Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of rhizobium etli

Applied and Environmental Microbiology

Volumn 76, Issue 5, 2010, Pages 1604-1614

  González, Víctor ^a   Acosta, José L ^a   Santamaría, Rosa I ^a   Fernández, Patricia Bustos José L ^a   Hernández González, Ismael L ^a   Díaz, Rafael ^a   Flores, Margarita ^a   Palacios, Rafael ^a   Mora, Jaime ^a   Dávila, Guillermo ^a  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL SPECIES; CHROMOSOMAL SEQUENCES; COMPLETE GENOMES; GENOME SEQUENCES; GENOMIC SEQUENCE; GEOGRAPHICAL ORIGINS; LARGE PLASMIDS; MOBILE ELEMENTS; PLASMID DNA; RHIZOBIUM ETLI; SECONDARY METABOLISM;

AMINO ACIDS; DNA; GENES; METABOLISM; MICROBIOLOGY; ORGANIC ACIDS; SUGAR (SUCROSE);

DNA SEQUENCES;

BACTERIAL DNA;

CHROMOSOME; GENOMICS; GEOGRAPHICAL DISTRIBUTION; NITRIFYING BACTERIUM; PLASMID; SYMBIOSIS;

ARTICLE; BACTERIAL GENOME; CHEMISTRY; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; GENETICS; GENOMIC ISLAND; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLASMID; RHIZOBIUM ETLI; SEQUENCE HOMOLOGY;

CLUSTER ANALYSIS; CONSERVED SEQUENCE; DNA, BACTERIAL; GENOME, BACTERIAL; GENOMIC ISLANDS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; RHIZOBIUM ETLI; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID;

BACTERIA (MICROORGANISMS); RHIZOBIUM ETLI;

EID: 77649204739     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02039-09     Document Type: Article

References (59)

