Sinorhizobium meliloti mutants lacking phosphotransferase system enzyme HPr or EIIA are altered in diverse processes, including carbon metabolism, cobalt requirements, and succinoglycan production

Journal of Bacteriology

Volumn 190, Issue 8, 2008, Pages 2947-2956

  Pinedo, Catalina Arango ^a   Bringhurst, Ryan M ^a   Gage, Daniel J ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; COBALT; CYCLIC AMP BINDING PROTEIN; NITROGEN; PHOSPHOTRANSFERASE; PROTEIN HPR; PROTEIN MANX; SUCCINOGLYCAN; UNCLASSIFIED DRUG;

ALFALFA; ARTICLE; BACTERIAL GENE; CARBOHYDRATE SYNTHESIS; CARBON METABOLISM; ENZYME DEFICIENCY; GENE DELETION; GENE REPRESSION; MUTANT; NODULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SINORHIZOBIUM MELILOTI; WILD TYPE;

BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CARBON; COBALT; GENE DELETION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MEDICAGO SATIVA; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; POLYSACCHARIDES, BACTERIAL; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

ALPHAPROTEOBACTERIA; MEDICAGO SATIVA; PUFFINUS AURICULARIS; SINORHIZOBIUM MELILOTI;

EID: 41949090827     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01917-07     Document Type: Article

References (75)

