Transitional forms between the three domains of life and evolutionary implications

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1723, 2011, Pages 3321-3328

  Reynaud, Emmanuel G ^a   Devos, Damien P ^b  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Archaea; Eukaryotic origin; Evolution; Platypus; Transition forms

Indexed keywords

EUKARYOTE; EVOLUTIONARY BIOLOGY; MONOTREME; PARADIGM SHIFT; PHYLOGENETICS; PROKARYOTE; SPECIATION (BIOLOGY);

ARCHAEA; BACTERIA (MICROORGANISMS); CHLAMYDIAE; EUKARYOTA; PLANCTOMYCETES; VERRUCOMICROBIAE;

EID: 80053935206     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1581     Document Type: Review

References (84)

1. Embley, T. M. & Martin, W. 2006 Eukaryotic evolution, changes and challenges. Nature 440, 623-630. (doi:10.1038/nature04546)
2. Harris, J. K., Kelley, S. T., Spiegelman, G. B. & Pace, N. R. 2003 The genetic core of the universal ancestor. Genome Res. 13, 407-412. (doi:10.1101/gr.652803)
3. Gribaldo, S., Poole, A. M., 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. (doi:10.1038/nrmicro2426)
4. Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. 2008 The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20356-20361. (doi:10.1073/pnas.0810647105)
5. Esser, C. 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. (doi:10.1093/molbev/msh160)
6. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. 1998 Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239-6244. (doi:10.1073/pnas.95.11.6239)
7. Woese, C. R. 2002 On the evolution of cells. Proc. Natl Acad. Sci. USA 99, 8742-8747. (doi:10.1073/pnas.132266999)
8. Wang, M., Yafremava, L. S., Caetano-Anollés, D., Mittenthal, J. E. & Caetano-Anollés, G. 2007 Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res. 17, 1572-1585. (doi:10.1101/gr.6454307)
9. Glansdorff, N., Xu, Y. & Labedan, B. 2008 The last universal common ancestor: emergence, constitution and genetic legacy of an elusive forerunner. Biol. Direct 3, 29. (doi:10.1186/1745-6150-3-29)
10. Sanderson, M. J., McMahon, M. M. & Steel, M. 2010 Phylogenomics with incomplete taxon coverage: the limits to inference. BMC Evol. Biol. 10, 155. (doi:10.1186/1471-2148-10-155)
11. Kamneva, O. K., Liberles, D. A. & Ward, N. L. 2010 Genome-wide influence of indel substitutions on evolution of bacteria of the PVC superphylum, revealed using a novel computational method. Genome Biol. Evol. 2, 870-886. (doi:10.1093/gbe/evq071)
12. Wagner, M. & Horn, M. 2006 The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17, 241-249. (doi:10.1016/j.copbio.2006.05.005)
13. Glöckner, F. O. et al. 2003 Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl Acad. Sci. USA 100, 8298-8303. (doi:10.1073/pnas.1431443100)
14. Griffiths, E. & Gupta, R. S. 2007 Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae. Microbiology 153, 2648-2654. (doi:10.1099/mic.0.2007/009118-0)
15. Heinz, E., Tischler, P., Rattei, T., Myers, G., Wagner, M. & Horn, M. 2009 Comprehensive in silico prediction and analysis of chlamydial outer membrane proteins reflects evolution and life style of the Chlamydiae. BMC Genomics 10, 634. (doi:10.1186/1471-2164-10-634)
16. Pilhofer, M., Rappl, K., Eckl, C., Bauer, A. P., Ludwig, W., Schleifer, K.-H. & Petroni, G. 2008 Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J. Bacteriol. 190, 3192-3202.
