{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T07:18:27Z","timestamp":1761895107117},"reference-count":58,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Microbiol"],"published-print":{"date-parts":[[2010,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>The TolC protein from <jats:italic>Sinorhizobium meliloti<\/jats:italic> has previously been demonstrated to be required for establishing successful biological nitrogen fixation symbiosis with <jats:italic>Medicago sativa<\/jats:italic>. It is also needed in protein and exopolysaccharide secretion and for protection against osmotic and oxidative stresses. Here, the transcriptional profile of free-living <jats:italic>S. meliloti<\/jats:italic> 1021 <jats:italic>tolC<\/jats:italic> mutant is described as a step toward understanding its role in the physiology of the cell.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>Comparison of <jats:italic>tolC<\/jats:italic> mutant and wild-type strains transcriptomes showed 1177 genes with significantly increased expression while 325 had significantly decreased expression levels. The genes with an increased expression suggest the activation of a cytoplasmic and extracytoplasmic stress responses possibly mediated by the sigma factor RpoH1 and protein homologues of the CpxRA two-component regulatory system of Enterobacteria, respectively. Stress conditions are probably caused by perturbation of the cell envelope. Consistent with gene expression data, biochemical analysis indicates that the <jats:italic>tolC<\/jats:italic> mutant suffers from oxidative stress. This is illustrated by the elevated enzyme activity levels detected for catalase, superoxide dismutase and glutathione reductase. The observed increase in the expression of genes encoding products involved in central metabolism and transporters for nutrient uptake suggests a higher metabolic rate of the <jats:italic>tolC<\/jats:italic> mutant. We also demonstrated increased swarming motility in the <jats:italic>tolC<\/jats:italic> mutant strain. Absence of functional TolC caused decreased expression mainly of genes encoding products involved in nitrogen metabolism and transport.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusion<\/jats:title>\n            <jats:p>This work shows how a mutation in the outer membrane protein TolC, common to many bacterial transport systems, affects expression of a large number of genes that act in concert to restore cell homeostasis. This finding further underlines the fundamental role of this protein in <jats:italic>Sinorhizobium meliloti<\/jats:italic> biology.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1471-2180-10-180","type":"journal-article","created":{"date-parts":[[2010,6,23]],"date-time":"2010-06-23T18:14:24Z","timestamp":1277316864000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Absence of functional TolC protein causes increased stress response gene expression in Sinorhizobium meliloti"],"prefix":"10.1186","volume":"10","author":[{"given":"M\u00e1rio R","family":"Santos","sequence":"first","affiliation":[]},{"given":"Ana M","family":"Cosme","sequence":"additional","affiliation":[]},{"given":"J\u00f6rg D","family":"Becker","sequence":"additional","affiliation":[]},{"given":"Jo\u00e3o MC","family":"Medeiros","sequence":"additional","affiliation":[]},{"given":"M\u00e1rcia F","family":"Mata","sequence":"additional","affiliation":[]},{"given":"Leonilde M","family":"Moreira","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2010,6,23]]},"reference":[{"key":"1136_CR1","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1146\/annurev.biochem.73.011303.074104","volume":"73","author":"V Koronakis","year":"2004","unstructured":"Koronakis V, Eswaran J, Hughes C: Structure and function of TolC: the bacterial exit duct for proteins and drugs. Annu Rev Biochem. 