Ribosomal proteins: Toward a next generation standard for prokaryotic systematics?

Molecular Phylogenetics and Evolution

Volumn 75, Issue 1, 2014, Pages 103-117

  Ramulu, Hemalatha Golaconda ^a,c   Groussin, Mathieu ^b,d   Talla, Emmanuel ^a   Planel, Remi ^a   Daubin, Vincent ^b   Brochier Armanet, Céline ^b  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITÉ LYON 1   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Compositional bias; Endosymbionts; Horizontal gene transfer; Long branch attraction; Non homogeneous models; SAR11

Indexed keywords

BACTERIAL DNA; RIBOSOME PROTEIN;

ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; COMPOSITIONAL BIAS; DNA SEQUENCE; ENDOSYMBIONTS; EPSILONPROTEOBACTERIA; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; LONG BRANCH ATTRACTION; NON-HOMOGENEOUS MODELS; PHYLOGENY; PROTEOBACTERIA; SAR11; SMALL RIBOSOMAL SUBUNIT; STATISTICAL MODEL;

COMPOSITIONAL BIAS; ENDOSYMBIONTS; HORIZONTAL GENE TRANSFER; LONG BRANCH ATTRACTION; NON-HOMOGENEOUS MODELS; SAR11;

BAYES THEOREM; BIOLOGICAL EVOLUTION; DNA, BACTERIAL; EPSILONPROTEOBACTERIA; GENE TRANSFER, HORIZONTAL; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY; PROTEOBACTERIA; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; SEQUENCE ANALYSIS, DNA;

EID: 84896030351     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2014.02.013     Document Type: Article

