BMC Genomics | |
Genomic basis of symbiovar mimosae in Rhizobium etli | |
Esperanza Martínez-Romero1  Ernesto Ormeño-Orrillo1  Julio Martínez-Romero1  Jaime Castro-Mondragón1  Luis Lozano3  Miguel Ángel Cevallos3  David Romero2  Víctor González3  Rosa I Santamaría3  Patricia Bustos3  Marco A Rogel1  | |
[1] Ecological Genomics programs, Genomics Science Center, CCG, Cuernavaca, Morelos, Mexico;Genome Engineering programs, Genomics Science Center, CCG, Cuernavaca, Morelos, Mexico;Evolutionary Genomics programs, Genomics Science Center, CCG, Cuernavaca, Morelos, Mexico | |
关键词: Host specificity; Nitrogen fixation; Bacterial symbiosis; Legume nodulation; | |
Others : 1216498 DOI : 10.1186/1471-2164-15-575 |
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received in 2013-09-02, accepted in 2014-07-01, 发布年份 2014 | |
【 摘 要 】
Background
Symbiosis genes (nod and nif) involved in nodulation and nitrogen fixation in legumes are plasmid-borne in Rhizobium. Rhizobial symbiotic variants (symbiovars) with distinct host specificity would depend on the type of symbiosis plasmid. In Rhizobium etli or in Rhizobium phaseoli, symbiovar phaseoli strains have the capacity to form nodules in Phaseolus vulgaris while symbiovar mimosae confers a broad host range including different mimosa trees.
Results
We report on the genome of R. etli symbiovar mimosae strain Mim1 and its comparison to that from R. etli symbiovar phaseoli strain CFN42. Differences were found in plasmids especially in the symbiosis plasmid, not only in nod gene sequences but in nod gene content. Differences in Nod factors deduced from the presence of nod genes, in secretion systems or ACC-deaminase could help explain the distinct host specificity. Genes involved in P. vulgaris exudate uptake were not found in symbiovar mimosae but hup genes (involved in hydrogen uptake) were found. Plasmid pRetCFN42a was partially contained in Mim1 and a plasmid (pRetMim1c) was found only in Mim1. Chromids were well conserved.
Conclusions
The genomic differences between the two symbiovars, mimosae and phaseoli may explain different host specificity. With the genomic analysis presented, the term symbiovar is validated. Furthermore, our data support that the generalist symbiovar mimosae may be older than the specialist symbiovar phaseoli.
【 授权许可】
2014 Rogel et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 1. | 30KB | Image | download |
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【 参考文献 】
- [1]López-Guerrero MG, Ormeño-Orrillo E, Velázquez E, Rogel MA, Acosta JL, Gónzalez V, Martínez J, Martínez-Romero E: Rhizobium etli taxonomy revised with novel genomic data and analyses. Syst Appl Microbiol 2012, 35:353-358.
- [2]Rogel MA, Ormeño-Orrillo E, Martinez Romero E: Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 2011, 34:96-104.
- [3]Cobo-Díaz JF, Martínez-Hidalgo P, Fernández-González AJ, Martínez-Molina E, Toro N, Velázquez E, Fernández-López M: The endemic Genista versicolor from Sierra Nevada National Park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst Appl Microbiol 2013, 37:177-185.
- [4]Gubry-Rangin C, Béna G, Cleyet-Marel JC, Brunel B: Definition and evolution of a new symbiovar, sv. rigiduloides, among Ensifer meliloti efficiently nodulating Medicago species. Syst Appl Microbiol 2013, 36:490-496.
- [5]Ramírez-Bahena MH, Chahboune R, Velázquez E, Gómez-Moriano A, Mora E, Peix A, Toro M: Centrosema is a promiscuous legume nodulated by several new putative species and symbiovars of Bradyrhizobium in various American countries. Syst Appl Microbiol 2013, 36:392-400.
- [6]Laranjo M, Young JP, Oliveira S: Multilocus sequence analysis reveals multiple symbiovars within Mesorhizobium species. Syst Appl Microbiol 2012, 35:359-367.
