Exopolysaccharide synthesis in Rhizobium leguminosarum bv. trifolii is related to various metabolic pathways

Research in Microbiology

Volumn 154, Issue 6, 2003, Pages 433-442

  Janczarek, Monika ^a   Skorupska, Anna ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

Exopolysaccharide production; pssA gene product; Rhizobium; Suppression of exo mutations; Transposon Tn5 mutagenesis

Indexed keywords

POLYSACCHARIDE;

ARTICLE; BACTERIAL METABOLISM; BIOSYNTHESIS; CONTROLLED STUDY; GENE DISRUPTION; GENE FUNCTION; GENE INSERTION; GENE LOCATION; GENE REPRESSION; GENE SEQUENCE; GENETIC CODE; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMID; PRIORITY JOURNAL; RHIZOBIUM LEGUMINOSARUM; SYMBIOSIS; TRANSPOSON;

INSERTION SEQUENCES; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM LEGUMINOSARUM BV. TRIFOLII; TRANSPOSON TN5; TRANSPOSONS; TRIFOLIUM;

EID: 0043209023     PISSN: 09232508     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0923-2508(03)00113-X     Document Type: Article

References (59)

1. Angerer A., Gaisser S., Braun V. Nucleotide sequences of the sfuA, sfuB and sfuC genes of Serratia marcescens suggest a periplasmic-binding-protein-dependent iron transport mechanism. J. Bacteriol. 172:1990;572-578.
2. Barnett M.J., Fisher R.F., Jones T., Komp C., Abola A.P., Barloy-Hubler F., Bowser L., Capela D., Galibert F., Gouzy J., Gurjal M., Hong A., Huizar L., Hyman R.W., Kahn D., Kahn M.L., Kalman S., Keating D.H., Palm C., Peck M.C., Surzycki R., Wells D.H., Yeh K.C., Davis R.W., Federspiel N.A., Long S.R. Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc. Natl. Acad. Sci. USA. 98:2001;9883-9888.
3. Becker A., Pühler A. Production of exopolysaccharides. Spaink H.P., Kondorosi A., Hooykaas P.J.J. Rhizobiaceae. 1998;97-118 Kluwer Academic, Dordrecht, Boston, London.
4. Bertram-Drogatz P.A., Quester I., Becker A., Pühler 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. 257:1998;433-441.
5. Bessman M.J., Frick D.N., O'Handley S.F. The MutT proteins or « Nudix » hydrolases, a family of versatile, widely distributed, « housecleaning » enzymes. J. Biol. Chem. 271:1996;25059-25062.
6. Bittinger M.A., Handelsman J. Identification of genes in the RosR regulon of Rhizobium etli. J. Bacteriol. 182:2000;1706-1713.
7. Bialek U., Skorupska A., Yang W.C., Bisseling T., Van Lammeren A.A.M. Disturbed gene expression and bacterial development in Trifolium pratense root nodules induced by a Tn5 mutant in exopolysaccharide synthesis. Planta. 197:1995;184-192.
8. Borthakur D., Barker C.E., Lamb J.W., Daniels M.J., Downie J.A., Johnston A.W.B. A mutation that blocks exopolysaccharide synthesis prevents nodulation of peas by Rhizobium leguminosarum but not of beans by R. phaseoli and is corrected by cloned DNA from Rhizobium or the phytopathogen Xanthomonas. Mol. Gen. Genet. 203:1986;320-323.
9. Borthakur D., Barker R.F., Latchford J.W., Rossen L., Johnston A.W.B. Analysis of pss genes in 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. 213:1988;155-162.
10. Borthakur D., Johnston A.W.B. 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. 207:1987;149-154.
11. Bossio J.C., Semino C.E., Inon de Iannino N., Dankert M.A. The in vitro biosynthesis of the exopolysaccharide produced by Rhizobium leguminosarum bv. trifolii, strain NA30. Cell. Mol. Biol. 42:1996;737-758.
12. Canter Cremers H.C.J., Batley M., Redmond J.W., Eysdems L., Breedveld M.W., Zevenhuizen L.P.T.M., Pees E., Wijffelman C.A., Lugtenberg B.J.J. Rhizobium leguminosarum exoB mutants are deficient in the synthesis of UDP-glucose 4 ′ -epimerase. J. Biol. Chem. 265:1990;21122-21127.
13. Capela D., Barloy-Hubler F., Gouzy J., Bothe G., Ampe F., Batut J., Boistard P., Becker A., Boutry M., Cadieu E., Dreano S., Gloux S., Godrie T., Goffeau A., Kahn D., Kiss E., Lelaure V., Masuy D., Pohl T., Portetelle D., Pühler A., Purnelle B., Ramsperger U., Renard C., Thebault P., Vandenbol M., Weidner S., Galibert F. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. USA. 98:2001;9877-9882.
14. Ditta G., Stanfield S., Corbin D., Helinski D.R. Broad host range DNA cloning system for Gram-negative bacteria: Construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA. 77:1980;347-351.
15. Djordjevic S.P., Chen H., Batley M., Redmond J.W., Rolfe B.G. Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by addition of homologous exopolysaccharides. J. Bacteriol. 169:1987;53-60.