17. Staley, J. T., Bouzek, H. & Jenkins, C. 2005 Eukaryotic signature proteins of Prosthecobacter dejongeii and Gemmata sp. Wa-1 as revealed by in silico analysis. FEMS Microbiol. Lett. 243, 9-14. (doi:10.1016/j.femsle.2004.11.034)
18. Strous, M. et al. 2006 Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790-794. (doi:10.1038/nature04647)
19. Ciccarelli, F. D., Doerks, T., von Mering, C., Creevey, C. J., Snel, B. & Bork, P. 2006 Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287. (doi:10.1126/science.1123061)
20. Wang, M. & Caetano-Anolles, G. 2006 Global phylogeny determined by the combination of protein domains in proteomes. Mol. Biol. Evol. 23, 2444-2454. (doi:10.1093/molbev/msl117)
21. Wu, D. et al. 2009 A phylogeny-driven genomic encyclopaedia of bacteria and Archaea. Nature 462, 1056-1060. (doi:10.1038/nature08656)
22. Yang, S., Doolittle, R. F. & Bourne, P. E. 2005 Phylogeny determined by protein domain content. Proc. Natl Acad. Sci. USA 102, 373-378. (doi:10.1073/pnas.0408810102)
23. Teeling, H., Lombardot, T., Bauer, M., Ludwig, W. & Glöckner, F. O. 2004 Evaluation of the phylogenetic position of the planctomycete 'Rhodopirellula baltica' SH 1 bymeans of concatenated ribosomal protein sequences, DNA-directed RNA polymerase subunit sequences and whole genome trees. Int. J. Syst. Evol. Microbiol. 54, 791-801. (doi:10.1099/ijs.0.02913-0)
24. Brochier, C. & Philippe, H. 2002 Phylogeny: a nonhyperthermophilic ancestor for bacteria. Nature 417, 244. (doi:10.1038/417244a)
25. Hou, S. et al. 2008 Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol. Direct 3, 26. (doi:10.1186/1745-6150-3-26)
26. Fuerst, J. A. & Sagulenko, E. 2011 Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat. Rev. Microbiol. 9, 403-413. (doi:10.1038/nrmicro2578)
27. Lindsay, M. R., Webb, R. I., Strous, M., Jetten, M. S., Butler, M. K., Forde, R. J. & Fuerst, J. A. 2001 Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175, 413-429. (doi:10.1007/s002030100280)
28. Lee, K.-C., Webb, R., Janssen, P., Sangwan, P., Romeo, T., Staley, J. & Fuerst, J. 2009 Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol. 9, 5. (doi:10.1186/1471-2180-9-5)
29. Santarella-Mellwig, R., Franke, J., Jaedicke, A., Gorjanacz, M., Bauer, U., Budd, A., Mattaj, I. W. & Devos, D. P. 2010 The compartmentalized bacteria of the planctomycetes-verrucomicrobia-chlamydiae superphylum have membrane coat-like proteins. PLoS Biol.8, e1000281. (doi:10.1371/journal.pbio.1000281)
30. Fuerst, J. A. 2005 Intracellular compartmentation in planctomycetes. Annu. Rev. Microbiol. 59, 299-328. (doi:10.1146/annurev.micro.59.030804.121258)
31. Fuerst, J. A. & Webb, R. I. 1991 Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc. Natl Acad. Sci. USA 88, 8184-8188. (doi:10.1073/pnas.88.18.8184)
32. Devos, D., Dokudovskaya, S., Alber, F., Williams, R., Chait, B. T., Sali, A. & Rout, M. P. 2004 Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol. 2, e380. (doi:10.1371/journal.pbio.0020380)
33. Stephens, R. S. et al. 1998 Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754-759. (doi:10.1126/science.282.5389.754)
34. Tao, S., Kaul, R. & Wenman, W. M. 1991 Identification and nucleotide sequence of a developmentally regulated gene encoding a eukaryotic histone H1-like protein from Chlamydia trachomatis. J. Bacteriol. 173, 2818-2822.