- [7]Ramírez-Bahena MH, Hernández M, Peix A, Velázquez E, León-Barrios M: Mesorhizobial strains nodulating Anagyris latifolia and Lotus berthelotii in Tamadaya ravine (Tenerife, Canary Islands) are two symbiovars of the same species, Mesorhizobium tamadayense sp. nov. Syst Appl Microbiol 2012, 35:334-341.
- [8]Crossman LC, Castillo-Ramírez S, McAnnula C, Lozano L, Vernikos GS, Acosta JL, Ghazoui ZF, Hernández-González I, Meakin G, Walker AW, Hynes MF, Young JP, Downie JA, Romero D, Johnston AW, Dávila G, Parkhill J, González V: A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria. PLoS One 2008, 3:e2567.
- [9]Wang ET, Rogel MA, García-de los Santos A, Martínez-Romero J, Cevallos MA, Martínez-Romero E: Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 1999, 49:1479-1491.
- [10]Ormeño-Orrillo E, Rogel-Hernández MA, Lloret L, López-López A, Martínez J, Barois I, Martínez-Romero E: Change in land use alters the diversity and composition of Bradyrhizobium communities and led to the introduction of Rhizobium etli into the tropical rain forest of Los Tuxtlas (Mexico). Microb Ecol 2012, 63:822-834.
- [11]Vázquez M, Dávalos A, de las Peñas A, Sánchez F, Quinto C: Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. J Bacteriol 1991, 173:1250-1258.
- [12]Silva C, Vinuesa P, Eguiarte LE, Souza V, Martínez-Romero E: Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol Ecol 2005, 14:4033-4050.
- [13]Martínez-Romero E: Coevolution in Rhizobium-legume symbiosis? DNA Cell Biol 2009, 28:361-370.
- [14]Delgado-Salinas A, Bibler R, Lavin M: Phylogeny of the genus Phaseolus (Leguminosae): a recent diversification in an ancient landscape. Syst Bot 2006, 31:779-791.
- [15]Dos Reis FBJ, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, Loureiro MF, de Queiroz LP, Scotti MR, Chen WM, Norén A, Rubio MC, de Faria SM, Bontemps C, Goi SR, Young JP, Sprent JI, James EK: Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 2010, 186:934-946.
- [16]Chen WM, de Faria SM, James EK, Elliott GN, Lin KY, Chou JH, Sheu SY, Cnockaert M, Sprent JI, Vandamme P: Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 2007, 57:1055-1059.
- [17]Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JP, Vandamme P: Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 2008, 58:2174-2179.
- [18]Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JP, Chen WM: Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 2012, 62:2272-2278.
- [19]Taulé C, Zabaleta M, Mareque C, Platero R, Sanjurjo L, Sicardi M, Frioni L, Battistoni F, Fabiano E: New Betaproteobacterial Rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol 2012, 78:1692.
- [20]Simon MF, Grether R, de Queiroz LP, Särkinen TE, Dutra VF, Hughes CE: The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants. Am J Bot 2011, 98:1201-1221.
- [21]Elliott GN, Chou JH, Chen WM, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JP, Sprent JI, James EK: Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 2009, 11:762-778.
- [22]Gehlot HS, Tak N, Kaushik M, Mitra S, Chen W-M, Poweleit N, Panwar D, Poonar N, Parihar R, Tak A, Sankhla IS, Ojha A, Rao SR, Simon MF, Dos Reis FB, Perigolo N, Tripathi A, Sprent JI, Young JPW, James EK, Gyaneshwar P: An invasive Mimosa in India does not adopt the symbionts of its native relatives. Ann Bot 2013. in press
- [23]Robledo M, Velázquez E, Ramírez-Bahena MH, García-Fraile P, Pérez-Alonso A, Rivas R, Martínez-Molina E, Mateos PF: The celC gene, a new phylogenetic marker useful for taxonomic studies in Rhizobium. Syst Appl Microbiol 2011, 34:393-399.
- [24]Toledo I, Lloret L, Martínez-Romero E: Sinorhizobium americanum sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst Appl Microbiol 2003, 26:54-64. Erratum in: Syst Appl Microbiol 2003, 26:319
- [25]Hynes MF, McGregor NF: Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 1990, 4:567-574.
