The evolution of eukaryotic cells from the perspective of peroxisomes: Phylogenetic analyses of peroxisomal beta-oxidation enzymes support mitochondria-first models of eukaryotic cell evolution

BioEssays

Volumn 37, Issue 2, 2015, Pages 195-203

  Bolte, Kathrin ^a   Rensing, Stefan A ^a,b   Maier, Uwe G ^a,c  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c Offensive for the Development of Scientific and Economic Excellence of the State of Hesse LOEWE   (Germany)

Author keywords

Alpha proteobacteria; Eukaryotic cell evolution; Fatty acid beta oxidation; Mitochondria; Peroxisomes

Indexed keywords

FATTY ACID;

ALPHAPROTEOBACTERIA; ARCHAEON; ARTICLE; BACTERIA; EUKARYOTE; EUKARYOTIC CELL; FATTY ACID OXIDATION; HOST CELL; KINETOPLASTIDA; MICROBODY; MITOCHONDRION; NONHUMAN; PEROXISOME; PHYLOGENY; PROTEIN CONTENT; METABOLISM; OXIDATION REDUCTION REACTION;

ALPHAPROTEOBACTERIA; ARCHAEA; EUKARYOTA; PROTEOBACTERIA;

EUKARYOTIC CELLS; FATTY ACIDS; MITOCHONDRIA; OXIDATION-REDUCTION; PEROXISOMES; PHYLOGENY;

EID: 84921472269     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400151     Document Type: Article

References (66)