1. Almengor, A. C., T. L. Kinkel, S. J. Day, and K. S. McIver. 2007. The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the group A streptococcus. J. Bacteriol. 189:8405-8416.
2. Asanuma, N., and T. Hino. 2003. Molecular characterization of HPr and related enzymes, and regulation of HPr phosphorylation in the ruminal bacterium Streptococcus bovis. Arch. Microbiol. 179:205-213.
3. Barabote, R. D., and M. H. Saier, Jr. 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608-634.
4. Barnett, M. J., R. F. Fisher, T. Jones, C. Komp, A. P. Abola, F. Barloy-Hubler, L. Bowser, D. Capela, F. Galibert, J. Gouzy, M. Gurjal, A. Hong, L. Huizar, R. W. Hyman, D. Kahn, M. L. Kahn, S. Kalman, D. H. Keating, C. Palm, M. C. Peck, R. Surzycki, D. H. Wells, K. C. Yeh, R. W. Davis, N. A. Federspiel, and S. R. Long. 2001. Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc. Natl. Acad. Sci. USA 98:9883-9888.
5. Barnett, M. J., V. Oke, and S. R. Long. 2000. New genetic tools for use in the Rhizobiaceae and other bacteria. Bio/Technology 29:240-242, 244-245.
6. Barra, L., C. Fontenelle, G. Ermel, A. Trautwetter, G. C. Walker, and C. Blanco. 2006. Interrelations between glycine betaine catabolism and methionine biosynthesis in Sinorhizobium meliloti strain 102F34. J. Bacteriol. 188:7195-7204.
7. Bergersen, F. J., and G. L. Turner. 1967. Nitrogen fixation by the bacteroid fraction of breis of soybean root nodules. Biochim. Biophys. Acta 141:507-515.
8. Boel, G., I. Mijakovic, A. Maze, S. Poncet, M. K. Taha, M. Larribe, E. Darbon, A. Khemiri, A. Galinier, and J. Deutscher. 2003. Transcription regulators potentially controlled by HPr kinase/phosphorylase in Gram-negative bacteria. J. Mol. Microbiol. Biotechnol. 5:206-215.
9. Brewin, N. J. 1991. Development of the legume root nodule. Annu. Rev. Cell Biol. 7:191-226.
10. Bringhurst, R. M., Z. G. Cardon, and D. J. Gage. 2001. Galactosides in the rhizosphere: utilization by Sinorhizobium meliloti and development of a biosensor. Proc. Natl. Acad. Sci. USA 98:4540-4545.
11. Bringhurst, R. M., and D. J. Gage. 2002. Control of inducer accumulation plays a key role in succinate-mediated catabolite repression in Sinorhizobium meliloti. J. Bacteriol. 184:5385-5392.
12. Brückner, R., and F. Titgemeyer. 2002. Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol. Lett. 209:141-148.
13. Campbell, G. R., M. E. Taga, K. Mistry, J. Lloret, P. J. Anderson, J. R. Roth, and G. C. Walker. 2006. Sinorhizobium meliloti bluB is necessary for production of 5,6-dimethylbenzimidazole, the lower ligand of B12. Proc. Natl. Acad. Sci. USA 103:4634-4639.
14. Capela, D., F. Barloy-Hubler, J. Gouzy, G. Bothe, F. Ampe, J. Batut, P. Boistard, A. Becker, M. Boutry, E. Cadieu, S. Dreano, S. Gloux, T. Godrie, A. Goffeau, D. Kahn, E. Kiss, V. Lelaure, D. Masuy, T. Pohl, D. Portetelle, A. Puhler, B. Purnelle, U. Ramsperger, C. Renard, P. Thebault, M. Vandenbol, S. Weidner, and F. Galibert. 2001. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. USA 98:9877-9882.
15. Cheng, H. P., and G. C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:5183-5191.
16. Cormack, B. P., R. H. Valdivia, and S. Falkow. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
17. 12 coenzyme-dependent ribonucleotide reductase in Rhizobium species and the effects of cobalt deficiency on the activity of the enzyme. J. Bacteriol. 97:1460-1465.
18. Dehertogh, A. A., P. A. Mayeux, and H. J. Evans. 1964. The relationship of cobalt requirement to propionate metabolism in Rhizobium. J. Biol. Chem. 239:2446-2453.
19. Denarie, J., F. Debelle, and J. C. Prome. 1996. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65:503-535.
20. Deutscher, J., C. Francke, and P. W. Postma. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939-1031.
21. Deutscher, J., R. Herro, A. Bourand, I. Mijakovic, and S. Poncet. 2005. P-Ser-HPr - a link between carbon metabolism and the virulence of some pathogenic bacteria. Biochim. Biophys. Acta 1754:118-125.
22. Deutscher, J., E. Kuster, U. Bergstedt, V. Charrier, and W. Hillen. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol. Microbiol. 15:1049-1053.
23. Egelhoff, T. T., and S. R. Long. 1985. Rhizobium meliloti nodulation genes: identification of nodDABC gene products, purification of nodA protein, and expression of nodA in Rhizobium meliloti. J. Bacteriol. 164:591-599.
24. Erni, B., B. Zanolari, P. Graff, and H. P. Kocher. 1989. Mannose permease of Escherichia coli. Domain structure and function of the phosphorylating subunit. J. Biol. Chem. 264:18733-18741.