- [26]Martinez-Romero E, Rosenblueth M: Increased bean (Phaseolus vulgaris L.) nodulation competitiveness of genetically modified Rhizobium strains. Appl Environ Microbiol 1990, 56:2384-2388.
- [27]Zerbino DR, Birney E: Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829.
- [28]Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W: Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27:578-579.
- [29]Gordon D, Abajian C, Green P: Consed: a graphical tool for sequence finishing. Genome Res 1998, 8:195-202.
- [30]Delcher AL, Harmon D, Kasif S, White O, Salzberg SL: Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999, 27:4636-4641.
- [31]Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M-A, Barrell B: Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945.
- [32]González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G: The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci U S A 2006, 103:3834-3839.
- [33]Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL: GenBank. Nucleic Acids Res 2008, 36:D25-D30.
- [34]Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MDR, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F, Sigrist CJA, Zdobnov EM: The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 2001, 29:37-40.
- [35]Richter M, Rossello-Mora R: Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009, 106:19126-19131.
- [36]Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL: Versatile and open software for comparing large genomes. Genome Biol 2004, 5:R12.
- [37]Enright AJ, Van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584.
- [38]Vernikos GS, Parkhill J: Interpolated variable order motifs for detection of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 2006, 22:2196-2203.
- [39]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
- [40]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.
- [41]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
- [42]Harrison PW, Lower RP, Kim NK, Young JP: Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid. Trends Microbiol 2010, 18:141-148.
- [43]Cevallos MA, Cervantes-Rivera R, Gutiérrez-Ríos RM: The repABC plasmid family. Plasmid 2008, 60:19-37.
- [44]Ribeiro RA, Ormeño-Orrillo E, Fuzinatto Dall’Agnol R, Graham PH, Martínez-Romero E, Hungria M: Novel Rhizobium lineages isolated from root nodules of common bean (Phaseolus vulgaris L.) in Andean and Mesoamerican areas. Res Microbiol 2013. in press
- [45]Pardo MA, Lagunez J, Miranda J, Martínez E: Nodulating ability of Rhizobium tropici is conditioned by a plasmid-encoded citrate synthase. Mol Microbiol 1994, 11:315-321.
- [46]Hernández-Lucas I, Pardo MA, Segovia L, Miranda J, Martínez-Romero E: Rhizobium tropici chromosomal citrate synthase gene. Appl Environ Microbiol 1995, 61:3992-3997.
- [47]Rosemeyer V, Michiels J, Verreth C, Vanderleyden J: luxI- and luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J Bacteriol 1998, 180:815-821.
- [48]Daniels R, De Vos DE, Desair J, Raedschelders G, Luyten E, Rosemeyer V, Verreth C, Schoeters E, Vanderleyden J, Michiels J: The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 2002, 277:462-468.
- [49]López-Guerrero MG, Ormeño-Orrillo E, Acosta JL, Mendoza-Vargas A, Rogel MA, Ramírez MA, Rosenblueth M, Martínez-Romero J, Martínez-Romero E: Rhizobial extrachromosomal replicon variability, stability and expression in natural niches. Plasmid 2012, 68:149-158.
- [50]Poupot R, Martinez-Romero E, Gautier N, Promé JC: Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors. J Biol Chem 1995, 270:6050-6055.
- [51]Laeremans T, Snoeck C, Mariën J, Verreth C, Martínez-Romero E, Promé JC, Vanderleyden J: Phaseolus vulgaris recognizes Azorhizobium caulinodans Nod factors with a variety of chemical substituents. Mol Plant Microbe Interact 1999, 12:820-824.
- [52]Waelkens F, Voets T, Vlassak K, Vanderleyden J, van Rhijn P: The nodS gene of Rhizobium tropici strain CIAT899 is necessary for nodulation on Phaseolus vulgaris and on Leucaena leucocephala. Mol Plant Microbe Interact 1995, 8:147-154.
- [53]Perret X, Staehelin C, Broughton WJ: Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 2000, 64:180-201.
- [54]van Rhijn P, Luyten E, Vlassak K, Vanderleyden J: Isolation and characterization of a pSym locus of Rhizobium sp. BR816 that extends nodulation ability of narrow host range Phaseolus vulgaris symbionts to Leucaena leucocephala. Mol Plant Microbe Interact 1996, 9:74-77.