2004, 73: 467-489. 10.1146\/annurev.biochem.73.011303.074104.","journal-title":"Annu Rev Biochem"},{"key":"1136_CR2","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1038\/nrmicro1464","volume":"4","author":"LJ Piddock","year":"2006","unstructured":"Piddock LJ: Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol. 2006, 4: 629-636. 10.1038\/nrmicro1464.","journal-title":"Nat Rev Microbiol"},{"key":"1136_CR3","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1128\/CMR.19.2.382-402.2006","volume":"19","author":"LJ Piddock","year":"2006","unstructured":"Piddock LJ: Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev. 2006, 19: 382-402. 10.1128\/CMR.19.2.382-402.2006.","journal-title":"Clin Microbiol Rev"},{"key":"1136_CR4","doi-asserted-by":"publisher","first-page":"7693","DOI":"10.1128\/JB.00853-08","volume":"190","author":"H Yamanaka","year":"2008","unstructured":"Yamanaka H, Kobayashi H, Takahashi E, Okamoto K: MacAB is involved in the secretion of Escherichia coli heat-stable enterotoxin II. J Bacteriol. 2008, 190: 7693-7698. 10.1128\/JB.00853-08.","journal-title":"J Bacteriol"},{"key":"1136_CR5","doi-asserted-by":"publisher","first-page":"6701","DOI":"10.1128\/JB.187.19.6701-6707.2005","volume":"187","author":"C Bleuel","year":"2005","unstructured":"Bleuel C, Grosse C, Taudte N, Scherer J, Wesenberg D, Krauss GJ, Nies DH, Grass G: TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol. 2005, 187: 6701-6707. 10.1128\/JB.187.19.6701-6707.2005.","journal-title":"J Bacteriol"},{"key":"1136_CR6","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.bbamcr.2004.05.001","volume":"1694","author":"P Delepelaire","year":"2004","unstructured":"Delepelaire P: Type I secretion in gram-negative bacteria. Biochim Biophys Acta. 2004, 1694: 149-161. 10.1016\/j.bbamcr.2004.05.001.","journal-title":"Biochim Biophys Acta"},{"key":"1136_CR7","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1006\/jmbi.2001.4578","volume":"308","author":"GJ German","year":"2001","unstructured":"German GJ, Misra R: The TolC protein of Escherichia coli serves as a cell-surface receptor for the newly characterized TLS bacteriophage. J Mol Biol. 2001, 308: 579-585. 10.1006\/jmbi.2001.4578.","journal-title":"J Mol Biol"},{"key":"1136_CR8","doi-asserted-by":"publisher","first-page":"5283","DOI":"10.1128\/JB.00507-09","volume":"191","author":"JL Rosner","year":"2009","unstructured":"Rosner JL, Martin RG: An excretory function for the Escherichia coli outer membrane pore TolC: upregulation of marA and soxS transcription and Rob activity due to metabolites accumulated in tolC mutants. J Bacteriol. 2009, 191: 5283-5292. 10.1128\/JB.00507-09.","journal-title":"J Bacteriol"},{"key":"1136_CR9","doi-asserted-by":"publisher","first-page":"5772","DOI":"10.1128\/JB.185.19.5772-5778.2003","volume":"185","author":"RD Barabote","year":"2003","unstructured":"Barabote RD, Johnson OL, Zetina E, San Francisco SK, Fralick JA, San Francisco MJ: Erwinia chrysanthemi tolC is involved in resistance to antimicrobial plant chemicals and is essential for phytopathogenesis. J Bacteriol. 2003, 185: 5772-5778. 10.1128\/JB.185.19.5772-5778.2003.","journal-title":"J Bacteriol"},{"key":"1136_CR10","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1094\/MPMI-20-4-0403","volume":"20","author":"JD Reddy","year":"2007","unstructured":"Reddy JD, Reddy SL, Hopkins DL, Gabriel DW: TolC is required for pathogenicity of Xylella fastidiosa in Vitis vinifera grapevines. Mol Plant Microbe Interact. 2007, 20: 403-410. 10.1094\/MPMI-20-4-0403.","journal-title":"Mol Plant Microbe Interact"},{"key":"1136_CR11","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1128\/IAI.01349-06","volume":"75","author":"DM Posadas","year":"2007","unstructured":"Posadas DM, Martin FA, Sabio y Garcia JV, Spera JM, Delpino MV, Baldi P, Campos E, Cravero SL, Zorreguieta A: The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence. Infect Immun. 