The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti

de Lucena DK, Pühler A, Weidner S (2010)
BMC Microbiology 10(1): 256.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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de Lucena, Daniella Karine; Pühler, AlfredUniBi ; Weidner, StefanUniBi
Abstract / Bemerkung
Background: Environmental pH stress constitutes a limiting factor for S. meliloti survival and development. The response to acidic pH stress in S. meliloti is versatile and characterized by the differential expression of genes associated with various cellular functions. The purpose of this study was to gain detailed insight into the participation of sigma factors in the complex stress response system of S. meliloti 1021 using pH stress as an effector. Results: In vitro assessment of S meliloti wild type and sigma factor mutants provided first evidence that the sigma factor RpoH1 plays a major role in the pH stress response. Differential expression of genes related to rhizobactin biosynthesis was observed in microarray analyses performed with the rpoH1 mutant at pH 7.0. The involvement of the sigma factor RpoH1 in the regulation of S. meliloti genes upon pH stress was analyzed by comparing timecourse experiments of the wild type and the rpoH1 mutant. Three classes of S. meliloti genes could be identified, which were transcriptionally regulated in an RpoH1-independent, an RpoH1-dependent or in a complex manner. The first class of S. meliloti genes, regulated in an RpoH1-independent manner, comprises the group of the exopolysaccharide I biosynthesis genes and also the group of genes involved in motility and flagellar biosynthesis. The second class of S. meliloti genes, regulated in an RpoH1-dependent manner, is composed of genes known from heat shock studies, like ibpA, grpE and groEL5, as well as genes involved in translation like tufA and rplC. Finally, the third class of S. meliloti genes was regulated in a complex manner, which indicates that besides sigma factor RpoH1, further regulation takes place. This was found to be the case for the genes dctA, ndvA and smc01505. Conclusions: Clustering of time-course microarray data of S. meliloti wild type and sigma factor rpoH1 mutant allowed for the identification of gene clusters, each with a unique time-dependent expression pattern, as well as for the classification of genes according to their dependence on RpoH1 expression and regulation. This study provided clear evidence that the sigma factor RpoH1 plays a major role in pH stress response.
Erscheinungsjahr
2010
Zeitschriftentitel
BMC Microbiology
Band
10
Ausgabe
1
Art.-Nr.
256
ISSN
1471-2180
Page URI
https://pub.uni-bielefeld.de/record/1903875