References (91)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Abby S.S., Tannier E., Gouy M., Daubin V. Detecting lateral gene transfers by statistical reconciliation of phylogenetic forests. BMC Bioinform. 2010, 11:324.
3. Abby S.S., Tannier E., Gouy M., Daubin V. Lateral gene transfer as a support for the tree of life. Proc. Natl. Acad. Sci. USA 2012, 109:4962-4967.
4. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 1997, 25:3389-3402.
5. Badger J.H., Eisen J.A., Ward N.L. Genomic analysis of Hyphomonas neptunium contradicts 16S rRNA gene-based phylogenetic analysis: implications for the taxonomy of the orders 'Rhodobacterales' and Caulobacterales. Int. J. Syst. Evol. Microbiol. 2005, 55:1021-1026.
6. Bazylinski D.A., Williams T.J., Lefevre C.T., Berg R.J., Zhang C.L., Bowser S.S., Dean A.J., Beveridge T.J. Magnetococcus marinus gen. nov., sp. nov., a marine, magnetotactic bacterium that represents a novel lineage (Magnetococcaceae fam. nov., Magnetococcales ord. nov.) at the base of the Alphaproteobacteria. Int. J. Syst. Evol. Microbiol. 2013, 63:801-808.
7. Bergsten J. A review of long-branch attraction. Cladistics 2005, 21:163-193.
8. Boussau B., Gouy M. Efficient likelihood computations with nonreversible models of evolution. Syst. Biol. 2006, 55:756-768.
9. Brindefalk B., Ettema T.J., Viklund J., Thollesson M., Andersson S.G. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PloS One 2011, 6:e24457.
10. Brochier C., Bapteste E., Moreira D., Philippe H. Eubacterial phylogeny based on translational apparatus proteins. Trends Gen.: TIG 2002, 18:1-5.
11. Brochier C., Philippe H., Moreira D. The evolutionary history of ribosomal protein RpS14: horizontal gene transfer at the heart of the ribosome. Trends Gen.: TIG 2000, 16:529-533.
12. Brown J.R., Douady C.J., Italia M.J., Marshall W.E., Stanhope M.J. Universal trees based on large combined protein sequence data sets. Nat. Gen. 2001, 28:281-285.
13. Cavalier-Smith T. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol. 2002, 52:7-76.
14. Chen K., Roberts E., Luthey-Schulten Z. Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4. BMC Evol. Biol. 2009, 9:179.
15. Chiari Y., Cahais V., Galtier N., Delsuc F. Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biol. 2012, 10:65.
16. Ciccarelli F.D., Doerks T., von Mering C., Creevey C.J., Snel B., Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science 2006, 311:1283-1287.
17. Cohen O., Gophna U., Pupko T. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol. Biol. Evol. 2011, 28:1481-1489.
18. Davalos L.M., Perkins S.L. Saturation and base composition bias explain phylogenomic conflict in Plasmodium. Genomics 2008, 91:433-442.
19. Delsuc F., Brinkmann H., Philippe H. Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 2005, 6:361-375.
20. DeLuca T.F., Cui J., Jung J.Y., St Gabriel K.C., Wall D.P. Roundup 2.0: enabling comparative genomics for over 1800 genomes. Bioinformatics 2012, 28:715-716.
21. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004, 32:1792-1797.
22. Embley T.M., van der Giezen M., Horner D.S., Dyal P.L., Bell S., Foster P.G. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 2003, 55:387-395.
23. Emerson D., Rentz J.A., Lilburn T.G., Davis R.E., Aldrich H., Chan C., Moyer C.L. A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PloS One 2007, 2:e667.
24. Felsenstein J. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 1978, 27:401-410.
25. Felsenstein, J., 2004. Inferring phylogenies. Sunderland, Massachusetts.
26. Galtier N., Gouy M. Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis. Mol. Biol. Evol. 1998, 15:871-879.
27. Giovannoni S.J., Tripp H.J., Givan S., Podar M., Vergin K.L., Baptista D., Bibbs L., Eads J., Richardson T.H., Noordewier M., Rappe M.S., Short J.M., Carrington J.C., Mathur E.J. Genome streamlining in a cosmopolitan oceanic bacterium. Science 2005, 309:1242-1245.
28. Gribaldo S., Brochier C. Phylogeny of prokaryotes: does it exist and why should we care?. Res. Microbiol. 2009, 160:513-521.
29. Gribaldo S., Philippe H. Ancient phylogenetic relationships. Theor. Popul. Biol. 2002, 61:391-408.
30. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
31. Gupta R.S. The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol. Rev. 2000, 24:367-402.
32. Hesselmann R.P., Werlen C., Hahn D., van der Meer J.R., Zehnder A.J. Enrichment, phylogenetic analysis and detection of a bacterium that performs enhanced biological phosphate removal in activated sludge. Syst. Appl. Microbiol. 1999, 22:454-465.
33. Husnik F., Chrudimsky T., Hypsa V. Multiple origins of endosymbiosis within the Enterobacteriaceae (gamma-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 2011, 9:87.
34. Jain R., Rivera M.C., Lake J.A. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl. Acad. Sci. USA 1999, 96:3801-3806.
