Expression of the Rhizobium leguminosarum bv. trifolii pssA gene, involved in Exopolysaccharide synthesis, is regulated by RosR, phosphate, and the carbon source

Journal of Bacteriology

Volumn 195, Issue 15, 2013, Pages 3412-3423

  Urbanik Sypniewska, Teresa ^a   Janczarek, Monika ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBON; CRP PROTEIN; CYAA PROTEIN; CYCLIC AMP BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; EXOPOLYSACCHARIDE; GLUCOSE; IRON; MUTANT PROTEIN; PHOB PROTEIN; PHOSPHATE; PSSA PROTEIN; REGULATOR PROTEIN; ROSR PROTEIN; SIGMA FACTOR; SIGMA FACTOR DELTA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CARBON SOURCE; CONTROLLED STUDY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; GENE INSERTION; GENE SEQUENCE; INVERTED REPEAT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; RHIZOBIUM LEGUMINOSARUM; TRANSCRIPTION INITIATION; WILD TYPE;

ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BASE SEQUENCE; BETA-GALACTOSIDASE; BINDING SITES; CARBON; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GLYCOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PHOSPHATES; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; RHIZOBIUM LEGUMINOSARUM; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84880681671     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02213-12     Document Type: Article

References (60)

1. Cooper JE. 2007. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J. Appl. Microbiol. 103:1355-1365.
2. Downie JA. 2010. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol. Rev. 34:150-170.
3. Rolfe BG, Carlson RW, Ridge RW, Dazzo RW, Mateos FB, Pankhurst CE. 1996. Defective infection and nodulation of clovers by exopolysaccharide mutants of Rhizobium leguminosarum bv. trifolii. Aust. J. Plant Physiol. 23:285-303.
4. van Workum WA, Canter Cremers HCJ, Wijfjes AHM, Van der Kolk C, Wijffelman CA, Kijne JW. 1997. Cloning and characterization of four genes of Rhizobium leguminosarum bv. trifolii involved in exopolysaccharide production and nodulation. Mol. Plant Microbe Interact. 10:290-301.
5. Janczarek M, Jaroszuk-Ścisel J, Skorupska A. 2009. Multiple copies of rosR and pssA genes enhance exopolysaccharide production, symbiotic competitiveness and clover nodulation in Rhizobium leguminosarum bv. trifolii. Antonie Van Leeuwenhoek 96:471-486.
6. Janczarek M. 2011. Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int. J. Mol. Sci. 12:7898-7933.
7. Borthakur D, Barker RF, Latchford JW, Rossen L, Johnston AWB. 1988. Analysis of pss genes of Rhizobium leguminosarum required for exopolysaccharide synthesis and nodulation of peas: their primary structure and their interaction with psi and other nodulation genes. Mol. Gen. Genet. 213:155-162.
8. Ivashina T, Khmelnitsky MI, Shlyapnikov MG, Kanapin AA, Ksenzenko VN. 1994. The pss4 gene from Rhizobium leguminosarum biovar viciae VF39: cloning, sequence and the possible role in polysaccharide production and nodule formation. Gene 150:111-116.
9. Janczarek M, Król J, Kutkowska J, Mazur A, Wielbo J, Borucki W, Kopcińska J, Lotocka B, Urbanik Sypniewska T, Skorupska A. 2001. Mutation in the pssB-pssA intergenic region of Rhizobium leguminosarum bv. trifolii affects the surface polysaccharide synthesis and nitrogen fixation ability. J. Plant Physiol. 158:1565-1574.
10. Król JE, Mazur A, Marczak M, Skorupska A. 2007. Syntenic arrangements of the surface polysaccharide biosynthesis genes in Rhizobium leguminosarum. Genomics 89:237-247.
11. Pollock TJ, Workum WA, Thorne L, Mikolajczak MJ, Yamazaki M, Kijne JW, Armentrout RW. 1998. Assignment of biochemical functions to glycosyl transferase genes which are essential for biosynthesis of exopolysaccharides in Sphingomonas strain S88 and Rhizobium leguminosarum. J. Bacteriol. 180:586-593.