2007, 75: 379-389. 10.1128\/IAI.01349-06.","journal-title":"Infect Immun"},{"key":"1136_CR12","doi-asserted-by":"publisher","first-page":"4681","DOI":"10.1128\/IAI.69.7.4681-4685.2001","volume":"69","author":"JE Bina","year":"2001","unstructured":"Bina JE, Mekalanos JJ: Vibrio cholerae tolC is required for bile resistance and colonization. Infect Immun. 2001, 69: 4681-4685. 10.1128\/IAI.69.7.4681-4685.2001.","journal-title":"Infect Immun"},{"key":"1136_CR13","doi-asserted-by":"publisher","first-page":"4276","DOI":"10.1128\/JB.00363-09","volume":"191","author":"MA Webber","year":"2009","unstructured":"Webber MA, Bailey AM, Blair JM, Morgan E, Stevens MP, Hinton JC, Ivens A, Wain J, Piddock LJ: The global consequence of disruption of the AcrAB-TolC efflux pump in Salmonella enterica includes reduced expression of SPI-1 and other attributes required to infect the host. J Bacteriol. 2009, 191: 4276-4285. 10.1128\/JB.00363-09.","journal-title":"J Bacteriol"},{"key":"1136_CR14","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1111\/j.1462-5822.2005.00671.x","volume":"8","author":"AM Buckley","year":"2006","unstructured":"Buckley AM, Webber MA, Cooles S, Randall LP, La Ragione RM, Woodward MJ, Piddock LJ: The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol. 2006, 8: 847-856. 10.1111\/j.1462-5822.2005.00671.x.","journal-title":"Cell Microbiol"},{"key":"1136_CR15","doi-asserted-by":"publisher","first-page":"947","DOI":"10.1094\/MPMI-21-7-0947","volume":"21","author":"AM Cosme","year":"2008","unstructured":"Cosme AM, Becker A, Santos MR, Sharypova LA, Santos PM, Moreira LM: The outer membrane protein TolC from Sinorhizobium meliloti affects protein secretion, polysaccharide biosynthesis, antimicrobial resistance, and symbiosis. Mol Plant Microbe Interact. 2008, 21: 947-957. 10.1094\/MPMI-21-7-0947.","journal-title":"Mol Plant Microbe Interact"},{"key":"1136_CR16","doi-asserted-by":"publisher","first-page":"2237","DOI":"10.1099\/00221287-146-9-2237","volume":"146","author":"LM Moreira","year":"2000","unstructured":"Moreira LM, Becker JD, Puhler A, Becker A: The Sinorhizobium meliloti ExpE1 protein secreted by a type I secretion system involving ExpD1 and ExpD2 is required for biosynthesis or secretion of the exopolysaccharide galactoglucan. Microbiology. 2000, 146: 2237-2248.","journal-title":"Microbiology"},{"key":"1136_CR17","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1128\/MMBR.00007-08","volume":"72","author":"E Guisbert","year":"2008","unstructured":"Guisbert E, Yura T, Rhodius VA, Gross CA: Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol Mol Biol Rev. 2008, 72: 545-554. 10.1128\/MMBR.00007-08.","journal-title":"Microbiol Mol Biol Rev"},{"key":"1136_CR18","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1099\/mic.0.021428-0","volume":"155","author":"JM Martinez-Salazar","year":"2009","unstructured":"Martinez-Salazar JM, Sandoval-Calderon M, Guo X, Castillo-Ramirez S, Reyes A, Loza MG, Rivera J, Alvarado-Affantranger X, Sanchez F, Gonzalez V: The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses. Microbiology. 2009, 155: 386-397. 10.1099\/mic.0.021428-0.","journal-title":"Microbiology"},{"key":"1136_CR19","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.1128\/JB.01542-06","volume":"189","author":"AN Bittner","year":"2007","unstructured":"Bittner AN, Foltz A, Oke V: Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti. J Bacteriol. 2007, 189: 1884-1889. 10.1128\/JB.01542-06.","journal-title":"J Bacteriol"},{"key":"1136_CR20","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1126\/science.8465200","volume":"260","author":"CP Selby","year":"1993","unstructured":"Selby CP, Sancar A: Molecular mechanism of transcription-repair coupling. Science. 