35. Hackstadt, T., Baehr, W. & Ying, Y. 1991 Chlamydia trachomatis developmentally regulated protein is homologous to eukaryotic histone H1. Proc. Natl Acad. Sci. USA 88, 3937-3941. (doi:10.1073/pnas.88.9.3937)
36. Perara, E., Ganem, D. & Engel, J. N. 1992 A developmentally regulated chlamydial gene with apparent homology to eukaryotic histone H1. Proc. Natl Acad. Sci. USA 89, 2125-2129. (doi:10.1073/pnas.89.6.2125)
37. Yee, B., Sagulenko, E. & Fuerst, J. A. 2011 Making heads or tails of the HU proteins in the planctomycete Gemmata obscuriglobus. Microbiology 157, 2012-2021. (doi:10.1099/mic.0.047605-0)
38. Franzmann, P. & Skerman, V. 1984 Gemmata obscuriglobus, a new genus and species of the budding bacteria. Antonie Van Leeuwenhoek 50, 261-268. (doi:10.1007/BF02342136)
39. Desmond, E. & Gribaldo, S. 2009 Phylogenomics of sterol synthesis: insights into the origin, evolution and diversity of a key eukaryotic feature. Genome Biol. Evol. 1, 364-381. (doi:10.1093/gbe/evp036)
40. Pearson, A., Budin, M. & Brocks, J. J. 2003 Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc. Natl Acad. Sci. USA 100, 15352-15357. (doi:10.1073/pnas.2536559100)
41. Kerger, B. D., Mancuso, C. A., Nichols, P. D., White, D. C., Langworthy, T., Sittig, M., Schlesner, H. & Hirsch, P. 1988 The budding bacteria, Pirellula and Planctomyces, with atypical 16S rRNA and absence of peptidoglycan, show eubacterial phospholipids and uniquely high proportions of long chain beta-hydroxy fatty acids in the lipopolysaccharide lipid A. Arch. Microbiol. 149, 255-260. (doi:10.1007/BF00422014)
42. Peretó, J., López-García, P. & Moreira, D. 2004 Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469-477. (doi:10.1016/j.tibs.2004.07.002)
43. Wächtershäuser, G. 2003 From pre-cells to Eukarya: a tale of two lipids. Mol. Microbiol. 47, 13-22. (doi:10.1046/j.1365-2958.2003.03267.x)
44. Sinninghe Damsté, J. S., Strous, M., Rijpstra, W. I. C., Hopmans, E. C., Geenevasen, J. A. J., van Duin, A. C. T., van Niftrik, L. A. & Jetten, M. S. M. 2002 Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419, 708-712. (doi:10.1038/nature01128)
45. Bauer, M., Lombardot, T., Teeling, H., Ward, N. L., Amann, R. I. & Glöckner, F. O. 2004 Archaea-like genes for C1-transfer enzymes in Planctomycetes: phylogenetic implications of their unexpected presence in this phylum. J. Mol. Evol. 59, 571-586. (doi:10.1007/s00239-004-2643-6)
46. Chistoserdova, L., Jenkins, C., Kalyuzhnaya, M. G., Marx, C. J., Lapidus, A., Vorholt, J. A., Staley, J. T. & Lidstrom, M. E. 2004 The enigmatic planctomycetes may hold a key to the origins of methanogenesis andmethylotrophy. Mol. Biol. Evol. 21, 1234-1241. (doi:10.1093/molbev/msh113)
47. Dunfield, P. F. et al. 2007 Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450, 879-882. (doi:10.1038/nature06411)
48. Kalyuzhnaya, M. G., Korotkova, N., Crowther, G., Marx, C. J., Lidstrom, M. E. & Chistoserdova, L. 2005 Analysis of gene islands involved in methanopterinlinked C1 transfer reactions reveals new functions and provides evolutionary insights. J. Bacteriol. 187, 4607-4614. (doi:10.1128/JB.187.13.4607-4614.2005)
49. Pilhofer, M., Rosati, G., Ludwig, W., Schleifer, K.-H. & Petroni, G. 2007 Coexistence of tubulins and ftsZ in different Prosthecobacter species. Mol. Biol. Evol. 24, 1439-1442. (doi:10.1093/molbev/msm069)
50. Yee, B., Lafi, F. F., Oakley, B., Staley, J. T. & Fuerst, J. A. 2007 A canonical FtsZ protein in Verrucomicrobium spinosum, a member of the Bacterial phylum Verrucomicrobia that also includes tubulin-producing Prosthecobacter species. BMC Evol. Biol. 7, 37. (doi:10.1186/1471-2148-7-37)
