Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Feb;179(4):1375–1384. doi: 10.1128/jb.179.4.1375-1384.1997

The 32-kilobase exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: genetic organization and properties of the encoded gene products.

A Becker 1, S Rüberg 1, H Küster 1, A A Roxlau 1, M Keller 1, T Ivashina 1, H P Cheng 1, G C Walker 1, A Pühler 1
PMCID: PMC178839  PMID: 9023225

Abstract

Proteins directing the biosynthesis of galactoglucan (exopolysaccharide II) in Rhizobium meliloti Rm2011 are encoded by the exp genes. Sequence analysis of a 32-kb DNA fragment of megaplasmid 2 containing the exp gene cluster identified previously (J. Glazebrook and G. C. Walker, Cell 56:661-672, 1989) revealed the presence of 25 open reading frames. Homologies of the deduced exp gene products to proteins of known function suggested that the exp genes encoded four proteins involved in the biosynthesis of dTDP-glucose and dTDP-rhamnose, six glycosyltransferases, an ABC transporter complex homologous to the subfamily of peptide and protein export complexes, and a protein homologous to Rhizobium NodO proteins. In addition, homologies of three Exp proteins to transcriptional regulators, methyltransferases, and periplasmic binding proteins were found. The positions of 26 Tn5 insertions in the exp gene cluster were determined, thus allowing the previously described genetic map to be correlated with the sequence. Operon analysis revealed that the exp gene cluster consists of five complementation groups. In comparison to the wild-type background, all exp complementation groups were transcribed at a substantially elevated level in the regulatory mucR mutant.

Full Text

The Full Text of this article is available as a PDF (320.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Astete S. G., Leigh J. A. mucS, a gene involved in activation of galactoglucan (EPS II) synthesis gene expression in Rhizobium meliloti. Mol Plant Microbe Interact. 1996 Jul;9(5):395–400. doi: 10.1094/mpmi-9-0395. [DOI] [PubMed] [Google Scholar]
  3. Battisti L., Lara J. C., Leigh J. A. Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5625–5629. doi: 10.1073/pnas.89.12.5625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Becker A., Kleickmann A., Arnold W., Pühler A. Analysis of the Rhizobium meliloti exoH/exoK/exoL fragment: ExoK shows homology to excreted endo-beta-1,3-1,4-glucanases and ExoH resembles membrane proteins. Mol Gen Genet. 1993 Apr;238(1-2):145–154. doi: 10.1007/BF00279541. [DOI] [PubMed] [Google Scholar]
  5. Becker A., Kleickmann A., Keller M., Arnold W., Pühler A. Identification and analysis of the Rhizobium meliloti exoAMONP genes involved in exopolysaccharide biosynthesis and mapping of promoters located on the exoHKLAMONP fragment. Mol Gen Genet. 1993 Nov;241(3-4):367–379. doi: 10.1007/BF00284690. [DOI] [PubMed] [Google Scholar]
  6. Becker A., Kleickmann A., Küster H., Keller M., Arnold W., Pühler A. Analysis of the Rhizobium meliloti genes exoU, exoV, exoW, exoT, and exoI involved in exopolysaccharide biosynthesis and nodule invasion: exoU and exoW probably encode glucosyltransferases. Mol Plant Microbe Interact. 1993 Nov-Dec;6(6):735–744. doi: 10.1094/mpmi-6-735. [DOI] [PubMed] [Google Scholar]
  7. Becker A., Küster H., Niehaus K., Pühler A. Extension of the Rhizobium meliloti succinoglycan biosynthesis gene cluster: identification of the exsA gene encoding an ABC transporter protein, and the exsB gene which probably codes for a regulator of succinoglycan biosynthesis. Mol Gen Genet. 1995 Dec 15;249(5):487–497. doi: 10.1007/BF00290574. [DOI] [PubMed] [Google Scholar]
  8. Becker A., Niehaus K., Pühler A. Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated ExoP protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain. Mol Microbiol. 1995 Apr;16(2):191–203. doi: 10.1111/j.1365-2958.1995.tb02292.x. [DOI] [PubMed] [Google Scholar]