1993, 260: 53-58. 10.1126\/science.8465200.","journal-title":"Science"},{"key":"1136_CR21","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1111\/j.1742-4658.2008.06743.x","volume":"276","author":"N Allocati","year":"2009","unstructured":"Allocati N, Federici L, Masulli M, Di Ilio C: Glutathione transferases in bacteria. Febs J. 2009, 276: 58-75. 10.1111\/j.1742-4658.2008.06743.x.","journal-title":"Febs J"},{"key":"1136_CR22","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1042\/BJ20081218","volume":"418","author":"A Cereda","year":"2009","unstructured":"Cereda A, Carpen A, Picariello G, Tedeschi G, Pagani S: The lack of rhodanese RhdA affects the sensitivity of Azotobacter vinelandii to oxidative events. Biochem J. 2009, 418: 135-143. 10.1042\/BJ20081218.","journal-title":"Biochem J"},{"key":"1136_CR23","doi-asserted-by":"crossref","first-page":"4509","DOI":"10.1128\/JB.181.15.4509-4516.1999","volume":"181","author":"R Santos","year":"1999","unstructured":"Santos R, Bocquet S, Puppo A, Touati D: Characterization of an atypical superoxide dismutase from Sinorhizobium meliloti. J Bacteriol. 1999, 181: 4509-4516.","journal-title":"J Bacteriol"},{"key":"1136_CR24","doi-asserted-by":"publisher","first-page":"5398","DOI":"10.1128\/JB.00092-09","volume":"191","author":"AE Sikora","year":"2009","unstructured":"Sikora AE, Beyhan S, Bagdasarian M, Yildiz FH, Sandkvist M: Cell envelope perturbation induces oxidative stress and changes in iron homeostasis in Vibrio cholerae. J Bacteriol. 2009, 191: 5398-5408. 10.1128\/JB.00092-09.","journal-title":"J Bacteriol"},{"key":"1136_CR25","doi-asserted-by":"publisher","first-page":"8484","DOI":"10.1128\/JB.00583-07","volume":"189","author":"AE Sikora","year":"2007","unstructured":"Sikora AE, Lybarger SR, Sandkvist M: Compromised outer membrane integrity in Vibrio cholerae Type II secretion mutants. J Bacteriol. 2007, 189: 8484-8495. 10.1128\/JB.00583-07.","journal-title":"J Bacteriol"},{"key":"1136_CR26","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1146\/annurev.micro.55.1.591","volume":"55","author":"TL Raivio","year":"2001","unstructured":"Raivio TL, Silhavy TJ: Periplasmic stress and ECF sigma factors. Ann Rev Microbiol. 2001, 55: 591-624. 10.1146\/annurev.micro.55.1.591.","journal-title":"Ann Rev Microbiol"},{"key":"1136_CR27","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1016\/j.mib.2005.02.013","volume":"8","author":"N Ruiz","year":"2005","unstructured":"Ruiz N, Silhavy TJ: Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol. 2005, 8: 122-126. 10.1016\/j.mib.2005.02.013.","journal-title":"Curr Opin Microbiol"},{"key":"1136_CR28","doi-asserted-by":"publisher","first-page":"1798","DOI":"10.1128\/JB.00798-08","volume":"191","author":"NL Price","year":"2009","unstructured":"Price NL, Raivio TL: Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol. 2009, 191: 1798-1815. 10.1128\/JB.00798-08.","journal-title":"J Bacteriol"},{"key":"1136_CR29","volume-title":"FEMS Microbiol Lett","author":"K Ronnebaumer","year":"2009","unstructured":"Ronnebaumer K, Sander G, Shutinoski B, Schmidt MA, Heusipp G: Controlled activation of the Cpx system is essential for growth of Yersinia enterocolitica. FEMS Microbiol Lett. 2009"},{"key":"1136_CR30","doi-asserted-by":"publisher","first-page":"7617","DOI":"10.1128\/JB.00719-06","volume":"188","author":"A Dominguez-Ferreras","year":"2006","unstructured":"Dominguez-Ferreras A, Perez-Arnedo R, Becker A, Olivares J, Soto MJ, Sanjuan J: Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol. 2006, 188: 7617-7625. 