16. D'Souza-Ault M.R., Cooley M.B., Kado C.I. Analysis of the Ros repressor of Agrobacterium virC and virD operons: Molecular intercommunication between plasmid and chromosomal genes. J. Bacteriol. 175:1993;3486-3490.
17. Dunn C.A., O'Handley S.F., Frick D.N., Bessman M.J. Studies on the ADP-ribose pyrophosphatase subfamily of the nudix hydrolases and tentative identification of trgB, a gene associated with tellurite resistance. J. Biol. Chem. 274:1999;32318-32324.
18. 2-fixing endosymbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA. 98:2001;9889-9894.
19. Frick D.N., Bessman M.J. Cloning, purification, and properties of a novel NADH pyrophosphatase: Evidence for a nucleotide pyrophosphatase catalytic domain in MutT-like enzymes. J. Biol. Chem. 270:1995;1529-1534.
20. Griffin A.M., Morris V.J., Gasson M.J. Identification, cloning and sequencing the aceA gene involved in acetan biosynthesis in Acetobacter xylinum. FEMS Microbiol. Lett. 137:1996;115-121.
21. Guerreiro N., Ksenzenko V.N., Djordjevic M.A., Ivashina T.V., Rolfe B.G. Elevated levels of synthesis of over 20 proteins results after mutation of the Rhizobium leguminosarum exopolysaccharide synthesis gene pssA. J. Bacteriol. 182:2000;4521-4532.
22. Hussain H., Johnston A.W.B. Iron-dependent transcription of the regulatory gene ros of Agrobacterium radiobacter. Mol. Plant Microbe Interact. 10:1997;1087-1093.
23. Ielpi L., Couso R.O., Dankert M.A. Sequencial asssembly and polymerization of the polyprenol-linked pentasaccharide repeating unit of the xantan polysaccharide in Xanthomonas campestris. J. Bacteriol. 175:1993;2490-2500.
24. Ivashina T.V., Khmelnitsky M.I., Shlyapnikov M.G., Kanapin A.A., Ksenzenko V.N. The pssA gene from Rhizobium leguminosarum bv. viciae VF39: Cloning, sequence and the possible role in polysaccharide production and nodule formation. Gene. 150:1994;111-116.
25. Janczarek M., Król J., Kutkowska J., Mazur A., Wielbo J., Borucki W., Kopcinska J., Lotocka B., Urbanik-Sypniewska T., Skorupska A. Mutation in the pssB-pssA intergenic region of Rhizobium leguminosarum bv. trifolii affects the surface polysaccharides synthesis and nitrogen fixation ability. J. Plant Physiol. 158:2001;1565-1574.
26. Janczarek M., Król J., Skorupska A. The pssB gene product of Rhizobium leguminosarum bv. trifolii is homologous to a family of inositol monophosphatases. FEMS Microbiol. Lett. 173:1999;319-325.
27. Janczarek M., Skorupska A. The Rhizobium leguminosarum bv. trifolii pssB gene product is an inositol monophosphatase that influences exopolysaccharide synthesis. Arch. Microbiol. 175:2001;143-151.
28. Król J., Wielbo J., Mazur A., Kopciñska J., Lotocka B., Golinowski W., Skorupska A. Molecular characterization of pssCDE genes of Rhizobium leguminosarum bv. trifolii strain TA1: pssD mutant is affected in exopolysaccharide synthesis and endocytosis of bacteria. Mol. Plant Microbe Interact. 11:1998;1142-1148.
29. Latchford J.W., Borthakur D., Johnston A.W.B. The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface. Mol. Microbiol. 5:1991;2107-2114.
30. Lawrence M.C., Barbosa J.A., Smith B.J., Hall N.E., Pilling P.A., Ooi H.C., Marcuccio S.M. Structure and mechanism of a sub-family of enzymes related to N-acetylneuraminate lyase. J. Mol. Biol. 266:1997;381-399.
31. LeVier K., Guerinot M.L. The Bradyrhizobium japonicum fegA gene encodes an iron-regulated outer membrane protein with similarity to hydroxamate-type siderophore receptors. J. Bacteriol. 178:1996;7265-7275.
32. Loewus F.A. Improvement in the anthrone method for determination of carbohydrates. Anal. Chem. 24:1952;219-223.
33. Mazur A., Król J., Wielbo J., Urbanik-Sypniewska T., Skorupska A. Rhizobium leguminosarum bv. trifolii PssP protein is required for exopolysaccharide biosynthesis and polymerization. Mol. Plant Microbe Interact. 15:2002;388-397.
34. Miller J.H. Experiments in Molecular Genetics. 1972;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Niehaus K., Kapp D., Pühler A. Plant defence and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient Rhizobium meliloti mutant. Planta. 190:1993;415-425.
36. Pellock B.J., Cheng H.P., Walker G.C. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:2000;4310-4318.