1. Abby, S., and V. Daubin. 2007. Comparative genomics and the evolution of prokaryotes. Trends Microbiol. 15: 135-141.
2. Andersson, S. G., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. Alsmark, R. M. Podowski, A. K. Naslund, A. S. Eriksson, H. H. Winkler, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133-140.
3. Bentley, S. 2009. Sequencing the species pan-genome. Nat. Rev. Microbiol. 7: 258-259.
4. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
5. Bergthorsson, U., and H. Ochman. 1995. Heterogeneity of genome sizes among natural isolates of Escherichia coli. J. Bacteriol. 177: 5784-5789.
6. Buell, C. R., V. Joardar, M. Lindeberg, J. Selengut, I. T. Paulsen, M. L. Gwinn, R. J. Dodson, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, S. Daugherty, L. Brinkac, M. J. Beanan, D. H. Haft, W. C. Nelson, T. Davidsen, N. Zafar, L. Zhou, J. Liu, Q. Yuan, H. Khouri, N. Fedorova, B. Tran, D. Russell, K. Berry, T. Utterback, S. E. Van Aken, T. V. Feldblyum, M. D'Ascenzo, W. L. Deng, A. R. Ramos, J. R. Alfano, S. Cartinhour, A. K. Chatterjee, T. P. Delaney, S. G. Lazarowitz, G. B. Martin, D. J. Schneider, X. Tang, C. L. Bender, O. White, C. M. Fraser, and A. Collmer. 2003. The complete genome sequence of Arabidopsis and the tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U. S. A. 100: 10181-10186.
7. Campbell, A. 1981. Evolutionary significance of accessory DNA elements in bacteria. Annu. Rev. Microbiol. 35: 55-83.
8. Carlson, R. W., B. Reuhs, T. B. Chen, U. R. Bhat, and K. D. Noel. 1995. Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen. J. Biol. Chem. 270:11783-11788.
9. Crossman, L. C., S. Castillo-Ramírez, C. McAnnula, L. Lozano, G. S. Vernikos, J. L. Acosta, Z. F. Ghazoui, I. Hernández-González, G. Meakin, A. W. Walker, M. F. Hynes, J. P. Young, J. A. Downie, D. Romero, A. W. Johnston, G. Dávila, J. Parkhill, and V. González. 2008. A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria. PLoS One 3: e2567.
10. Deicher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27: 4636-4641.
11. Deicher, A. L., A. Phillippy, J. Carlton, and S. L. Salzberg. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30: 2478-2483.
12. Delcher, A. L., S. L. Salzberg, and A. M. Phillippy. 2003. Using MUMmer to identify similar regions in large sequence sets. Chapter 10, unit 10.3. Curr. Protoc. Bioinformatics 2003:10.3.1-10.3.18. doi:10.1002/0471250953. bil003s00.
13. Duelli, D. M., A. Tobin, J. M. Box, V. S. Kolli, R. W. Carlson, and K. D. Noel. 2001. Genetic locus required for antigenic maturation of Rhizobium etli CE3 lipopolysaccharide. J. Bacteriol. 183: 6054-6064.
14. Enright, A. J., S. Van Dongen, and C. A. Ouzounis. 2002. An efficient algoridim for large-scale detection of protein families. Nucleic Acids Res. 30: 1575-1584.
15. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186-194.
16. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175-185.
17. Feil, E. J., B. C. Li, D. M. Aanensen, W. P. Hanage, and B. G. Spratt 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186: 1518-1530.
18. Flores, M., L. Morales, A. Avila, V. González, P. Bustos, D. García, Y. Mora, X. Guo, J. Collado-Vides, D. Pinero, G. Dávila, J. Mora, and R. Palacios. 2005. Diversification of DNA sequences in the symbiotic genome oí Rhizobium etli. J. Bacteriol. 187: 7185-7192.
19. Fraser, C. M., and R. D. Fleischmann. 1997. Strategies for whole microbial genome sequencing and analysis. Electrophoresis 18: 1207-1216. (Pubitemid 27371429)
20. Giuntini, E., A. Mengoni, C. De Filippo, D. Cavalieri, N. Aubin-Horth, C. R. Landry, A. Becker, and M. Bazzicalupo. 2005. Large-scale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains. BMC Genomics 6: 158.
21. González, V., P. Bustos, M. A. Ramírez-Romero, A. Medrano-Soto, H. Salgado, I. Hernández-González, J. C. Hernández-Celis, V. Quintero, G. Moreno-Hagelsieb, L. Girard, O. Rodríguez, M. Flores, M. A. Cevallos, J. Collado-Vides, D. Romero, and G. Dávila. 2003. The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments. Genome Biol. 4:R36.
22. González, V., L. Lozano, S. Castillo-Ramírez, I. Hernández-González, P. Bustos, R. I. Santamaría, J. L. Fernández, J. L. Acosta, and G. Dávila. 2008. Evolutionary genomics of the nitrogen-fixing symbiotic bacteria, p. 183-198. In P. Dion and C. S. Nautiyal (ed.), Molecular mechanisms of plant and microbe coexistence, vol.15. Springer, Heidelberg, Germany.