25. 2-fixing endosymbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 98:9889-9894.
26. Finan, T. M., J. M. Wood, and D. C. Jordan. 1983. Symbiotic properties of C4-dicarboxylic acid transport mutants of Rhizobium leguminosarum. J. Bacteriol. 154:1403-1413.
27. Gage, D. J., T. Bobo, and S. R. Long. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:7159-7166.
28. Gardiol, A. 1982. Succinate dehydrogenase mutant of Rhizobium meliloti. J. Bacteriol. 151:1621-1623.
29. Gilbreth, S. E., A. K. Benson, and R. W. Hutkins. 2004. Catabolite repression and virulence gene expression in Listeria monocytogenes. Curr. Microbiol. 49:95-98.
30. Glenn, A. R., P. S. Poole, and J. F. Hudman. 1980. Succinate uptake by free-living and bacteroid forms of Rhizobium leguminosarum. J. Gen. Microbiol. 119:267-271.
31. Gonzalez, J. E., B. L. Reuhs, and G. C. Walker. 1996. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:8636-8641.
32. Gulati, A., and S. Mahadevan. 2000. Mechanism of catabolite repression in the bgl operon of Escherichia coli: involvement of the anti-terminator BglG, CRP-cAMP and EIIAGlc in mediating glucose effect downstream of transcription initiation. Genes Cells 5:239-250.
33. Hester, K. L., K. T. Madhusudhan, and J. R. Sokatch. 2000. Catabolite repression control by Crc in 2xYT medium is mediated by posttranscriptional regulation of bkdR expression in Pseudomonas putida. J. Bacteriol. 182:1150-1153.
34. Hirsch, A. M. 1992. Developmental biology of legume nodulation. New Phytol. 122:211-237.
35. Hondorp, E. R., and K. S. McIver. 2007. The Mga virulence regulon: infection where the grass is greener. Mol. Microbiol. 66:1056-1065.
36. Hornez, J.-P., M. Timinouni, C. Defives, and J.-C. Derieux. 1994. Unaffected nodulation and nitrogen fixation in carbohydrate pleiotropic mutants of Rhizobium meliloti. Curr. Microbiol. 28:225-229.
37. Hu, K.-Y., and M. J. Saier. 2002. Phylogeny of phosphoryl transfer proteins of the phosphoenolpyruvate-dependent sugar-transporting phosphotransferase system. Res. Microbiol. 153:405-415.
38. Inada, T., K. Kimata, and H. Aiba. 1996. Mechanism responsible for glucose-lactose diauxie in Escherichia coli: challenge to the cAMP model. Genes Cells 1:293-301.
39. Jelesko, J. G., and J. A. Leigh. 1994. Genetic characterization of a Rhizobium meliloti lactose utilization locus. Mol. Microbiol. 11:165-173.
40. Kimata, K., H. Takahashi, T. Inada, P. Postma, and H. Aiba. 1997. cAMP receptor protein-cAMP plays a crucial role in glucose-lactose diauxie by activating the major glucose transporter gene in Escherichia coli. Proc. Natl. Acad. Sci. USA 94:12914-12919.
41. Kraus, A., E. Kuster, A. Wagner, K. Hoffmann, and W. Hillen. 1998. Identification of a co-repressor binding site in catabolite control protein CcpA. Mol. Microbiol. 30:955-963.
42. Kravanja, M., R. Engelmann, V. Dossonnet, M. Bluggel, H. E. Meyer, R. Frank, A. Galinier, J. Deutscher, N. Schnell, and W. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol. Microbiol. 31:59-66.
43. Kuroda, M., T. H. Wilson, and T. Tsuchiya. 2001. Regulation of galactoside transport by the PTS. J. Mol. Microbiol. Biotechnol. 3:381-384.
44. + transporter TrkA. Proc. Natl. Acad. Sci. USA 104:4124-4129.
45. Leigh, J. A., E. R. Signer, and G. C. Walker. 1985. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:6231-6235.
46. Long, S. R. 1996. Rhizobium symbiosis: nod factors in perspective. Plant Cell 8:1885-1898.
47. MacGregor, C. H., S. K. Arora, P. W. Hager, M. B. Dail, and P. V. Phibbs, Jr. 1996. The nucleotide sequence of the Pseudomonas aeruginosa pyrE-crc- rph region and the purification of the crc gene product. J. Bacteriol. 178:5627-5635.
48. Matthews, R. G. 2001. Cobalamin-dependent methyltransferases. Acc. Chem. Res. 34:681-689.
49. Mijakovic, I., S. Poncet, A. Galinier, V. Monedero, S. Fieulaine, J. Janin, S. Nessler, J. A. Marquez, K. Scheffzek, S. Hasenbein, W. Hengstenberg, and J. Deutscher. 2002. Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc. Natl. Acad. Sci. USA 99:13442-13447.
50. Miller, J. H. (ed.). 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
51. Monedero, V., O. P. Kuipers, E. Jamet, and J. Deutscher. 2001. Regulatory functions of serine-46-phosphorylated HPr in Lactococcus lactis. J. Bacteriol. 183:3391-3398.
52. Moreno, R., A. Ruiz-Manzano, L. Yuste, and F. Rojo. 2007. The Pseudomonas putida Crc global regulator is an RNA binding protein that inhibits translation of the AlkS transcriptional regulator. Mol. Microbiol. 64:665-675.