35. Ji, B., Zhang, S.D., Arnoux, P., Rouy, Z., Alberto, F., Philippe, N., Murat, D., Zhang, W.J., Rioux, J.B., Ginet, N., Sabaty, M., Mangenot, S., Pradel, N., Tian, J., Yang, J., Zhang, L., Zhang, W., Pan, H., Henrissat, B., Coutinho, P.M., Li, Y., Xiao, T., Medigue, C., Barbe, V., Pignol, D., Talla, E., Wu, L.F., 2013. Comparative genomic analysis provides insights into the evolution and niche adaptation of marine Magnetospira sp. QH-2 strain. Environ. Microbiol.
36. Jobb G., von Haeseler A., Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol. 2004, 4:18.
37. Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Briefings Bioinform. 2008, 9:286-298.
38. Kelly D.P., Wood A.P. Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int. J. Syst. Evol. Microbiol. 2000, 50:489-500.
39. Kelly, S., Wickstead, B., Gull, K., 2010. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. In: Proceedings. Biological Sciences/The Royal Society.
40. Kersters K., Devos P., Gillis M., Swings J., Vandamme P., Stackebrandt E. Introduction to the proteobacteria. In the Prokaryotes: A Handbook on the Biology of Bacteria 2006, 3-37. Springer, New York. M. Dworkin, S. Falkow, E. Rosenberg, K.H. Schleifer, E. Stackebrandt (Eds.).
41. Kuzniar A., van Ham R.C., Pongor S., Leunissen J.A. The quest for orthologs: finding the corresponding gene across genomes. Trends Gen.: TIG 2008, 24:539-551.
42. Lang B.F., Gray M.W., Burger G. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 1999, 33:351-397.
43. Lang J.M., Darling A.E., Eisen J.A. Phylogeny of bacterial and archaeal genomes using conserved genes: supertrees and supermatrices. PloS One 2013, 8:e62510.
44. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
45. Lartillot N., Brinkmann H., Philippe H. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol. Biol. 2007, 7(Suppl. 1):S4.
46. Lartillot N., Lepage T., Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 2009, 25:2286-2288.
47. Lartillot N., Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 2004, 21:1095-1109.
48. Le S.Q., Gascuel O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 2008, 25:1307-1320.
49. Lee K.B., Liu C.T., Anzai Y., Kim H., Aono T., Oyaizu H. The hierarchical system of the 'Alphaproteobacteria': description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. Int. J. Syst. Evol. Microbiol. 2005, 55:1907-1919.
50. Lefevre C.T., Bernadac A., Yu-Zhang K., Pradel N., Wu L.F. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ. Microbiol. 2009, 11:1646-1657.
51. Leigh J.W., Schliep K., Lopez P., Bapteste E. Let them fall where they may: congruence analysis in massive phylogenetically messy data sets. Mol. Biol. Evol. 2011, 28:2773-2785.
52. Lerat E., Daubin V., Moran N.A. From gene trees to organismal phylogeny in prokaryotes: the case of the gamma-Proteobacteria. PLoS Biol. 2003, 1:E19.
53. Lopez-Garcia P., Moreira D. Tracking microbial biodiversity through molecular and genomic ecology. Res. Microbiol. 2008, 159:67-73.
54. Maki Y., Yoshida H., Wada A. Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells 2000, 5:965-974.
55. Marthey S., Aguileta G., Rodolphe F., Gendrault A., Giraud T., Fournier E., Lopez-Villavicencio M., Gautier A., Lebrun M.H., Chiapello H. FUNYBASE: a FUNgal phYlogenomic dataBASE. BMC Bioinform. 2008, 9:456.
56. Matte-Tailliez O., Brochier C., Forterre P., Philippe H. Archaeal phylogeny based on ribosomal proteins. Mol. Biol. Evol. 2002, 19:631-639.
57. McCutcheon J.P., McDonald B.R., Moran N.A. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Gen. 2009, 5:e1000565.
58. Miller W.G., Parker C.T., Rubenfield M., Mendz G.L., Wosten M.M., Ussery D.W., Stolz J.F., Binnewies T.T., Hallin P.F., Wang G., Malek J.A., Rogosin A., Stanker L.H., Mandrell R.E. The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PloS One 2007, 2:e1358.
59. Moran N.A., McCutcheon J.P., Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 2008, 42:165-190.
60. Morris R.M., Rappe M.S., Connon S.A., Vergin K.L., Siebold W.A., Carlson C.A., Giovannoni S.J. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 2002, 420:806-810.
61. Nakabachi A., Yamashita A., Toh H., Ishikawa H., Dunbar H.E., Moran N.A., Hattori M. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 2006, 314:267.
62. Philippe H. MUST, a computer package of management utilities for sequences and trees. Nucl. Acids Res. 1993, 21:5264-5272.
63. Philippe H., Douady C.J. Horizontal gene transfer and phylogenetics. Curr. Opin. Microbiol. 2003, 6:498-505.
64. Philippe H., Forterre P. The rooting of the universal tree of life is not reliable. J. Mol. Evol. 1999, 49:509-523.
65. Philippe H., Laurent J. How good are deep phylogenetic trees?. Curr. Opin. Gen. Develop. 1998, 8:616-623.
66. Philippe H., Sörhannus U., Baroin A., Perasso R., Gasse F., Adoutte A. Comparison of molecular and paleontological data in diatoms suggests a major gap in the fossil record. J. Evol. Biol. 1994, 7:247-265.