1. Woese CR, Fox GE. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74: 5088-90.
2. Woese CR, Kandler O, Wheelis ML. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87: 4576-9.
3. Williams TA, Foster PG, Cox CJ, Embley TM. 2013. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504: 231-6.
4. Williams TA, Embley TM. 2014. Archaeal "dark matter" and the origin of eukaryotes. Genome Biol Evol 6: 474-81.
5. 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: 449-55.
6. Gray MW. 2012. Mitochondrial evolution. Cold Spring Harb Perspect Biol 4: a011403.
7. Müller M, Mentel M, van Hellemond JJ, Henze K, et al. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76: 444-95.
8. Keeling PJ. 2013. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64: 583-607.
9. Bolte K, Bullmann L, Hempel F, Bozarth A, et al. 2009. Protein targeting into secondary plastids. J Eukaryot Microbiol 56: 9-15.
10. Price DC, Chan CX, Yoon HS, Yang EC, et al. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335: 843-7.
11. Islinger M, Grille S, Fahimi HD, Schrader M. 2012. The peroxisome: an update on mysteries. Histochem Cell Biol 137: 547-74.
12. de Duve C. 1982. Peroxisomes and related particles in historical perspective. Ann N Y Acad Sci 386: 1-4.
13. de Duve C. 1983. Microbodies in the living cell. Sci Am 248: 74-84.
14. Cavalier-Smith T. 1987. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci 503: 55-71.
15. Balsera M, Soll J, Bolter B. 2009. Protein import machineries in endosymbiotic organelles. Cell Mol Life Sci 66: 1903-23.
16. Schluter A, Fourcade S, Ripp R, Mandel JL, et al. 2006. The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol Biol Evol 23: 838-45.
17. Gabaldón T, Snel B, van Zimmeren F, Hemrika W, et al. 2006. Origin and evolution of the peroxisomal proteome. Biol Direct 1: 8.
18. Schliebs W, Girzalsky W, Erdmann R. 2010. Peroxisomal protein import and ERAD: variations on a common theme. Nat Rev Mol Cell Biol 11: 885-90.
19. Bolte K, Gruenheit N, Felsner G, Sommer MS, et al. 2011. Making new out of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. BioEssays 33: 368-76.
20. Hoepfner D, Schildknegt D, Braakman I, Philippsen P, et al. 2005. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122: 85-95.
21. van der Zand A, Braakman I, Tabak HF. 2010. Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol Biol Cell 21: 2057-65.
22. van der Zand A, Gent J, Braakman I, Tabak HF. 2012. Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 149: 397-409.
23. Mohanty A, McBride HM. 2013. Emerging roles of mitochondria in the evolution, biogenesis, and function of peroxisomes. Front Physiol 4: 268.
24. Dagan T, Artzy-Randrup Y, Martin W. 2008. Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci USA 105: 10039-44.
25. Dacks JB, Peden AA, Field MC. 2009. Evolution of specificity in the eukaryotic endomembrane system. Int J Biochem Cell Biol 41: 330-40.
26. Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11: 209.
27. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nature 440: 623-30.
28. Sogin ML. 1991. Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1: 457-63.
29. Searcy DG. 1992. Origins of mitochondria and chloroplasts from sulphur-based symbioses. In Hartmann H, Matsuno H, eds; The Origin and Evolution of the Cell. Singapore: World Scientific. p. 47-78.
30. Lake JA, Moore JE, Simonson AB, Rivera MC. 2005. Fullfilling Darwin's dream. In Sapp J, ed; Microbial phylogeny and evolution. New York: Oxford University Press. p. 184-206.
31. Gupta RS, Golding GB. 1996. The origin of the eukaryotic cell. Trends Biochem Sci 21: 166-71.
32. Martin W, Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392: 37-41.
33. Moreira D, Lopez-Garcia P. 1998. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol 47: 517-30.
34. Vellai T, Takacs K, Vida G. 1998. A new aspect to the origin and evolution of eukaryotes. J Mol Evol 46: 499-507.
35. Margulis L, Dolan MF, Guerrero R. 2000. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci USA 97: 6954-9.
36. Cavalier-Smith T. 2009. Predation and eukaryote cell origins: a coevolutionary perspective. Int J Biochem Cell Biol 41: 307-22.
37. Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52: 297-354.
38. Cavalier-Smith T. 1975. The origin of nuclei and of eukaryotic cells. Nature 256: 463-8.
39. Speijer D. 2011. Oxygen radicals shaping evolution: Why fatty acid catabolism leads to peroxisomes while neurons do without it. BioEssays 33: 88-94.
40. Speijer D. 2014. How the mitochondrion was shaped by radical differences in substrates. BioEssays 36: 634-43.
41. Wanders RJ, Ferdinandusse S, Brites P, Kemp S. 2010. Peroxisomes, lipid metabolism and lipotoxicity. Biochim Biophys Acta 1801: 272-80.
42. Mannaerts GP, van Veldhoven PP. 1996. Functions and organization of peroxisomal beta-oxidation. Ann N Y Acad Sci 804: 99-115.
43. Baker A, Graham IA, Holdsworth M, Smith SM, et al. 2006. Chewing the fat: beta-oxidation in signalling and development. Trends Plant Sci 11: 124-32.
44. Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK. 2006. Peroxisomal beta-oxidation - a metabolic pathway with multiple functions. Biochim Biophys Acta 1763: 1413-26.
45. Wanders RJ, Waterham HR. 2006. Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75: 295-332.
46. Barlett K, Eaton S. 2004. Mitochondrial β-oxidation. Eur J Biochem 271: 462-9.
47. Ramsay RR. 2000. The carnitine acyltransferases: modulators of acyl-CoA-dependent reactions. Biochem Soc Trans 28: 182-6.
48. Klenk HP, Clayton RA, Tomb JF, White O, et al. 1997. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390: 364-70.
49. Mardanov AV, Gumerov VM, Beletsky AV, Prokofeva MI, et al. 2011. Complete genome sequence of the thermoacidophilic crenarchaeon Thermoproteus uzoniensis 768-20. J Bacteriol 193: 3156-7.
50. Gumerov VM, Mardanov AV, Beletsky AV, Prokofeva MI, et al. 2011. Complete genome sequence of "Vulcanisaeta moutnovskia" strain 768-28, a novel member of the hyperthermophilic crenarchaeal genus Vulcanisaeta. J Bacteriol 193: 2355-6.
51. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-4.
52. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-3.
53. Shen YQ, Lang BF, Burger G. 2009. Diversity and dispersal of a ubiquitous protein family: acyl-CoA dehydrogenases. Nucleic Acids Res 37: 5619-31.
54. Gabaldón T. 2014. A metabolic scenario for the evolutionary origin of peroxisomes from the endomembranous system. Cell Mol Life Sci 71: 2373-6.
55. Gabaldón T. 2014. Evolutionary considerations on the origin of peroxisomes from the endoplasmic reticulum, and their relationships with mitochondria. Cell Mol Life Sci 71: 2379-82.
56. Speijer D. 2014. Reconsidering ideas regarding the evolution of peroxisomes: the case for a mitochondrial connection. Cell Mol Life Sci 71: 2377-8.
57. Martin W, Koonin EV. 2006. Introns and the origin of nucleus-cytosol compartmentalization. Nature 440: 41-5.
58. Altschul SF, Madden TL, Schaffer AA, Zhang J, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-402.
59. Katoh K, Kuma K-i, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-8.
60. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20: 426-7.
61. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-5.
62. Schluter A, Fourcade S, Domenech-Estevez E, Gabaldon T, et al. 2007. PeroxisomeDB: a database for the peroxisomal proteome, functional genomics and disease. Nucleic Acids Res 35: D815-22.
63. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, et al. 2003. Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328: 581-92.
64. Rachubinski RA, Subramani S. 1995. How proteins penetrate peroxisomes. Cell 83: 525-8.
65. Rucktäschel R, Girzalsky W, Erdmann R. 2011. Protein import machineries of peroxisomes. Biochim Biophys Acta 1808: 892-900.
66. Reumann S, Babujee L, Ma C, Wienkoop S, et al. 2007. Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19: 3170-93.