  9. Becker A., Schmidt M., Jäger W., Pühler A. New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene. 1995 Aug 30;162(1):37–39. doi: 10.1016/0378-1119(95)00313-u. [DOI] [PubMed] [Google Scholar]
  10. Beringer J. E. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974 Sep;84(1):188–198. doi: 10.1099/00221287-84-1-188. [DOI] [PubMed] [Google Scholar]
  11. Brewin N. J. Development of the legume root nodule. Annu Rev Cell Biol. 1991;7:191–226. doi: 10.1146/annurev.cb.07.110191.001203. [DOI] [PubMed] [Google Scholar]
  12. Buendia A. M., Enenkel B., Köplin R., Niehaus K., Arnold W., Pühler A. The Rhizobium meliloti exoZl exoB fragment of megaplasmid 2: ExoB functions as a UDP-glucose 4-epimerase and ExoZ shows homology to NodX of Rhizobium leguminosarum biovar viciae strain TOM. Mol Microbiol. 1991 Jun;5(6):1519–1530. doi: 10.1111/j.1365-2958.1991.tb00799.x. [DOI] [PubMed] [Google Scholar]
  13. Charles T. C., Finan T. M. Analysis of a 1600-kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo. Genetics. 1991 Jan;127(1):5–20. doi: 10.1093/genetics/127.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clarke B. R., Bronner D., Keenleyside W. J., Severn W. B., Richards J. C., Whitfield C. Role of Rfe and RfbF in the initiation of biosynthesis of D-galactan I, the lipopolysaccharide O antigen from Klebsiella pneumoniae serotype O1. J Bacteriol. 1995 Oct;177(19):5411–5418. doi: 10.1128/jb.177.19.5411-5418.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cohen S. P., Hächler H., Levy S. B. Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol. 1993 Mar;175(5):1484–1492. doi: 10.1128/jb.175.5.1484-1492.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dehoux P., Cossart P. Homologies between salmolysin and some bacterial regulatory proteins. Mol Microbiol. 1995 Feb;15(3):591–591. doi: 10.1111/j.1365-2958.1995.tb02272.x. [DOI] [PubMed] [Google Scholar]
  17. Delepelaire P., Wandersman C. Protease secretion by Erwinia chrysanthemi. Proteases B and C are synthesized and secreted as zymogens without a signal peptide. J Biol Chem. 1989 May 25;264(15):9083–9089. [PubMed] [Google Scholar]
  18. Dinh T., Paulsen I. T., Saier M. H., Jr A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J Bacteriol. 1994 Jul;176(13):3825–3831. doi: 10.1128/jb.176.13.3825-3831.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Economou A., Hamilton W. D., Johnston A. W., Downie J. A. The Rhizobium nodulation gene nodO encodes a Ca2(+)-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J. 1990 Feb;9(2):349–354. doi: 10.1002/j.1460-2075.1990.tb08117.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
  21. Fath M. J., Kolter R. ABC transporters: bacterial exporters. Microbiol Rev. 1993 Dec;57(4):995–1017. doi: 10.1128/mr.57.4.995-1017.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fellay R., Frey J., Krisch H. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene. 1987;52(2-3):147–154. doi: 10.1016/0378-1119(87)90041-2. [DOI] [PubMed] [Google Scholar]
  23. Felmlee T., Pellett S., Lee E. Y., Welch R. A. Escherichia coli hemolysin is released extracellularly without cleavage of a signal peptide. J Bacteriol. 1985 Jul;163(1):88–93. doi: 10.1128/jb.163.1.88-93.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Finke A., Bronner D., Nikolaev A. V., Jann B., Jann K. Biosynthesis of the Escherichia coli K5 polysaccharide, a representative of group II capsular polysaccharides: polymerization in vitro and characterization of the product. J Bacteriol. 1991 Jul;173(13):4088–4094. doi: 10.1128/jb.173.13.4088-4094.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  26. Franssen H. J., Vijn I., Yang W. C., Bisseling T. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol. 1992 May;19(1):89–107. doi: 10.1007/BF00015608. [DOI] [PubMed] [Google Scholar]
  27. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  28. Glazebrook J., Walker G. C. A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell. 1989 Feb 24;56(4):661–672. doi: 10.1016/0092-8674(89)90588-6. [DOI] [PubMed] [Google Scholar]