23. González, V., R. I. Santamaría, P. Bustos, I. Hernández-González, A. Medrano-Soto, G. Moreno-Hagelsieb, S. C. Jangá, M. A. Ramírez, V. JiménezJacinto, J. Collado-Vides, and G. Dávila. 2006. The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicóos. Proc. Natl. Acad. Sci. U. S. A. 103: 3834-3839.
24. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8: 195-202. (Pubitemid 28177231)
25. Guerrero, G., H. Peralta, A. Aguilar, R. Diaz, M. A. Villalobos, A. MedranoSoto, and J. Mora. 2005. Evolutionary, structural and functional relationships revealed by comparative analysis of syntenic genes in Rhizobiales. BMC Evol. Biol. 5: 55.
26. Guo, H., S. Sun, B. Eardly, T. Finan, and J. Xu. 2009. Genome variation in the symbiotic nitrogen-fixing bacterium Sinorhizobium meliloti. Genome 52: 862-875.
27. Hiller, N. L., B. Janto, J. S. Hogg, R. Boissy, S. Yu, E. Powell, R. Keefe, N. E. Ehrlich, K. Shen, J. Hayes, K. Barbadora, W. Klimke, D. Dernovoy, T. Tatusova, J. Parkhill, S. D. Bentley, J. C. Post, G. D. Ehrlich, and F. Z. Hu. 2007. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J. Bacteriol. 189: 8186-8195.
28. Hogg, J. S., F. Z. Hu, B. Janto, R. Boissy, J. Hayes, R. Keefe, J. C. Post, and G. D. Ehrlich. 2007. Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains. Genome Biol. 8: R103.
29. Itakura, M., K. Saeki, H. Omori, T. Yokoyama, T. Kaneko, S. Tabata, T. Ohwada, S. Tajima, T. Uchiumi, K. Honnma, K. Fujita, H. Iwata, Y. Saeki, Y. Hara, S. Ikeda, S. Eda, H. Mitsui, and K. Minamisawa. 2009. Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. ISME J. 3: 326-339.
30. Johnston, A. W. B., J. L. Beynon, A. V. Buchanan-Wollaston, S. M. Setchell, P. R. Hirsh, and J. E. Beringer. 1978. High frequency transfer of nodulating ability between strains and species oí Rhizobium. Nature 276: 634-636.
31. Jumas-Bilak, E., S. Michaux-Charachon, G. Bourg, M. Ramuz, and A. Allardet-Servent. 1998. Unconventional genomic organization in the alpha subgroup of me Proteobacteria. J. Bacteriol. 180: 2749-2755. (Pubitemid 28213277)
32. Konstantinidis, K. T., and J. M. Tiedje. 2004. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc. Natl. Acad. Sci. U. S. A. 101: 3160-3165.
33. Lander, E. S., and M. S. Waterman. 1988. Genomic mapping by fingerprinting random clones: a mathematical analysis. Genomics 2: 231-239.
34. Legault, B. A., A. Lopez-Lopez, J. C. Alba-Casado, W. F. Doolittle, H. Bolhuis, F. Rodriguez-Valera, and R. T. Papke. 2006. Environmental genomics of "Haloquadratum walsbyi" in a saltern ciystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 7: 171.
35. Li, L., C. J. Stoeckert, Jr., and D. S. Roos. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178-2189. (Pubitemid 37161775)
36. Masson-Boivin, C., E. Giraud, X. Perret, and J. Batut. 2009. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol. 17: 458-466.
37. Medini, D., C. Donati, H. Tettelin, V. Masignani, and R. Rappuoli. 2005. The microbial pan-genome. Curr. Opin. Genet. Dev. 15: 589-594.
38. Palacios, R., M. Flores, S. Brom, E. Martínez, V. González, S. Frenk, C. Quinto, M. A. Cevallos, L. Girard, D. Romero, A. Garciarrubio, D. Pinero, and G. Dávila. 1986. Organization of the Rhizobium phaseoli genome, p. 151-156. In D. P. S. Verma and N. Brisson (ed.), Molecular genetics of plant-microbe interactions. Martinus Nijhoff Publishers Organization, Dordrecht, the Netherlands.
39. Pallen, M. J., and B. W. Wren. 2007. Bacterial pattiogenomics. Nature 449: 835-842.
40. Paulsen, I. T., R. Seshadri, K. E. Nelson, J. A. Eisen, J. F. Heidelberg, T. D. Read, R. J. Dodson, L. Umayam, L. M. Brinkac, M. J. Beanan, S. C. Daugherty, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, W. C. Nelson, B. Ayodeji, M. Kraul, J. Shetty, J. Malek, S. E. Van Aken, S. Riedmuller, H Tettelin, S. R. Gill, O. White, S. L. Salzberg, D. L. Hoover, L. E. Lindler, S. M. Hailing, S. M. Boyle, and C. M. Fraser. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant padiogens and symbionts. Proc. Natl. Acad. Sci. U. S. A. 99: 13148-13153.
41. Piñero, D., E. Martinez, and R. K. Selander. 1988. Genetic diversity and relationships among isolates of Rhizobium leguminosarum biovar phaseoli. Appl. Environ. Microbiol. 54: 2825-2832.
42. Rasko, D. A., M. J. Rosovitz, G. S. Myers, E. F. Mongodin, W. F. Fricke, P. Gajer, J. Crabtree, M. Sebaihia, N. R. Thomson, R. Chaudhuri, I. R. Henderson, V. Sperandio, and J. Ravel. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190: 6881-6893.
