Altschul SF, Lipman DJ, et al (2012). Domain enhanced lookup time accelerated BLAST. Biol Direct 7: 12.
81. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ (1998) Bioinformatics 14: 892-893.
82. Price MN, Arkin AP, Alm EJ (2006) The life-cycle of operons. PLoS Genet 2: e96.
83. Hung CL, Lee C, Lin CY, Chang CH, Chung YC, et al (2010) Feature amplified voting algorithm for functional analysis of protein superfamily. BMC Genomics 11 (Suppl 3): S14.
84. Dam B, Dam S, Kube M, Reinhardt R, Liesack W (2012) Complete genome sequence of Methylocystis sp. strain SC2, an aerobic methanotroph with highaffinity methane oxidation potential. J. Bacteriol 194: 6008-6009.
85. Lange C, Hunte C (2002) Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c. Proc Natl Acad Sci U S A 99: 2800- 2805.
86. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci U S A 82: 4443-4447. (Pubitemid 15234250)
87. Fitzpatrick DA, Creevey CJ, McInerney JO (2006) Genome phylogenies indicate a meaningful alpha-proteobacterial phylogeny and support a grouping of the mitochondria with the Rickettsiales. Mol Biol Evol 23: 74-85. (Pubitemid 41785955)
88. Sakurai K, Arai H, Ishii M, Igarashi Y (2011) Transcriptome response to different carbon sources in Acetobacter aceti. Microbiology 157 (Pt 3): 899-910.
89. Gómez-Manzo S, Chavez-Pacheco JL, Contreras-Zentella M, Sosa-Torres ME, Arreguín-Espinosa R, et al (2010) Molecular and catalytic properties of the aldehyde dehydrogenase of Gluconacetobacter diazotrophicus, a quinoheme protein containing pyrroloquinoline quinone, cytochrome b, and cytochrome c. J Bacteriol 192: 5718-5724.