51. Jenkins, C. et al. 2002 Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc. Natl Acad. Sci. USA 99, 17049-17054.
52. Schlieper, D., Oliva, M. A., Andreu, J. M. & Löwe, J. 2005 Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc. Natl Acad. Sci. USA 102, 9170-9175. (doi:10.1073/pnas.0502859102)
53. Sontag, C. A., Staley, J. T. & Erickson, H. P. 2005 In vitro assembly and GTP hydrolysis by bacterial tubulins BtubA and BtubB. J. Cell Biol. 169, 233-238. (doi:10.1083/jcb.200410027)
54. Sontag, C. A., Sage, H. & Erickson, H. P. 2009 BtubABtubB Heterodimer is an essential intermediate in Protofilament assembly. PLoS ONE 4, e7253. (doi:10.1371/journal.pone.0007253)
55. Dienes, L. & Bullivant, S. 1968 Morphology and reproductive processes of the L forms of bacteria. II. Comparative study of L forms and Mycoplasma with the electron microscope. J. Bacteriol. 95, 672-687.
56. Leaver, M., Domínguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. 2009 Life without a wall or division machine in Bacillus subtilis. Nature 457, 849-853. (doi:10.1038/nature07742)
57. Onoda, T., Enokizono, J., Kaya, H., Oshima, A., Freestone, P. & Norris, V. 2000 Effects of calcium and calcium chelators on growth and morphology of Escherichia coli L-form NC-7. J. Bacteriol. 182, 1419-1422. (doi:10.1128/JB.182.5.1419-1422.2000)
58. Joseleau-Petit, D., Liébart, J.-C., Ayala, J. A. & D'Ari, R. 2007 Unstable Escherichia coli L forms revisited: growth requires peptidoglycan synthesis. J. Bacteriol. 189, 6512-6520. (doi:10.1128/JB.00273-07)
59. Leung, K. F., Dacks, J. B. & Field, M. C. 2008 Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698-1716. (doi:10.1111/j.1600-0854.2008.00797.x)
60. Lonhienne, T. G. A., Sagulenko, E., Webb, R. I., Lee, K.-C., Franke, J., Devos, D. P., Nouwens, A., Carroll, B. J. & Fuerst, J. A. 2010 Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc. Natl Acad. Sci. USA 107, 12883-12888. (doi:10.1073/pnas.1001085107)
61. Murat, D., Byrne, M. & Komeili, A. 2010 Cell biology of prokaryotic organelles. Cold Spring Harbor Perspect. Biol. 2, (doi:10.1101/cshperspect.a000422)
62. Löwe, J. & Amos, L. A.2009 Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochemis. Cell Biol. 41, 323-329. (doi:10.1016/j.biocel.2008.08.010)
63. Devos, D. P. & Reynaud, E. G. 2010 Evolution. Intermediate steps. Science 330, 1187-1188. (doi:10.1126/science.1196720)
64. Forterre, P. 2010 A new fusion hypothesis for the origin of Eukarya: better than previous ones, but probably also wrong. Res. Microbiol. 162, 77-91. (doi:10.1016/j.resmic.2010.10.005)
65. Fuchsman, C. A. & Rocap, G. 2006 Whole-genome reciprocal BLAST analysis reveals that planctomycetes do not share an unusually large number of genes with Eukarya and Archaea. Appl. Environ. Microbiol. 72, 6841-6844. (doi:10.1128/AEM.00429-06)
66. De Duve, C. & Wattiaux, R. 1966 Functions of lysosomes. Annu. Rev. Physiol. 28, 435-492. (doi:10.1146/annurev.ph.28.030166.002251)
67. Dacks, J.B. & Field, M.C. 2007 Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J. Cell. Sci. 120, 2977-2985. (doi:10.1242/jcs.013250)