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de Lucena DK, Pühler A, Weidner S. The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiology. 2010;10(1): 256.
de Lucena, D. K., Pühler, A., & Weidner, S. (2010). The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiology, 10(1), 256. https://doi.org/10.1186/1471-2180-10-256
de Lucena, Daniella Karine, Pühler, Alfred, and Weidner, Stefan. 2010. “The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti”. BMC Microbiology 10 (1): 256.
de Lucena, D. K., Pühler, A., and Weidner, S. (2010). The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiology 10:256.
de Lucena, D.K., Pühler, A., & Weidner, S., 2010. The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiology, 10(1): 256.
D.K. de Lucena, A. Pühler, and S. Weidner, “The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti”, BMC Microbiology, vol. 10, 2010, : 256.
de Lucena, D.K., Pühler, A., Weidner, S.: The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiology. 10, : 256 (2010).
de Lucena, Daniella Karine, Pühler, Alfred, and Weidner, Stefan. “The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti”. BMC Microbiology 10.1 (2010): 256.
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23 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia.
Alloing G, Mandon K, Boncompagni E, Montrichard F, Frendo P., Antioxidants (Basel) 7(12), 2018
PMID: 30563061
Evolution of a multi-step phosphorelay signal transduction system in Ensifer: recruitment of the sigma factor RpoN and a novel enhancer-binding protein triggers acid-activated gene expression.
Tian R, Heiden S, Osman WA, Ardley JK, James EK, Gollagher MM, Tiwari R, Seshadri R, Kyrpides NC, Reeve WG., Mol Microbiol 103(5), 2017
PMID: 27935141
Can stress response genes be used to improve the symbiotic performance of rhizobia?
da-Silva JR, Alexandre A, Brígido C, Oliveira S., AIMS Microbiol 3(3), 2017
PMID: 31294167
An RpoHI-Dependent Response Promotes Outgrowth after Extended Stationary Phase in the Alphaproteobacterium Rhodobacter sphaeroides.
Remes B, Rische-Grahl T, Müller KMH, Förstner KU, Yu SH, Weber L, Jäger A, Peuser V, Klug G., J Bacteriol 199(14), 2017
PMID: 28507242
Regulator LdhR and d-Lactate Dehydrogenase LdhA of Burkholderia multivorans Play Roles in Carbon Overflow and in Planktonic Cellular Aggregate Formation.
Silva IN, Ramires MJ, Azevedo LA, Guerreiro AR, Tavares AC, Becker JD, Moreira LM., Appl Environ Microbiol 83(19), 2017
PMID: 28733286
The Symbiotic Performance of Chickpea Rhizobia Can Be Improved by Additional Copies of the clpB Chaperone Gene.
Paço A, Brígido C, Alexandre A, Mateos PF, Oliveira S., PLoS One 11(2), 2016
PMID: 26845770
Transcriptomic analysis of the process of biofilm formation in Rhizobium etli CFN42.
Reyes-Pérez A, Vargas Mdel C, Hernández M, Aguirre-von-Wobeser E, Pérez-Rueda E, Encarnacion S., Arch Microbiol 198(9), 2016
PMID: 27226009
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis.
Penterman J, Abo RP, De Nisco NJ, Arnold MF, Longhi R, Zanda M, Walker GC., Proc Natl Acad Sci U S A 111(9), 2014
PMID: 24501120
The Sinorhizobium meliloti EmrR regulator is required for efficient colonization of Medicago sativa root nodules.
Santos MR, Marques AT, Becker JD, Moreira LM., Mol Plant Microbe Interact 27(4), 2014
PMID: 24593245
Global mapping of transcription start sites and promoter motifs in the symbiotic α-proteobacterium Sinorhizobium meliloti 1021.
Schlüter JP, Reinkensmeier J, Barnett MJ, Lang C, Krol E, Giegerich R, Long SR, Becker A., BMC Genomics 14(), 2013
PMID: 23497287
Next-generation annotation of prokaryotic genomes with EuGene-P: application to Sinorhizobium meliloti 2011.
Sallet E, Roux B, Sauviac L, Jardinaud MF, Carrère S, Faraut T, de Carvalho-Niebel F, Gouzy J, Gamas P, Capela D, Bruand C, Schiex T., DNA Res 20(4), 2013
PMID: 23599422
Adaptation of Pseudomonas aeruginosa to a pulsed light-induced stress.
Massier S, Rincé A, Maillot O, Feuilloley MG, Orange N, Chevalier S., J Appl Microbiol 112(3), 2012
PMID: 22188372
Dual RpoH sigma factors and transcriptional plasticity in a symbiotic bacterium.
Barnett MJ, Bittner AN, Toman CJ, Oke V, Long SR., J Bacteriol 194(18), 2012
PMID: 22773790
Sinorhizobium meliloti sigma factors RpoE1 and RpoE4 are activated in stationary phase in response to sulfite.
Bastiat B, Sauviac L, Picheraux C, Rossignol M, Bruand C., PLoS One 7(11), 2012
PMID: 23226379
A ClpB chaperone knockout mutant of Mesorhizobium ciceri shows a delay in the root nodulation of chickpea plants.
Brígido C, Robledo M, Menéndez E, Mateos PF, Oliveira S., Mol Plant Microbe Interact 25(12), 2012
PMID: 23134119
Mechanism of acid tolerance in a rhizobium strain isolated from Pueraria lobata (Willd.) Ohwi.
Lei Z, Jian-ping G, Shi-qing W, Ze-yang Z, Chao Z, Yongxiong Y., Can J Microbiol 57(6), 2011
PMID: 21635219

65 References

Daten bereitgestellt von Europe PubMed Central.

