Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies

Genome Biology

Volumn 14, Issue 2, 2013, Pages

  Sugawara, Masayuki ^a   Epstein, Brendan ^a   Badgley, Brian D ^a   Unno, Tatsuya ^a   Xu, Lei ^a   Reese, Jennifer ^a   Gyaneshwar, Prasad ^b   Denny, Roxanne ^a   Mudge, Joann ^c   Bharti, Arvind K ^c   Farmer, Andrew D ^c   May, Gregory D ^c   Woodward, Jimmy E ^c   Médigue, Claudine ^d   Vallenet, David ^d   Lajus, Aurélie ^d   Rouy, Zoé ^d   Martinez Vaz, Betsy ^e   Tiffin, Peter ^a   Young, Nevin D ^a   Sadowsky, Michael J ^a   more..

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^c NATIONAL CENTER FOR GENOME RESOURCES   (United States)

^d UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^e HAMLINE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ORGANOSULFUR DERIVATIVE; POLYSACCHARIDE; LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CONJUGATION; CONTROLLED STUDY; DENITRIFICATION; GENETIC VARIABILITY; GENOMICS; GENUS; HEME SYNTHESIS; HOST; LEGUME; MEDICAGO; MUTATIONAL ANALYSIS; NITROGEN FIXATION; NODULATION; NONHUMAN; PHENOTYPE; SINORHIZOBIUM; SINORHIZOBIUM MEDICAE; SINORHIZOBIUM MELILOTI; SPECIES; SYMBIOSIS; TAXONOMY; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; BACTERIAL SECRETION SYSTEM; BIOSYNTHESIS; CLASSIFICATION; GENETICS; PHYLOGENY;

BACTERIAL SECRETION SYSTEMS; GENOME, BACTERIAL; LIPOPOLYSACCHARIDES; NITROGEN FIXATION; PHYLOGENY; SINORHIZOBIUM; SYMBIOSIS;

EID: 84873965566     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-2-r17     Document Type: Article

References (58)