53. Mylona, P., K. Pawlowski, and T. Bisseling. 1995. Symbiotic nitrogen fixation. Plant Cell 7:869-885.
54. Nessler, S., S. Fieulaine, S. Poncet, A. Galinier, J. Deutscher, and J. Janin. 2003. HPr kinase/phosphorylase, the sensor enzyme of catabolite repression in gram-positive bacteria: structural aspects of the enzyme and the complex with its protein substrate. J. Bacteriol. 185:4003-4010.
55. Pellock, B. J., H. P. Cheng, and G. C. Walker. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:4310-4318.
56. Plamondon, P., D. Brochu, S. Thomas, J. Fradette, L. Gauthier, K. Vaillancourt, N. Buckley, M. Frenette, and C. Vadeboncoeur. 1999. Phenotypic consequences resulting from a methionine-to-valine substitution at position 48 in the HPr protein of Streptococcus salivarius. J. Bacteriol. 181:6914-6921.
57. Poole, P. S., A. Blyth, C. J. Reid, and K. Walters. 1994. myo-Inositol catabolism and catabolite repression in Rhizobium leguminosarum bv. viciae. Microbiology 140:2787-2795.
58. Powell, B. S., D. L. Court, T. Inada, Y. Nakamura, V. Michotey, X. Cui, A. Reizer, M. H. Saier, Jr., and J. Reizer. 1995. Novel proteins of the phosphotransferase system encoded within the rpoN operon of Escherichia coli. Enzyme IIANtr affects growth on organic nitrogen and the conditional lethality of an erats mutant. J. Biol. Chem. 270:4822-4839.
59. Reed, J. W., J. Glazebrook, and G. C. Walker. 1991. The exoR gene of Rhizobium meliloti affects RNA levels of other exo genes but lacks homology to known transcriptional regulators. J. Bacteriol. 173:3789-3794.
60. Reizer, J., C. Hoischen, F. Titgemeyer, C. Rivolta, R. Rabus, J. Stulke, D. Karamata, M. H. Saier, Jr., and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:1157-1169.
61. Reizer, J., S. L. Sutrina, M. H. Saier, G. C. Stewart, A. Peterkofsky, and P. Reddy. 1989. Mechanistic and physiological consequences of HPr(ser) phosphorylation on the activities of the phosphoenolpyruvate:sugar phosphotransferase system in gram-positive bacteria: studies with site-specific mutants of HPr. EMBO J. 8:2111-2120.
62. Ronson, C. W., and P. M. Astwood. 1985. Genes involved in the carbon metabolism of bacteroids, p. 201-207. In H. J. Evan, P. J. Bottomley, and W. E. Newton (ed.), Nitrogen fixation research progress. Martinus Nijoff Publishers, Dordrecht, The Netherlands.
63. Ronson, C. W., P. M. Astwood, and J. A. Downie. 1984. Molecular cloning and genetic organization of C4-dicarboxylate transport genes from Rhizobium leguminosarum. J. Bacteriol. 160:903-909.
64. Rosado, M., and D. J. Gage. 2003. A gfp reporter for monitoring rRNA synthesis and growth rate of the nodulating symbiont Sinorhizobium meliloti: use in the laboratory and in a model complex environment, the rhizosphere. FEMS Microbiol. Lett. 226:15-22.
65. Saier, M. J. 1998. Multiple mechanisms controlling carbon metabolism in bacteria. Biotechnol. Bioeng. 58:170-174.
66. Spaink, H. P. 1995. The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33:345-368.
67. Stulke, J., and W. Hillen. 1999. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2:195-201.
68. Tsvetanova, B., A. C. Wilson, C. Bongiorni, C. Chiang, J. A. Hoch, and M. Perego. 2007. Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis. Mol. Microbiol. 63:644-655.
69. Ucker, D. S. 1978. Catabolite repression-like phenomenon in Rhizobium meliloti. J. Bacteriol. 136:1197-1200.
70. Velazquez, F., K. Pfluger, I. Cases, L. I. De Eugenio, and V. de Lorenzo. 2007. The phosphotransferase system formed by PtsP, PtsO, and PtsN proteins controls production of polyhydroxyalkanoates in Pseudomonas putida. J. Bacteriol. 189:4529-4533.
71. Viana, R., V. Monedero, V. Dossonnet, C. Vadeboncoeur, G. Perez-Martinez, and J. Deutscher. 2000. Enzyme I and HPr from Lactobacillus casei: their role in sugar transport, carbon catabolite repression and inducer exclusion. Mol. Microbiol. 36:570-584.
72. Warner, J. B., and J. S. Lolkema. 2003. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
73. Watson, R. J., R. Heys, T. Martin, and M. Savard. 2001. Sinorhizobium meliloti cells require biotin and either cobalt or methionine for growth. Appl. Environ. Microbiol. 67:3767-3770.
74. Yao, S. Y., L. Luo, K. J. Har, A. Becker, S. Ruberg, G. Q. Yu, J. B. Zhu, and H. P. Cheng. 2004. Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J. Bacteriol. 186:6042-6049.
75. York, G. M., and G. C. Walker. 1997. The Rhizobium meliloti exoK gene and prsD/prsE/exsH genes are components of independent degradative pathways which contribute to production of low-molecular-weight succinoglycan. Mol. Microbiol. 25:117-134.