  29. Glucksmann M. A., Reuber T. L., Walker G. C. Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti. J Bacteriol. 1993 Nov;175(21):7033–7044. doi: 10.1128/jb.175.21.7033-7044.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Glucksmann M. A., Reuber T. L., Walker G. C. Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol. 1993 Nov;175(21):7045–7055. doi: 10.1128/jb.175.21.7045-7055.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. González J. E., Reuhs B. L., Walker G. C. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8636–8641. doi: 10.1073/pnas.93.16.8636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Göhmann S., Manning P. A., Alpert C. A., Walker M. J., Timmis K. N. Lipopolysaccharide O-antigen biosynthesis in Shigella dysenteriae serotype 1: analysis of the plasmid-carried rfp determinant. Microb Pathog. 1994 Jan;16(1):53–64. doi: 10.1006/mpat.1994.1005. [DOI] [PubMed] [Google Scholar]
  33. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  34. Her G. R., Glazebrook J., Walker G. C., Reinhold V. N. Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm1021. Carbohydr Res. 1990 May 1;198(2):305–312. doi: 10.1016/0008-6215(90)84300-j. [DOI] [PubMed] [Google Scholar]
  35. Holland I. B., Kenny B., Blight M. Haemolysin secretion from E coli. Biochimie. 1990 Feb-Mar;72(2-3):131–141. doi: 10.1016/0300-9084(90)90138-7. [DOI] [PubMed] [Google Scholar]
  36. Hussain K., Elliott E. J., Salmond G. P. The parD- mutant of Escherichia coli also carries a gyrAam mutation. The complete sequence of gyrA. Mol Microbiol. 1987 Nov;1(3):259–273. doi: 10.1111/j.1365-2958.1987.tb01932.x. [DOI] [PubMed] [Google Scholar]
  37. Hussain M., Lenard J. Characterization of PDR4, a Saccharomyces cerevisiae gene that confers pleiotropic drug resistance in high-copy number: identity with YAP1, encoding a transcriptional activator [corrected]. Gene. 1991 May 15;101(1):149–152. doi: 10.1016/0378-1119(91)90238-7. [DOI] [PubMed] [Google Scholar]
  38. Jiang X. M., Neal B., Santiago F., Lee S. J., Romana L. K., Reeves P. R. Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol Microbiol. 1991 Mar;5(3):695–713. doi: 10.1111/j.1365-2958.1991.tb00741.x. [DOI] [PubMed] [Google Scholar]
  39. Keller M., Roxlau A., Weng W. M., Schmidt M., Quandt J., Niehaus K., Jording D., Arnold W., Pühler A. Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan. Mol Plant Microbe Interact. 1995 Mar-Apr;8(2):267–277. doi: 10.1094/mpmi-8-0267. [DOI] [PubMed] [Google Scholar]
  40. Koronakis V., Koronakis E., Hughes C. Isolation and analysis of the C-terminal signal directing export of Escherichia coli hemolysin protein across both bacterial membranes. EMBO J. 1989 Feb;8(2):595–605. doi: 10.1002/j.1460-2075.1989.tb03414.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Köplin R., Wang G., Hötte B., Priefer U. B., Pühler A. A 3.9-kb DNA region of Xanthomonas campestris pv. campestris that is necessary for lipopolysaccharide production encodes a set of enzymes involved in the synthesis of dTDP-rhamnose. J Bacteriol. 1993 Dec;175(24):7786–7792. doi: 10.1128/jb.175.24.7786-7792.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Long S., Reed J. W., Himawan J., Walker G. C. Genetic analysis of a cluster of genes required for synthesis of the calcofluor-binding exopolysaccharide of Rhizobium meliloti. J Bacteriol. 1988 Sep;170(9):4239–4248. doi: 10.1128/jb.170.9.4239-4248.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ludwig A., Jarchau T., Benz R., Goebel W. The repeat domain of Escherichia coli haemolysin (HlyA) is responsible for its Ca2+-dependent binding to erythrocytes. Mol Gen Genet. 1988 Nov;214(3):553–561. doi: 10.1007/BF00330494. [DOI] [PubMed] [Google Scholar]