1. Bohlool BB, Ladha JK, Garrity DP, George T: Biological Nitrogen-Fixation for Sustainable Agriculture -a Perspective. Plant Soil 1992, 141:1-11.
2. Martínez-Romero E, Caballero-Mellado J: Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 1996, 15:113-140.
3. Young JPW, Haukka KE: Diversity and phylogeny of rhizobia. New Phytol 1996, 133:87-94.
4. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de Los Santos P, Gross E, Dos Reis FB, Sprent JI, Young JP, James EK: Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant-Microbe Interact 2011, 24:1276-1288.
5. Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC: Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Bacteriol 1996, 46:972-980.
6. de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, Dreyfus B, Kersters K, Gillis M: Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 1994, 44:715-733.
7. Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, et al: The composite genome of the legume symbiont Sinorhizobium meliloti. Science 2001, 293:668-672.
8. Reeve W, Chain P, O'Hara G, Ardley J, Nandesena K, Brau L, Tiwari R, Malfatti S, Kiss H, Lapidus A, Copeland A, Nolan M, Land M, Hauser L, Chang Y-J, Mavromatis K, Markowitz V, Kyrpides NC, Gollagher M, Yates R, Dilworth M, Howieson J: Complete genome sequence of the Medicago microsymbiont Ensifer (Sinorhizobium) medicae strain WSM419. Stand Genomic Sci 2010, 2:77-86.
9. Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quere A, Wollherr A, Heinemeyer I, Morgenstern B, Pommerening-Roser A, Flores M, Palacios R, Brenner S, Gottschalk G, Schmitz RA, Broughton WJ, Perret X, Strittmatter AW, Streit WR: Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 2009, 75:4035-4045.
10. Galardini M, Mengoni A, Brilli M, Pini F, Fioravanti A, Lucas S, Lapidus A, Cheng JF, Goodwin L, Pitluck S, Land M, Hauser L, Woyke T, Mikhailova N, Ivanova N, Daligault H, Bruce D, Detter C, Tapia R, Han C, Teshima H, Mocali S, Bazzicalupo M, Biondi EG: Exploring the symbiotic pangenome of the nitrogen-fixing bacterium Sinorhizobium meliloti. BMC Genomics 2011, 12:235.
11. Weidner S, Becker A, Bonilla I, Jaenicke S, Lloret J, Margaret I, Puhler A, Ruiz-Sainz JE, Schneiker-Bekel S, Szczepanowski R, Vinardell JM, Zehner S, Göttfert M: Genome sequence of the soybean symbiont Sinorhizobium fredii HH103. J Bacteriol 2012, 194:1617-1618.
12. Tian CF, Zhou YJ, Zhang YM, Li QQ, Zhang YZ, Li DF, Wang S, Wang J, Gilbert LB, Li YR, Chen WX: Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci USA 2012, 109:8629-8634.
13. Bailly X, Giuntini E, Sexton MC, Lower RP, Harrison PW, Kumar N, Young JP: Population genomics of Sinorhizobium medicae based on low-coverage sequencing of sympatric isolates. ISME J 2011, 5:1722-1734.
14. Denarie J, Cullimore J: Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell 1993, 74:951-954.
15. Leigh JA, Walker GC: Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet 1994, 10:63-67.
16. Breedveld MW, Miller KJ:: Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev 1994, 58:145-161.
17. Fauvart M, Michiels J: Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 2008, 285:1-9.
18. MacLean AM, Finan TM, Sadowsky MJ: Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 2007, 144:615-622.
19. Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D, Carrere S, Cruveiller S, Dossat C, Lajus A, Marchetti M, Poinsot V, Rouy Z, Servin B, Saad M, Schenowitz C, Barbe V, Batut J, Médigue C, Masson-Boivin C: Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 2008, 18:1472-1483.
20. Epstein B, Branca A, Mudge J, Bharti AK, Briskine R, Farmer AD, Sugawara M, Young ND, Sadowsky MJ, Tiffin P: Population genomics of the facultatively mutualistic bacteria Sinorhizobium meliloti and S. medicae. PLoS Genet 2012, 8:e1002868.
21. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD, Mudge J, Bharti AK, Woodward JE, May GD, Gentzbittel L, Ben C, Denny R, Sadowsky MJ, Ronfort J, Bataillon T, Young ND, Tiffin P: Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci USA 2011, 108:E864-870.
22. Young ND, Debellé F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, Mudge J, Bharti AK, Murray JD, Naoumkina MA, Rosen B, Silverstein KA, Tang H, Rombauts S, Zhao PX, Zhou P, et al: The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480:520-524.
23. Sugawara M, Shah GR, Sadowsky MJ, Paliy O, Speck J, Vail AW, Gyaneshwar P: Expression and functional roles of Bradyrhizobium japonicum genes involved in the utilization of inorganic and organic sulfur compounds in free-living and symbiotic conditions. Mol Plant-Microbe Interact 2011, 24:451-457.
24. Autry AR, Fitzgerald JW: Sulfonate-S -a major form of forest soil organic sulfur. Biol Fert Soils 1990, 10:50-56.
25. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M: Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 2007, 316:1307-1312.
26. Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJ: A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 1991, 354:125-130.
27. Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, Chun JY, Forsberg LS, Carlson R: nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J Bacteriol 1994, 176:620-633.