12. Ivashina TV, Fedorova EE, Ashina NP, Kalinchuk NA, Druzhinina TN, Shashkov AS, Shibaev VN, Ksenzenko VN. 2010. Mutation in the pssM gene encoding ketal pyruvate transferase leads to disruption of Rhizobium leguminosarum bv. viciae-Pisum sativum symbiosis. J. Appl. Microbiol. 109:731-742.
13. Borthakur D, Johnston AWB. 1987. Sequence of psi, a gene of the symbiotic plasmid of Rhizobium phaseoli which inhibits exopolysaccharide synthesis and nodulation and demonstration that its transcription is inhibited by psr, another gene on the symbiotic plasmid. Mol. Gen. Genet. 207:149-154.
14. Latchford JW, Borthakur D, Johnston AWB. 1991. The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface. Mol. Microbiol. 5:2107-2114.
15. Mimmack ML, Hong GF, Johnston AWB. 1994. Sequence and regulation of psrA, a gene on the Sym plasmid of Rhizobium leguminosarum biovar phaseoli which inhibits transcription of the psi genes. Microbiology 140:455-461.
16. Janczarek M, Skorupska A. 2001. The Rhizobium leguminosarum bv. trifolii pssB gene product is an inositol monophosphatase that influences exopolysaccharide synthesis. Arch. Microbiol. 175:143-151.
17. Reeve WG, Dilworth MJ, Tiwari RP, Glenn AR. 1997. Regulation of exopolysaccharide production in Rhizobium leguminosarum biovar viciae WSM710 involves exoR. Microbiology 143:1951-1958.
18. Janczarek M, Skorupska A. 2007. The Rhizobium leguminosarum bv. trifolii RosR: transcriptional regulator involved in exopolysaccharide production. Mol. Plant Microbe Interact. 20:867-881.
19. Janczarek M, Skorupska A. 2009. Rhizobium leguminosarum bv. trifolii rosR gene expression is regulated by catabolic repression. FEMS Microbiol. Lett. 291:112-119.
20. Janczarek M, Skorupska A. 2011. Modulation of rosR expression and exopolysaccharide production in Rhizobium leguminosarum bv. trifolii by phosphate and clover root exudates. Int. J. Mol. Sci. 12:4132-4155.
21. Janczarek M, Skorupska A. 2004. Regulation of pssA and pssB gene expression in R. leguminosarum bv. trifolii in response to environmental factors. Antonie Van Leeuwenhoek 85:217-227.
22. Vincent JM. 1970. A manual for the practical study of root nodule bacteria. International biological program handbook 15. Blackwell Scientific Publications, Ltd., Oxford, United Kingdom.
23. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Brown CM, Dilworth MJ. 1975. Ammonia assimilation by Rhizobium cultures and bacteroids. J. Gen. Microbiol. 86:39-48.
25. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.
26. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Loewus FA. 1952. Improvement in the anthrone method for determination of carbohydrates. Anal. Chem. 24:219.
28. Wósten MM. 1998. Eubacterial sigma-factors. FEMS Microbiol. Rev. 22:127-150.
29. Browning DF, Busby SJ. 2004. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2:57-65.
30. MacLellan SR, MacLean AM, Finan TM. 2006. Promoter prediction in the rhizobia. Microbiology 152:1751-1763.
31. Todd JD, Wexler M, Sawers G, Yeoman KH, Poole PS, Johnston AWB. 2002. RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148:4059-4071.
32. Todd JD, Sawers G, Rodionov DA, Johnston AW. 2006. The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability. Mol. Genet. Genomics 275:564-577.
33. Yeoman KH, Curson AR, Todd JD, Sawers G, Johnston AWB. 2004. Evidence that the Rhizobium regulatory protein RirA binds to cis-acting iron-responsive operators (IROs) at promoters of some Fe-regulated genes. Microbiology 150:4065-4074.
34. Wielbo J, Mazur A, Krol JE, Marczak M, Skorupska A. 2004. Environmental modulation of the pssTNOP gene expression in Rhizobium leguminosarum bv. trifolii. Can. J. Microbiol. 50:1-11.
35. Cheng HP, Yao SY. 2004. The key Sinorhizobium meliloti succinoglycan biosynthesis gene exoY is expressed from two promoters. FEMS Microbiol. Lett. 231:131-136.
36. Quester I, Becker A. 2004. Four promoters subject to regulation by ExoR and PhoB direct transcription of the Sinorhizobium meliloti exoYFQ operon involved in the biosynthesis of succinoglycan. J. Mol. Microbiol. Biotechnol. 7:115-132.