10.1128\/JB.00719-06.","journal-title":"J Bacteriol"},{"key":"1136_CR31","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.jbiotec.2003.08.005","volume":"106","author":"S Ruberg","year":"2003","unstructured":"Ruberg S, Tian ZX, Krol E, Linke B, Meyer F, Wang Y, Puhler A, Weidner S, Becker A: Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J Biotechnol. 2003, 106: 255-268. 10.1016\/j.jbiotec.2003.08.005.","journal-title":"J Biotechnol"},{"key":"1136_CR32","doi-asserted-by":"publisher","first-page":"4218","DOI":"10.1128\/AEM.02244-07","volume":"74","author":"S Rossbach","year":"2008","unstructured":"Rossbach S, Mai DJ, Carter EL, Sauviac L, Capela D, Bruand C, de Bruijn FJ: Response of Sinorhizobium meliloti to elevated concentrations of cadmium and zinc. Appl Environ Microbiol. 2008, 74: 4218-4221. 10.1128\/AEM.02244-07.","journal-title":"Appl Environ Microbiol"},{"key":"1136_CR33","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1186\/1471-2180-9-37","volume":"9","author":"C Hellweg","year":"2009","unstructured":"Hellweg C, Puhler A, Weidner S: The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol. 2009, 9: 37-10.1186\/1471-2180-9-37.","journal-title":"BMC Microbiol"},{"key":"1136_CR34","doi-asserted-by":"publisher","first-page":"4204","DOI":"10.1128\/JB.00175-07","volume":"189","author":"L Sauviac","year":"2007","unstructured":"Sauviac L, Philippe H, Phok K, Bruand C: An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. J Bacteriol. 2007, 189: 4204-4216. 10.1128\/JB.00175-07.","journal-title":"J Bacteriol"},{"key":"1136_CR35","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1146\/annurev.micro.61.080706.093440","volume":"61","author":"AJ Carpousis","year":"2007","unstructured":"Carpousis AJ: The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Ann Rev Microbiol. 2007, 61: 71-87. 10.1146\/annurev.micro.61.080706.093440.","journal-title":"Ann Rev Microbiol"},{"key":"1136_CR36","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1128\/JB.180.1.73-82.1998","volume":"180","author":"GO Bylund","year":"1998","unstructured":"Bylund GO, Wipemo LC, Lundberg LA, Wikstrom PM: RimM and RbfA are essential for efficient processing of 16 S rRNA in Escherichia coli. J Bacteriol. 1998, 180: 73-82.","journal-title":"J Bacteriol"},{"key":"1136_CR37","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1016\/j.cbpa.2008.09.024","volume":"12","author":"SA Woodson","year":"2008","unstructured":"Woodson SA: RNA folding and ribosome assembly. Curr Opin Chem Biol. 2008, 12: 667-673. 10.1016\/j.cbpa.2008.09.024.","journal-title":"Curr Opin Chem Biol"},{"key":"1136_CR38","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1016\/j.jmb.2004.05.019","volume":"340","author":"Z Yang","year":"2004","unstructured":"Yang Z, Shipman L, Zhang M, Anton BP, Roberts RJ, Cheng X: Structural characterization and comparative phylogenetic analysis of Escherichia coli HemK, a protein (N5)-glutamine methyltransferase. J Mol Biol. 2004, 340: 695-706. 10.1016\/j.jmb.2004.05.019.","journal-title":"J Mol Biol"},{"issue":"3","key":"1136_CR39","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/j.micpath.2008.05.001","volume":"45","author":"P Shah","year":"2008","unstructured":"Shah P, Romero DG, Swiatlo E: Role of polyamine transport in Streptococcus pneumoniae response to physiological stress and murine septicemia. Microb Pathog. 2008, 45 (3): 167-172. 10.1016\/j.micpath.2008.05.001.","journal-title":"Microb Pathog"},{"key":"1136_CR40","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1128\/MMBR.66.2.203-222.2002","volume":"66","author":"EJ Patriarca","year":"2002","unstructured":"Patriarca EJ, Tate R, Iaccarino M: Key role of bacterial NH(4)(+) metabolism in Rhizobium-plant symbiosis. Microbiol Mol Biol Rev. 2002, 66: 203-222. 10.1128\/MMBR.66.2.203-222.2002.","journal-title":"Microbiol Mol Biol Rev"},{"key":"1136_CR41","doi-asserted-by":"publisher","first-page":"1340","DOI":"10.1111\/j.1365-2958.2005.04912.x","volume":"58","author":"AK Hottes","year":"2005","unstructured":"Hottes AK, Shapiro L, McAdams HH: DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol. 2005, 58: 1340-1353. 