67. Puigbo P., Wolf Y.I., Koonin E.V. The tree and net components of prokaryote evolution. Gen. Biol. Evol. 2010, 2:745-756.
68. Rappe M.S., Connon S.A., Vergin K.L., Giovannoni S.J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 2002, 418:630-633.
69. Rodriguez-Ezpeleta N., Embley T.M. The SAR11 group of alpha-proteobacteria is not related to the origin of mitochondria. PloS One 2012, 7:e30520.
70. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 2002, 51:492-508.
71. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
72. Spring S., Lins U., Amann R., Schleifer K.H., Ferreira L.C., Esquivel D.M., Farina M. Phylogenetic affiliation and ultrastructure of uncultured magnetic bacteria with unusually large magnetosomes. Arch. Microbiol. 1998, 169:136-147.
73. Stackebrandt E., Murray R.G.E., Trüper H.G. Proteobacteria classis nov., a name for the phylogenetic taxon that includes the "purple bacteria and their relatives". Int. J. Syst. Bacteriol. 1988, 38:321-325.
74. Steindler L., Schwalbach M.S., Smith D.P., Chan F., Giovannoni S.J. Energy starved Candidatus Pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PloS One 2011, 6:e19725.
75. Suarez S., Ferroni A., Lotz A., Jolley K.A., Guérin P., Leto J., Dauphin B., Jamet A., Maiden M.C., Nassif X., Armengaud J. Ribosomal proteins as biomarkers for bacterial identification by mass spectrometry in the clinical microbiology laboratory. J. Microbiol. Meth. 2013, 94:390-396.
76. Swithers K.S., Gogarten J.P., Fournier G.P. Trees in the web of life. J. Biol. 2009, 8:54.
77. Tamames J., Gil R., Latorre A., Pereto J., Silva F.J., Moya A. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol. Biol. 2007, 7:181.
78. Tamura H., Hotta Y., Sato H. Novel accurate bacterial discrimination by MALDI-time-of-flight MS based on ribosomal proteins coding in S10-spc-alpha operon at strain level S10-GERMS. J. Am. Soc. Mass Spectrom. 2013, 24:1185-1193.
79. Tettelin H., Masignani V., Cieslewicz M.J., Donati C., Medini D., Ward N.L., Angiuoli S.V., Crabtree J., Jones A.L., Durkin A.S., Deboy R.T., Davidsen T.M., Mora M., Scarselli M., Margarit Ros I., Peterson J.D., Hauser C.R., Sundaram J.P., Nelson W.C., Madupu R., Brinkac L.M., Dodson R.J., Rosovitz M.J., Sullivan S.A., Daugherty S.C., Haft D.H., Selengut J., Gwinn M.L., Zhou L., Zafar N., Khouri H., Radune D., Dimitrov G., Watkins K., O'Connor K.J., Smith S., Utterback T.R., White O., Rubens C.E., Grandi G., Madoff L.C., Kasper D.L., Telford J.L., Wessels M.R., Rappuoli R., Fraser C.M. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. USA 2005, 102:13950-13955.
80. Thrash J.C., Boyd A., Huggett M.J., Grote J., Carini P., Yoder R.J., Robbertse B., Spatafora J.W., Rappe M.S., Giovannoni S.J. Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Scientific Reports 2011, 1:13.
81. Touchon M., Hoede C., Tenaillon O., Barbe V., Baeriswyl S., Bidet P., Bingen E., Bonacorsi S., Bouchier C., Bouvet O., Calteau A., Chiapello H., Clermont O., Cruveiller S., Danchin A., Diard M., Dossat C., Karoui M.E., Frapy E., Garry L., Ghigo J.M., Gilles A.M., Johnson J., Le Bouguenec C., Lescat M., Mangenot S., Martinez-Jehanne V., Matic I., Nassif X., Oztas S., Petit M.A., Pichon C., Rouy Z., Ruf C.S., Schneider D., Tourret J., Vacherie B., Vallenet D., Medigue C., Rocha E.P., Denamur E. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Gen. 2009, 5:e1000344.
82. Van Leuven J.T., McCutcheon J.P. An AT mutational bias in the tiny GC-rich endosymbiont genome of Hodgkinia. Gen. Biol. Evol. 2012, 4:24-27.
83. Viklund J., Ettema T.J., Andersson S.G. Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade. Mol. Biol. Evol. 2011.
84. Wang Z., Wu M. A phylum-level bacterial phylogenetic marker database. Mol. Biol. Evol. 2013, 30:1258-1262.
85. Williams K.P., Gillespie J.J., Sobral B.W., Nordberg E.K., Snyder E.E., Shallom J.M., Dickerman A.W. Phylogeny of gammaproteobacteria. J. Bacteriol. 2010, 192:2305-2314.
86. Williams K.P., Sobral B.W., Dickerman A.W. A robust species tree for the alphaproteobacteria. J. Bacteriol. 2007, 189:4578-4586.
87. Woese C.R., Fox G.E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA 1977, 74:5088-5090.
88. Wu D., Jospin G., Eisen J.A. Systematic identification of gene families for use as "markers" for phylogenetic and phylogeny-driven ecological studies of bacteria and archaea and their major subgroups. PloS One 2013, 8:e77033.
89. Yang Z. Computational Molecular Evolution 2006, Oxford University Press, Oxford, England.
90. Yang Z., Roberts D. On the use of nucleic acid sequences to infer early branchings in the tree of life. Mol. Biol. Evol. 1995, 12:451-458.
91. Yutin N., Puigbò P., Koonin E.V., Wolf Y.I. Phylogenomics of Prokaryotic Ribosomal Proteins. PloS One 2012, 7:e36972.