Eubacterial sigma-factors.
Wosten MM., FEMS Microbiol. Rev. 22(3), 1998
PMID: 9818380
Multiple sigma subunits and the partitioning of bacterial transcription space.
Gruber TM, Gross CA., Annu. Rev. Microbiol. 57(), 2003
PMID: 14527287
Molecular chaperones in cellular protein folding.
Hartl FU., Nature 381(6583), 1996
PMID: 8637592
Small heat shock proteins are molecular chaperones.
Jakob U, Gaestel M, Engel K, Buchner J., J. Biol. Chem. 268(3), 1993
PMID: 8093612
The heat shock response of Escherichia coli.
Arsene F, Tomoyasu T, Bukau B., Int. J. Food Microbiol. 55(1-3), 2000
PMID: 10791710
Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response.
Guisbert E, Yura T, Rhodius VA, Gross CA., Microbiol. Mol. Biol. Rev. 72(3), 2008
PMID: 18772288
Regulation of the heat-shock response.
Yura T, Nakahigashi K., Curr. Opin. Microbiol. 2(2), 1999
PMID: 10322172
An RpoH-like heat shock sigma factor is involved in stress response and virulence in Brucella melitensis 16M.
Delory M, Hallez R, Letesson JJ, De Bolle X., J. Bacteriol. 188(21), 2006
PMID: 16936018
Acid shock proteins of Escherichia coli.
Heyde M, Portalier R., FEMS Microbiol. Lett. 57(1-2), 1990
PMID: 2199304
The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses.
Martinez-Salazar JM, Sandoval-Calderon M, Guo X, Castillo-Ramirez S, Reyes A, Loza MG, Rivera J, Alvarado-Affantranger X, Sanchez F, Gonzalez V, Davila G, Ramirez-Romero MA., Microbiology (Reading, Engl.) 155(Pt 2), 2009
PMID: 19202087
Surviving heat shock: control strategies for robustness and performance.
El-Samad H, Kurata H, Doyle JC, Gross CA, Khammash M., Proc. Natl. Acad. Sci. U.S.A. 102(8), 2005
PMID: 15668395
Genes and signals in the rhizobium-legume symbiosis.
Long SR., Plant Physiol. 125(1), 2001
PMID: 11154299
Bacteroid formation in the Rhizobium-legume symbiosis.
Oke V, Long SR., Curr. Opin. Microbiol. 2(6), 1999
PMID: 10607628
Root nodulation and infection factors produced by rhizobial bacteria.
Spaink HP., Annu. Rev. Microbiol. 54(), 2000
PMID: 11018130
Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti.
Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S., DNA Res. 7(6), 2000
PMID: 11214968
Three disparately regulated genes for sigma 32-like transcription factors in Bradyrhizobium japonicum.
Narberhaus F, Krummenacher P, Fischer HM, Hennecke H., Mol. Microbiol. 24(1), 1997
PMID: 9140968
The composite genome of the legume symbiont Sinorhizobium meliloti.
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, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J., Science 293(5530), 2001
PMID: 11474104
Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti.
Oke V, Rushing BG, Fisher EJ, Moghadam-Tabrizi M, Long SR., Microbiology (Reading, Engl.) 147(Pt 9), 2001
PMID: 11535780
Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti.
Ono Y, Mitsui H, Sato T, Minamisawa K., Mol. Gen. Genet. 264(6), 2001
PMID: 11254138
Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa.
Mitsui H, Sato T, Sato Y, Ito N, Minamisawa K., Mol. Genet. Genomics 271(4), 2004
PMID: 15007732
Acid tolerance in root nodule bacteria.
Glenn AR, Reeve WG, Tiwari RP, Dilworth MJ., Novartis Found. Symp. 221(), 1999
PMID: 10207916
Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions
AUTHOR UNKNOWN, 1992
Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici Umr1899
AUTHOR UNKNOWN, 1994
Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti.
Lynch D, O'Brien J, Welch T, Clarke P, Cuiv PO, Crosa JH, O'Connell M., J. Bacteriol. 183(8), 2001
PMID: 11274118
Universal chemical assay for the detection and determination of siderophores.
Schwyn B, Neilands JB., Anal. Biochem. 160(1), 1987