10.1111\/j.1365-2958.2005.04912.x.","journal-title":"Mol Microbiol"},{"key":"1136_CR42","doi-asserted-by":"crossref","first-page":"3139","DOI":"10.1128\/jb.175.10.3139-3145.1993","volume":"175","author":"YX Butler","year":"1993","unstructured":"Butler YX, Abhayawardhane Y, Stewart GC: Amplification of the Bacillus subtilis maf gene results in arrested septum formation. J Bacteriol. 1993, 175: 3139-3145.","journal-title":"J Bacteriol"},{"key":"1136_CR43","doi-asserted-by":"crossref","first-page":"5426","DOI":"10.1128\/JB.180.20.5426-5431.1998","volume":"180","author":"A Kereszt","year":"1998","unstructured":"Kereszt A, Kiss E, Reuhs BL, Carlson RW, Kondorosi A, Putnoky P: Novel rkp gene clusters of Sinorhizobium meliloti involved in capsular polysaccharide production and invasion of the symbiotic nodule: the rkpK gene encodes a UDP-glucose dehydrogenase. J Bacteriol. 1998, 180: 5426-5431.","journal-title":"J Bacteriol"},{"key":"1136_CR44","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/s004380050667","volume":"257","author":"PA Bertram-Drogatz","year":"1998","unstructured":"Bertram-Drogatz PA, Quester I, Becker A, Puhler A: The Sinorhizobium meliloti MucR protein, which is essential for the production of high-molecular-weight succinoglycan exopolysaccharide, binds to short DNA regions upstream of exoH and exoY. Mol Gen Genet. 1998, 257: 433-441. 10.1007\/s004380050667.","journal-title":"Mol Gen Genet"},{"key":"1136_CR45","doi-asserted-by":"publisher","first-page":"6042","DOI":"10.1128\/JB.186.18.6042-6049.2004","volume":"186","author":"SY Yao","year":"2004","unstructured":"Yao SY, Luo L, Har KJ, Becker A, Ruberg S, Yu GQ, Zhu JB, Cheng HP: Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J Bacteriol. 2004, 186: 6042-6049. 10.1128\/JB.186.18.6042-6049.2004.","journal-title":"J Bacteriol"},{"key":"1136_CR46","doi-asserted-by":"publisher","first-page":"3456","DOI":"10.1128\/JB.00062-08","volume":"190","author":"C Bahlawane","year":"2008","unstructured":"Bahlawane C, Baumgarth B, Serrania J, Ruberg S, Becker A: Fine-tuning of galactoglucan biosynthesis in Sinorhizobium meliloti by differential WggR (ExpG)-, PhoB-, and MucR-dependent regulation of two promoters. J Bacteriol. 2008, 190: 3456-3466. 10.1128\/JB.00062-08.","journal-title":"J Bacteriol"},{"key":"1136_CR47","doi-asserted-by":"publisher","first-page":"6231","DOI":"10.1073\/pnas.82.18.6231","volume":"82","author":"JA Leigh","year":"1985","unstructured":"Leigh JA, Signer ER, Walker GC: Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci USA. 1985, 82: 6231-6235. 10.1073\/pnas.82.18.6231.","journal-title":"Proc Natl Acad Sci USA"},{"key":"1136_CR48","doi-asserted-by":"publisher","first-page":"5067","DOI":"10.1128\/JB.184.18.5067-5076.2002","volume":"184","author":"BJ Pellock","year":"2002","unstructured":"Pellock BJ, Teplitski M, Boinay RP, Bauer WD, Walker GC: A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J Bacteriol. 2002, 184: 5067-5076. 10.1128\/JB.184.18.5067-5076.2002.","journal-title":"J Bacteriol"},{"key":"1136_CR49","doi-asserted-by":"publisher","first-page":"4329","DOI":"10.1128\/AEM.03072-05","volume":"72","author":"N Pobigaylo","year":"2006","unstructured":"Pobigaylo N, Wetter D, Szymczak S, Schiller U, Kurtz S, Meyer F, Nattkemper TW, Becker A: Construction of a large signature-tagged mini-Tn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti. Appl Environ Microbiol. 2006, 72: 4329-4337. 