37. Philip-Hollingsworth S., Hollingsworth R.I., Dazzo F.B. Host-range related structural features of the acidic extracellular polysaccharides of Rhizobium trifolii and Rhizobium leguminosarum. J. Biol. Chem. 264:1989;1461-1466.
38. Pollock T.J., van Workum W.A.T., Thorne L., Mikolajczak M.J., Yamazaki M., Kijne J.W., Armentrout R.W. Assignment of biochemical functions to glycosyl transferase genes which are essential for biosynthesis of exopolysaccharides in Sphingomonas strain S88 and Rhizobium leguminosarum. J. Bacteriol. 180:1998;586-593.
39. Pollock T.J., Thorne L., Mikolajczak M., Armentrout R.W. Mechanism of bacitracin in Gram-negative bacteria that synthesize exopolysaccharides. J. Bacteriol. 176:1994;6229-6237.
40. Reed J.W., Capage M., Walker G.C. Rhizobium meliloti exoG and exoJ mutations affect the ExoX-ExoY system for modulation of exopolysaccharide production. J. Bacteriol. 173:1991;3776-3788.
41. Reizer J., Reizer A., Saier M.H. Jr. A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci. 1:1992;1326-1332.
42. Rolfe B.G., Carlson R.W., Ridge R.W., Dazzo F.B., Mateos P.F., Pankhurst C.E. Defective infection and nodulation of clovers by exopolysaccharide mutants of Rhizobium leguminosarum bv. trifolii. Aust. J. Plant Physiol. 23:1996;285-303.
43. - mutant AR20. System. Appl. Microbiol. 19:1996;1-8.
44. Sadykov M.R., Ivashina T.V., Kanapin A.A., Shlyapnikov M.G., Ksenzenko V.N. Structural and functional organization of the exopolysaccharide biosynthesis genes in Rhizobium leguminosarum bv. viciae VF39. Mol. Biol. 32:1998;665-671.
45. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:1987;47-56.
47. Simon R., Priefer U., Pühler A. A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in Gram-negative bacteria. Biotechnology. 1:1983;784-791.
48. Skorupska A., Bialek U., Urbanik-Sypniewska T., van Lammeren A. Two types of nodules induced on Trifolium pratense by mutants of Rhizobium leguminosarum bv. trifolii deficient in exopolysaccharide production. J. Plant Physiol. 147:1995;93-100.
49. Spaink H.P., Okker R.J.H., Wijffelman C.A., Pees E., Lugtenberg B.J.J. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol. Biol. 9:1987;27-39.
50. Stanley J., Dowling D.N., Stucker M., Broughton W.J. Screening costramid libraries for chromosomal genes: Alternative interspecific hybridization methods. FEMS Microbiol. Lett. 48:1987;25-30.
51. Tiburtius A., de Luca N.G., Hussain H., Johnston A.W.B. Expression of the exoY gene, required for exopolysaccharide synthesis in Agrobacterium, is activated by the regulatory ros gene. Microbiology. 142:1996;2621-2629.
52. Tsang A.W., Horswill A.R., Escalante-Semerena J.C. Studies of regulation of expression of the propionate (prpBCDE) operon provide insights into how Salmonella typhimurium LT2 integrates its 1,2-propanediol and propionate catabolic pathways. J. Bacteriol. 180:1998;6511-6518.
53. van Workum W.A., Canter-Cremers H.C.J., Wijfies A.H.M., van der Kolk C., Wijffelman C.A., Kijne J.W. Cloning and characterization of four genes of Rhizobium leguminosarum bv. trifolii involved in exopolysaccharide production and nodulation. Mol. Plant Microbe Interact. 10:1997;290-301.
54. van Workum W.A., van Slageren S., van Brussel A.A., Kijne J.W. Role of exopolysaccharides of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol. Plant Microbe Interact. 11:1998;1233-1241.
55. Vincent J.M. A Manual for the Practical Study of the Root-Nodule Bacteria. IBP Handbook No. 15. 1970;Blackwell Scientific, Oxford.
56. Wang L., Reeves P.R. Involvement of the galactosyl-1-phosphate transferase encoded by the Salmonella enterica rfbP gene in O-antigen subunit processing. J. Bacteriol. 176:1994;4348-4356.
57. Wang L., Wang Y., Pellock B., Walker G.C. Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181:1999;6788-6796.
58. Yamazaki M., Thorne L., Mikolajczak M., Armentrout R.W., Pollock T.J. Linkage of genes essential for synthesis of a polysaccharide capsule in Sphingomonas strain S88. J. Bacteriol. 178:1996;2676-2687.
59. Yeoman K.H., Wisniewski-Dye F., Timony C., Stevens J.B., de Luca N.G., Downie J.A., Johnston A.W.B. Analysis of the Rhizobium leguminosarum siderophore-uptake gene fhuA: Differential expression in free-living bacteria and nitrogen-fixing bacteroids and distribution of an fhuA pseudogene in different strains. Microbiology. 146:2000;829-837.