PMID: 2952030
Regulation of succinoglycan and galactoglucan biosynthesis in Sinorhizobium meliloti.
Becker A, Ruberg S, Baumgarth B, Bertram-Drogatz PA, Quester I, Puhler A., J. Mol. Microbiol. Biotechnol. 4(3), 2002
PMID: 11931545
Sensory transduction to the flagellar motor of Sinorhizobium meliloti.
Scharf B, Schmitt R., J. Mol. Microbiol. Biotechnol. 4(3), 2002
PMID: 11931544
Probing for pH-regulated proteins in Sinorhizobium medicae using proteomic analysis.
Reeve WG, Tiwari RP, Guerreiro N, Stubbs J, Dilworth MJ, Glenn AR, Rolfe BG, Djordjevic MA, Howieson JG., J. Mol. Microbiol. Biotechnol. 7(3), 2004
PMID: 15263818
The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions.
Reeve WG, Brau L, Castelli J, Garau G, Sohlenkamp C, Geiger O, Dilworth MJ, Glenn AR, Howieson JG, Tiwari RP., Microbiology (Reading, Engl.) 152(Pt 10), 2006
PMID: 17005985
New substrates for the dicarboxylate transport system of Sinorhizobium meliloti.
Yurgel S, Mortimer MW, Rogers KN, Kahn ML., J. Bacteriol. 182(15), 2000
PMID: 10894729
Sinorhizobium meliloti 1021 loss-of-function deletion mutation in chvI and its phenotypic characteristics.
Wang C, Kemp J, Da Fonseca IO, Equi RC, Sheng X, Charles TC, Sobral BW., Mol. Plant Microbe Interact. 23(2), 2010
PMID: 20064059
The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon.
Suziedeliene E, Suziedelis K, Garbenciute V, Normark S., J. Bacteriol. 181(7), 1999
PMID: 10094685
A genomic perspective on protein families.
Tatusov RL, Koonin EV, Lipman DJ., Science 278(5338), 1997
PMID: 9381173
GrpE, a nucleotide exchange factor for DnaK.
Harrison C., Cell Stress Chaperones 8(3), 2003
PMID: 14984054
Multiple small heat shock proteins in rhizobia.
Munchbach M, Nocker A, Narberhaus F., J. Bacteriol. 181(1), 1999
PMID: 9864316
Effects of organic acids and low pH on Rhizobium meliloti 104A14.
Perez-Galdona R, Kahn ML., Microbiology (Reading, Engl.) 140 ( Pt 5)(), 1994
PMID: 8025689
Escherichia coli acid resistance: tales of an amateur acidophile.
Foster JW., Nat. Rev. Microbiol. 2(11), 2004
PMID: 15494746
Sinorhizobium meliloti rpoE2 is necessary for H(2)O(2) stress resistance during the stationary growth phase.
Flechard M, Fontenelle C, Trautwetter A, Ermel G, Blanco C., FEMS Microbiol. Lett. 290(1), 2008
PMID: 19025578
A sigma54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene.
Janaszak A, Majczak W, Nadratowska B, Szalewska-Palasz A, Konopa G, Taylor A., Microbiology (Reading, Engl.) 153(Pt 1), 2007
PMID: 17185540
Exploring the metabolic and genetic control of gene expression on a genomic scale.
DeRisi JL, Iyer VR, Brown PO., Science 278(5338), 1997
PMID: 9381177

AUTHOR UNKNOWN, 1989
R factor transfer in Rhizobium leguminosarum.
Beringer JE., J. Gen. Microbiol. 84(1), 1974
PMID: 4612098

AUTHOR UNKNOWN, 1970
Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression.
Ruberg S, Tian ZX, Krol E, Linke B, Meyer F, Wang Y, Puhler A, Weidner S, Becker A., J. Biotechnol. 106(2-3), 2003
PMID: 14651866
EMMA: a platform for consistent storage and efficient analysis of microarray data.
Dondrup M, Goesmann A, Bartels D, Kalinowski J, Krause L, Linke B, Rupp O, Sczyrba A, Puhler A, Meyer F., J. Biotechnol. 106(2-3), 2003
PMID: 14651856
Sinorhizobium meliloti 1021 Sm14kOLI
AUTHOR UNKNOWN, 0
Genesis: cluster analysis of microarray data.
Sturn A, Quackenbush J, Trajanoski Z., Bioinformatics 18(1), 2002
PMID: 11836235
EMMA server
AUTHOR UNKNOWN, 0
Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants.
Grant SG, Jessee J, Bloom FR, Hanahan D., Proc. Natl. Acad. Sci. U.S.A. 87(12), 1990
PMID: 2162051
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