10.1128\/AEM.03072-05.","journal-title":"Appl Environ Microbiol"},{"key":"1136_CR50","first-page":"188","volume":"84","author":"JE Beringer","year":"1974","unstructured":"Beringer JE: R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974, 84: 188-198.","journal-title":"J Gen Microbiol"},{"key":"1136_CR51","doi-asserted-by":"crossref","first-page":"RESEARCH0032","DOI":"10.1186\/gb-2001-2-10-reports0032","volume":"2","author":"C Li","year":"2001","unstructured":"Li C, Wong WH: Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2001, 2: RESEARCH0032-","journal-title":"Genome Biol"},{"key":"1136_CR52","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1073\/pnas.98.1.31","volume":"98","author":"C Li","year":"2001","unstructured":"Li C, Wong WH: Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA. 2001, 98: 31-36. 10.1073\/pnas.011404098.","journal-title":"Proc Natl Acad Sci USA"},{"key":"1136_CR53","doi-asserted-by":"publisher","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","volume":"29","author":"MW Pfaffl","year":"2001","unstructured":"Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29: e45-10.1093\/nar\/29.9.e45.","journal-title":"Nucleic Acids Res"},{"key":"1136_CR54","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","volume":"72","author":"MM Bradford","year":"1976","unstructured":"Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976, 72: 248-254. 10.1016\/0003-2697(76)90527-3.","journal-title":"Anal Biochem"},{"key":"1136_CR55","doi-asserted-by":"publisher","first-page":"532","DOI":"10.1016\/0003-2697(84)90204-5","volume":"140","author":"DA Clare","year":"1984","unstructured":"Clare DA, Duong MN, Darr D, Archibald F, Fridovich I: Effects of molecular oxygen on detection of superoxide radical with nitroblue tetrazolium and on activity stains for catalase. Anal Biochem. 1984, 140: 532-537. 10.1016\/0003-2697(84)90204-5.","journal-title":"Anal Biochem"},{"key":"1136_CR56","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1016\/0003-2697(88)90564-7","volume":"175","author":"IK Smith","year":"1988","unstructured":"Smith IK, Vierheller TL, Thorne CA: Assay of glutathione reductase in crude tissue homogenates using 5,5'-dithiobis(2-nitrobenzoic acid). Anal Biochem. 1988, 175: 408-413. 10.1016\/0003-2697(88)90564-7.","journal-title":"Anal Biochem"},{"key":"1136_CR57","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1093\/jac\/dkn217","volume":"62","author":"I Couto","year":"2008","unstructured":"Couto I, Costa SS, Viveiros M, Martins M, Amaral L: Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide. J Antimicrob Chemother. 2008, 62: 504-513. 10.1093\/jac\/dkn217.","journal-title":"J Antimicrob Chemother"},{"key":"1136_CR58","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1046\/j.1365-2958.2002.02749.x","volume":"43","author":"MJ Soto","year":"2002","unstructured":"Soto MJ, Fernandez-Pascual M, Sanjuan J, Olivares J: A fadD mutant of Sinorhizobium meliloti shows multicellular swarming migration and is impaired in nodulation efficiency on alfalfa roots. Mol Microbiol. 2002, 43: 371-382. 10.1046\/j.1365-2958.2002.02749.x.","journal-title":"Mol Microbiol"}],"container-title":["BMC Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2180-10-180.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T12:34:02Z","timestamp":1630499642000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmicrobiol.biomedcentral.com\/articles\/10.1186\/1471-2180-10-180"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,6,23]]},"references-count":58,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2010,12]]}},"alternative-id":["1136"],"URL":"https:\/\/doi.org\/10.1186\/1471-2180-10-180","relation":{},"ISSN":["1471-2180"],"issn-type":[{"value":"1471-2180","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,6,23]]},"assertion":[{"value":"17 February 2010","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 June 2010","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 June 2010","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"180"}}