43. Reanney, D. 1976. Extrachromosomal elements as possible agents of adaptation and development. Bacteriol. Rev. 40: 552-590.
44. Salzberg, S. L., A. L. Delcher, S. Kasif, and O. White. 1998. Microbial gene identification using interpolated Markov models. Nucleic Acids Res. 26: 544-548.
45. a.Shinegobu, S., H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
46. Silva, C., P. Vinuesa, L. E. Eguiarte, V. Souza, and E. Martinez-Romero. 2005. Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. MoI. Ecol. 14: 4033-4050.
47. Slater, S. C., B. S. Goldman, B. Goodner, J. C. Setubal, S. K. Farrand, E. W. Nester, T. J. Burr, L. Banta, A. W. Dickerman, I. Paulsen, L. Otten, G. Suen, R. Welch, N. F. Almeida, F. Arnold, O. T. Burton, Z. Du, A. Ewing, E. Godsy, S. Heisel, K. L. Houmiel, J. Jhaveri, J. Lu, N. M. Miller, S. Norton, Q. Chen, W. Phoolcharoen, V. Ohlin, D. Ondrusek, N. Pride, S. L. Stricklin, J. Sun, C. Wheeler, L. Wilson, H. Zhu, and D. W. Wood. 2009. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J. Bacteriol. 191: 2501-2511.
48. Smith, T. F., and M. S. Waterman. 1981. Identification of common molecular subsequences. J. Mol. Biol. 147: 195-197.
49. Snel, B., M. A. Huynen, and B. E. Dutilh. 2005. Genome trees and the nature of genome evolution. Annu. Rev. Microbiol. 59: 191-209.
50. Sobral, B. W., R. J. Honeycutt, and A. G. Atherly. 1991. The genomes of the family Rhizobiaceae: size, stability, and rarely cutting restriction endonucleases. J. Bacteriol. 173: 704-709.
51. Spratt, B. G., W. P. Hanage, B. Li, D. M. Aanensen, and E. J. Feil. 2004. Displaying the relatedness among isolates of bacterial species-the eBURST approach. FEMS Microbiol. Lett. 241: 129-134.
52. Tamames, J. 2001. Evolution of gene order conservation in prokaryotes. Genome Biol. 2: RESEARCH0020.
53. Tettelin, H., V. Masignani, M. J. Cieslewicz, C. Donati, D. Medini, N. L. Ward, S. V. Angiuoli, J. Crabtree, A. L, Jones, A. S. Durkin, R. T. Deboy, T. M. Davidsen, M. Mora, M. Scarselli, I. Margarit y Ros, J. D. Peterson, C. R. Hauser, J. P. Sundaram, W. C. Nelson, R. Madupu, L. M. Brinkac, R. J. Dodson, M. J. Rosovitz, S. A. Sullivan, S. C. Daugherty, D. H. Haft, J. Selengut, M. L. Gwinn, L. Zhou, N. Zafar, H. Khouri, D. Radune, G. Dimitrov, K. Watkins, K. J. O'Connor, S. Smith, T. R. Utterback, O. White, C. E. Rubens, G. Grandi, L. C. Madoff, D. L. Kasper, J. L. Telford, M. R. Wessels, R. Rappuoli, and C. M. Fraser. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome." Proc. Natl. Acad. Sci. U. S. A. 102: 13950-13955.
54. Tettelin, H., V. Masignani, M. J. Cieslewicz, J. A. Eisen, S. Peterson, M. R. Wessels, I. T. Paulsen, K. E. Nelson, I. Margarit, T. D. Read, L. C. Madoff, A. M. Wolf, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. T. DeBoy, A. S. Durkin, J. F. Kolonay, R. Madupu, M. R. Lewis, D. Radune, N. B. Fedorova, D. Scanlan, H. Khouri, S. Mulligan, H. A. Carty, R. T. Cline, S. E. Van Aken, J. Gill, M. Scarselli, M. Mora, E. T. Iacobini, C. Brettoni, G. Galli, M. Mariáni, F. Vegni, D. Maione, D. Rinaudo, R. Rappuoli, J. L. Telford, D. L. Kasper, G. Grandi, and C. M. Fraser. 2002. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc. Natl. Acad. Sci. U. S. A. 99: 12391-12396.
55. Tettelin, H., D. Riley, C. Cattuto, and D. Medini. 2008. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11: 472-477.
56. Vernikos, G. S., and J. Parkhill. 2006. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196-2203.
57. Welch, R. A., V. Burland, G. Plunkett III, P. Redford, P. Roesch, D. Rasko, E. L. Buckles, S. R. Liou, A. Boutin, J. Hackett, D. Stroud, G. F. Mayhew, D. J. Rose, S. Zhou, D. C. Schwartz, N. T. Perna, H. L. Mobley, M. S. Donnenberg, and F. R. Blattner. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99: 17020-17024.
58. Wolf, Y. I., I. B. Rogozin, N. V. Grishin, R. L. Tatusov, and E. V. Koonin. 2001. Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol. Biol. 1: 8.
59. Young, J. P., L. C. Crossman, A. W. Johnston, N. R. Thomson, Z. F. Ghazoui, K. H. Hull, M. Wexler, A. R. Curson, J. D. Todd, P. S. Poole, T. H. Mauchline, A. K. East, M. A. Quail, C. Churcher, C. Arrowsmith, I. Cherevach, T. Chillingworth, K. Clarke, A. Cronin, P. Davis, A. Fraser, Z. Hance, H. Hauser, K. Jagels, S. Moule, K. Mungall, H. Norbertczak, E. Rabbinowitsch, M. Sanders, M. Simmonds, S. Whitehead, and J. Parkhill. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7: R34.