37. 2+ targets the mgtA transcript for degradation by RNase E. FEMS Microbiol. Lett. 280:226-234.
38. Bertram-Drogatz PA, Quester I, Becker A, Pühler A. 1998. 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. 257:433-441.
39. Bieleski RL. 1973. Phosphate pools, phosphate transport and phosphate availability. Annu. Rev. Plant Physiol. 24:225-252.
40. Bardin S, Dan S, Osteras M, Finan TM. 1996. A phosphate transport system is required for symbiotic nitrogen fixation by Rhizobium meliloti. J. Bacteriol. 178:4540-4547.
41. Bahlawane C, McIntosh M, Krol E, Becker A. 2008. Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol. Plant Microbe Interact. 21:1498-1509.
42. Rüberg S, Pühler A, Becker A. 1999. Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology 145:603-611.
43. Yuan Z, Zaheer R, Morton R, Finan TM. 2006. Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res. 34:2686-2697.
44. Krol E, Becker A. 2004. Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol. Genet. Genomics 272:1-17.
45. Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Praser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7:R34. doi:10.1186/gb-2006-7-4-r34.
46. Reeve W, O'Hara G, Chain P, Ardley J, Bräu L, Nandesena K, Tiwari R, Copeland A, Nolan M, Han C, Brettin T, Land M, Ovchinikova G, Ivanova N, Mavromatis K, Markowitz V, Kyrpides N, Melino V, Denton M, Yates R, Howieson J. 2010. Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM1325, an effective microsymbiont of annual Mediterranean clovers. Stand. Genomic Sci. 2:347-356.
47. Riley M, Abe T, Arnaud MB, Berlyn MK, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett GIII, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL. 2006. Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res. 34:1-9.
48. Busby S, Ebright RH. 1999. Transcription activation by catabolite activator protein (CAP). J. Mol. Biol. 293:199-213.
49. Beatty CM, Browning DF, Busby SJW, Wolfe AJ. 2003. Cyclic AMP receptor protein-dependent activation of the Escherichia coli acsP2 promoter by a synergistic class III mechanism. J. Bacteriol. 185:5148-5157.
50. Pinedo CA, Gage DJ. 2009. HPrK regulates succinate-mediated catabolite repression in the gram negative symbiont Sinorhizobium meliloti. J. Bacteriol. 191:298-309.
51. Tellez-Sosa J, Soberon N, Vega-Segura A, Torres-Marquez ME, Cevallos MA. 2002. The Rhizobium etli cyaC product: characterization of a novel adenylate cyclase class. J. Bacteriol. 184:3560-3568.
52. Vanderlinde EM, Yost CK. 2012. Mutation of the sensor kinase chvG in Rhizobium leguminosarum negatively impacts cellular metabolism, outer membrane stability and symbiosis. J. Bacteriol. 194:768-777.
53. Janczarek M, Kutkowska J, Piersiak T, Skorupska A. 2010. Rhizobium leguminosarum bv. trifolii rosR is required for interaction with clover, biofilm formation and adaptation to the environment. BMC Microbiol. 10:284. doi:10.1186/1471-2180-10-284.
54. Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AW. 2001. The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol. Microbiol. 41:801-816.
55. Wexler M, Todd JD, Kolade O, Bellini D, Hemmings AM, Sawers G, Johnston AWB. 2003. Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149:1357-1365.
56. Charles TC, Newcomb W, Finan TM. 1991. ndvF, a novel locus located on megaplasmid pRmeSU47b (pExo) of Rhizobium meliloti, is required for normal nodule development. J. Bacteriol. 173:3981-3992.
57. Gaal T, Bartlett MS, Ross W, Turnbough JCL, Gourse RL. 1997. Transcription regulation by initiatingNTPconcentration: rRNA synthesis in bacteria. Science 278:2092-2097.
58. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gramnegative bacteria. Nat. Biotechnol. 1:784-791.
59. Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ. 1987. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol. Biol. 9:27-39.
60. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic resistance cassettes. Gene 166:175-176.