68. Degrasse, J. A., Dubois, K. N., Devos, D., Siegel, T. N., Sali, A., Field, M. C., Rout, M. P. & Chait, B. T. 2009 Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell Proteomics 8, 2119-2130. (doi:10.1074/mcp.M900038-MCP200)
69. Field, M. C. & Dacks, J. B. 2009 First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol. 21, 4-13. (doi:10.1016/j.ceb.2008.12.004)
70. Saier, M. H. 2006 Protein secretion and membrane insertion systems in gram-negative bacteria. J. Membr. Biol. 214, 75-90. (doi:10.1007/s00232-006-0049-7)
71. Fu, X., Jiao, W. & Chang, Z. 2006 Phylogenetic and biochemical studies reveal a potential evolutionary origin of small heat shock proteins of animals from bacterial class A. J. Mol. Evol. 62, 257-266. (doi:10.1007/s00239-005-0076-5)
72. Walsh, N. P., Alba, B. M., Bose, B., Gross, C. A. & Sauer, R. T. 2003 OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113, 61-71. (doi:10.1016/S0092-8674(03)00203-4)
73. Mashburn-Warren, L. M. & Whiteley, M. 2006 Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61, 839-846. (doi:10.1111/j.1365-2958.2006.05272.x)
74. Aires, J. R. & Nikaido, H. 2005 Aminoglycosides are captured from both periplasm and cytoplasm by the AcrD multidrug efflux transporter ofEscherichia coli. J. Bacteriol. 187, 1923-1929. (doi:10.1128/JB.187.6.1923-1929.2005)
75. Krupa, A. & Srinivasan, N. 2002 Lipopolysaccharide phosphorylating enzymes encoded in the genomes of Gramnegative bacteria are related to the eukaryotic protein kinases. Protein Sci. 11, 1580-1584. (doi:10.1110/ps.3560102)
76. van Niftrik, L. A., Fuerst, J. A., Sinninghe Damsté, J. S., Kuenen, J. G., Jetten, M. S. M. & Strous, M. 2004 The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol. Lett. 233, 7-13. (doi:10.1016/j.femsle.2004.01.044)
77. Rachel, R., Wyschkony, I., Riehl, S. & Huber, H. 2002 The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1, 9-18. (doi:10.1155/2002/307480)
78. Makarova, K. S., Yutin, N., Bell, S. D. & Koonin, E. V. 2010 Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731-741. (doi:10.1038/nrmicro2406)
79. Cavalier-Smith, T. 2002 The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol. 52, 7-76.
80. Gil, R., Latorre, A. & Moya, A. 2004 Bacterial endosymbionts of insects: insights from comparative genomics. Environ. Microbiol. 6, 1109-1122. (doi:10.1111/j.1462-2920.2004.00691.x)
81. Desmond, E., Brochier-Armanet, C., Forterre, P. & Gribaldo, S. 2010 On the last common ancestor and early evolution of eukaryotes: reconstructing the history of mitochondrial ribosomes. Res. Microbiol. 162, 53-70. (doi:10.1016/j.resmic.2010.10.004)
82. Brinkman, F. S. L. et al. 2002 Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and thechloroplast. Genome Res. 12, 1159-1167. (doi:10.1101/gr.341802)
83. Kurland, C. G. & Andersson, S. G. E. 2000 Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786-820. (doi:10.1128/MMBR.64.4.786-820.2000)
84. Searcy, D. G. 2003 Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 13, 229-238. (doi:10.1038/sj.cr.7290168)