- [55]Vlassak KM, Luyten E, Verreth C, van Rhijn P, Bisseling T, Vanderleyden J: The Rhizobium sp. BR816 nodO gene can function as a determinant for nodulation of Leucaena leucocephala, Phaseolus vulgaris, and Trifolium repens by a diversity of Rhizobium spp. Mol Plant Microbe Interact 1998, 11:383-392.
- [56]Tittabutr P, Awaya JD, Li QX, Borthakur D: The cloned 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene from Sinorhizobium sp. strain BL3 in Rhizobium sp. strain TAL1145 promotes nodulation and growth of Leucaena leucocephala. Syst Appl Microbiol 2008, 31:141-150.
- [57]González V, Bustos P, Ramírez-Romero MA, Medrano-Soto A, Salgado H, Hernández-González I, Hernández-Celis JC, Quintero V, Moreno-Hagelsieb G, Girard L, Rodríguez O, Flores M, Cevallos MA, Collado-Vides J, Romero D, Dávila G: The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments. Genome Biol 2003, 4:R36.
- [58]Girard L, Brom S, Dávalos A, López O, Soberón M, Romero D: Differential regulation of fixN-reiterated genes in Rhizobium etli by a novel fixL–fixK cascade. Mol Plant Microbe Interact 2000, 12:1283-1292.
- [59]Zamorano-Sánchez D, Reyes-González A, Gómez-Hernández N, Rivera P, Georgellis D, Girard L: FxkR provides the missing link in the fixL-fixK signal transduction cascade in Rhizobium etli CFN42. Mol Plant Microbe Interact 2012, 25:1506-1517.
- [60]Rosenblueth M, Hynes MF, Martínez-Romero E: Rhizobium tropici teu genes involved in specific uptake of Phaseolus vulgaris bean-exudate compounds. Mol Gen Genet 1998, 258:587-598.
- [61]Fauvart M, Michiels J: Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 2008, 285:1-9.
- [62]Baginsky C, Brito B, Imperial J, Palacios J-M, Ruiz-Argüeso T: Diversity and evolution of hydrogenase systems in rhizobia. Appl Environ Microbiol 2002, 68:4915-4924.
- [63]Brito B, Prieto RI, Cabrera E, Mandrand-Berthelot MA, Imperial J, Ruiz-Argueso T, Palacios JM: Rhizobium leguminosarum hupE encodes a nickel transporter required for hydrogenase activity. J Bacteriol 2010, 192:925-935.
- [64]López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E: Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 2010, 33:322-327.
- [65]Lozano L, Hernández-González I, Bustos P, Santamaría RI, Souza V, Young JP, Dávila G, González V: Evolutionary dynamics of insertion sequences in relation to the evolutionary histories of the chromosome and symbiotic plasmid genes of Rhizobium etli populations. Appl Environ Microbiol 2010, 76:6504-6513.
- [66]González V, Acosta JL, Santamaría RI, Bustos P, Fernández JL, Hernández González IL, Díaz R, Flores M, Palacios R, Mora J, Dávila G: Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of Rhizobium etli. Appl Environ Microbiol 2010, 76:1604-1614.
- [67]Brom S, Girard L, Tun-Garrido C, García-de los Santos A, Bustos P, González V, Romero D: Transfer of the symbiotic plasmid of Rhizobium etli CFN42 requires cointegration with p42a, which may be mediated by site-specific recombination. J Bacteriol 2004, 186:7538-7548.
- [68]González-Pasayo R, Martínez-Romero E: Multiresistance genes of Rhizobium etli CFN42. Mol Plant Microbe Interact 2000, 13:572-577.
- [69]Ramachandran VK, East AK, Karunakaran R, Downie JA, Poole PS: Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics. Genome Biol 2011, 12:R106.
- [70]Borthakur D, Soedarjo M: Isolation and Characterization of a DNA Fragment Containing Genes for Mimosine Degradation from Rhizobium sp. Strain TAL1145. In Highlights of Nitrogen Fixation Research. Edited by Martinez E, Hernandez G. New York: Kluwer/Plenum; 1999:91-95.
- [71]Soedarjo M, Borthakur D: Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol Biochem 1998, 30:1605-1613.