28. Lewin A, Cervantes E, Chee-Hoong W, Broughton WJ: nodSU, two new nod genes of the broad host range Rhizobium strain NGR234 encode host-specific nodulation of the tropical tree Leucaena leucocephala. Mol Plant-Microbe Interact 1990, 3:317-326.
29. Jabbouri S, Relic B, Hanin M, Kamalaprija P, Burger U, Prome D, Prome JC, Broughton WJ: nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. J Biol Chem 1998, 273:12047-12055.
30. Lorquin J, Lortet G, Ferro M, Mear N, Dreyfus B, Prome JC, Boivin C: Nod factors from Sinorhizobium saheli and S. teranga bv. sesbaniae are both arabinosylated and fucosylated, a structural feature specific to Sesbania rostrata symbionts. Mol Plant-Microbe Interact 1997, 10:879-890.
31. Chen H, Gao K, Kondorosi E, Kondorosi A, Rolfe BG: Functional genomic analysis of global regulator NolR in Sinorhizobium meliloti. Mol Plant-Microbe Interact 2005, 18:1340-1352.
32. Cren M, Kondorosi A, Kondorosi E: An insertional point mutation inactivates NolR repressor in Rhizobium meliloti 1021. J Bacteriol 1994, 176:518-519.
33. Tseng TT, Tyler BM, Setubal JC: Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 2009, 9(Suppl 1):S2.
34. Lopez-Baena FJ, Vinardell JM, Perez-Montano F, Crespo-Rivas JC, Bellogin RA, Espuny Mdel R, Ollero FJ: Regulation and symbiotic significance of nodulation outer proteins secretion in Sinorhizobium fredii HH103. Microbiol 2008, 154:1825-1836.
35. Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X: Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 1998, 28:1381-1389.
36. Cascales E, Christie PJ: The versatile bacterial type IV secretion systems. Nat Rev Microbiol 2003, 1:137-149.
37. Jones KM, Lloret J, Daniele JR, Walker GC:: The type IV secretion system of Sinorhizobium meliloti strain 1021 is required for conjugation but not for intracellular symbiosis. J Bacteriol 2007, 189:2133-2138.
38. Hubber AM, Sullivan JT, Ronson CW: Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Mol Plant-Microbe Interact 2007, 20:255-261.
39. Bladergroen MR, Badelt K, Spaink HP: Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant-Microbe Interact 2003, 16:53-64.
40. Mesa S, Gottfert M, Bedmar EJ: The nir, nor, and nos denitrification genes are dispersed over the Bradyrhizobium japonicum chromosome. Arch Microbiol 2001, 176:136-142.
41. Torres MJ, Rubia MI, Bedmar EJ, Delgado MJ: Denitrification in Sinorhizobium meliloti. Biochem Soc Trans 2011, 39:1886-1889.
42. Koch M, Delmotte N, Rehrauer H, Vorholt JA, Pessi G, Hennecke H: Rhizobial adaptation to hosts, a new facet in the legume root-nodule symbiosis. Mol Plant Microbe Interact 2010, 23:784-790.
43. Hummerjohann J, Laudenbach S, Retey J, Leisinger T, Kertesz MA: The sulfur-regulated arylsulfatase gene cluster of Pseudomonas aeruginosa, a new member of the cys regulon. J Bacteriol 2000, 182:2055-2058.
44. Ardourel M, Lortet G, Maillet F, Roche P, Truchet G, Prome JC, Rosenberg C: In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol Microbiol 1995, 17:687-699.
45. van Berkum P, Elia P, Eardly BD: Multilocus sequence typing as an approach for population analysis of Medicago-nodulating rhizobia. J Bacteriol 2006, 188:5570-5577.
46. Heath KD: Intergenomic epistasis and coevolutionary constraint in plants and rhizobia. Evolution 2010, 64:1446-1458.
47. ABySS.. [http://www.bcgsc.ca/platform/ bioinfo/software/abyss/].
48. Bocs S, Cruveiller S, Vallenet D, Nuel G, Medigue C: AMIGene: Annotation of Microbial Genes. Nucleic Acids Res 2003, 31:3723-3726.
49. Vallenet D, Engelen S, Mornico D, Cruveiller S, Fleury L, Lajus A, Rouy Z, Roche D, Salvignol G, Scarpelli C, Medigue C: MicroScope: a platform for microbial genome annotation and comparative genomics. Database (Oxford) 2009, 2009:bap021.
50. Becker A, Barnett MJ, Capela D, Dondrup M, Kamp PB, Krol E, Linke B, Rüberg S, Runte K, Schroeder BK, Weidner S, Yurgel SN, Batut J, Long SR, Pühler A, Goesmann A: A portal for rhizobial genomes: RhizoGATE integrates a Sinorhizobium meliloti genome annotation update with postgenome data. J Biotechnol 2009, 140:45-50.
51. MaGe interface.. [https://www.genoscope.cns.fr/agc/microscope/home/ index.php].
52. CD-HIT.. [http://weizhong-lab.ucsd.edu/cd-hit/].
53. Felsenstein J: PHYLIP -Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164.
54. Sukumaran J, Holder MT: DendroPy: a Python library for phylogenetic computing. Bioinformatics 2010, 26:1569-1571.
55. Bucciarelli B, Hanan J, Palmquist D, Vance CP: A standardized method for analysis of Medicago truncatula phenotypic development. Plant Physiol 2006, 142:207-219.
56. Sadowsky MJ, Tully RE, Cregan PB, Keyser HH: Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotypespecific nodulation of soybean. Appl Environ Microbiol 1987, 53:2624-2630.
57. R 2.14.1.. [http://cran.r-project.org/bin/windows/base/].
58. O'Hara GW, Franklin M, Dilworth MJ: Effect of sulfur supply on sulfate uptake, and alkaline sulfatase activity in free-living and symbiotic bradyrhizobia. Arch Microbiol 1987, 149:163-167.