  44. Létoffé S., Delepelaire P., Wandersman C. Cloning and expression in Escherichia coli of the Serratia marcescens metalloprotease gene: secretion of the protease from E. coli in the presence of the Erwinia chrysanthemi protease secretion functions. J Bacteriol. 1991 Apr;173(7):2160–2166. doi: 10.1128/jb.173.7.2160-2166.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Létoffé S., Delepelaire P., Wandersman C. Protease secretion by Erwinia chrysanthemi: the specific secretion functions are analogous to those of Escherichia coli alpha-haemolysin. EMBO J. 1990 May;9(5):1375–1382. doi: 10.1002/j.1460-2075.1990.tb08252.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. MacLachlan P. R., Kadam S. K., Sanderson K. E. Cloning, characterization, and DNA sequence of the rfaLK region for lipopolysaccharide synthesis in Salmonella typhimurium LT2. J Bacteriol. 1991 Nov;173(22):7151–7163. doi: 10.1128/jb.173.22.7151-7163.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Marklund B. I., Tennent J. M., Garcia E., Hamers A., Båga M., Lindberg F., Gaastra W., Normark S. Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol. 1992 Aug;6(16):2225–2242. doi: 10.1111/j.1365-2958.1992.tb01399.x. [DOI] [PubMed] [Google Scholar]
  48. Masepohl B., Klipp W., Pühler A. Genetic characterization and sequence analysis of the duplicated nifA/nifB gene region of Rhodobacter capsulatus. Mol Gen Genet. 1988 Apr;212(1):27–37. doi: 10.1007/BF00322441. [DOI] [PubMed] [Google Scholar]
  49. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol. 1982 Jan;149(1):114–122. doi: 10.1128/jb.149.1.114-122.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Myers E. W., Miller W. Optimal alignments in linear space. Comput Appl Biosci. 1988 Mar;4(1):11–17. doi: 10.1093/bioinformatics/4.1.11. [DOI] [PubMed] [Google Scholar]
  51. Müller P., Keller M., Weng W. M., Quandt J., Arnold W., Pühler A. Genetic analysis of the Rhizobium meliloti exoYFQ operon: ExoY is homologous to sugar transferases and ExoQ represents a transmembrane protein. Mol Plant Microbe Interact. 1993 Jan-Feb;6(1):55–65. doi: 10.1094/mpmi-6-055. [DOI] [PubMed] [Google Scholar]
  52. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pridmore R. D. New and versatile cloning vectors with kanamycin-resistance marker. Gene. 1987;56(2-3):309–312. doi: 10.1016/0378-1119(87)90149-1. [DOI] [PubMed] [Google Scholar]
  54. Reinhold B. B., Chan S. Y., Reuber T. L., Marra A., Walker G. C., Reinhold V. N. Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021. J Bacteriol. 1994 Apr;176(7):1997–2002. doi: 10.1128/jb.176.7.1997-2002.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Reuber T. L., Walker G. C. Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell. 1993 Jul 30;74(2):269–280. doi: 10.1016/0092-8674(93)90418-p. [DOI] [PubMed] [Google Scholar]
  56. Saxena I. M., Brown R. M., Jr, Fevre M., Geremia R. A., Henrissat B. Multidomain architecture of beta-glycosyl transferases: implications for mechanism of action. J Bacteriol. 1995 Mar;177(6):1419–1424. doi: 10.1128/jb.177.6.1419-1424.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene. 1994 Jul 22;145(1):69–73. doi: 10.1016/0378-1119(94)90324-7. [DOI] [PubMed] [Google Scholar]
  58. Simon R. High frequency mobilization of gram-negative bacterial replicons by the in vitro constructed Tn5-Mob transposon. Mol Gen Genet. 1984;196(3):413–420. doi: 10.1007/BF00436188. [DOI] [PubMed] [Google Scholar]
  59. Staden R., McLachlan A. D. Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res. 1982 Jan 11;10(1):141–156. doi: 10.1093/nar/10.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Staden R. The current status and portability of our sequence handling software. Nucleic Acids Res. 1986 Jan 10;14(1):217–231. doi: 10.1093/nar/14.1.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sugiyama T., Kido N., Komatsu T., Ohta M., Jann K., Jann B., Saeki A., Kato N. Genetic analysis of Escherichia coli O9 rfb: identification and DNA sequence of phosphomannomutase and GDP-mannose pyrophosphorylase genes. Microbiology. 1994 Jan;140(Pt 1):59–71. doi: 10.1099/13500872-140-1-59. [DOI] [PubMed] [Google Scholar]
  62. Sulavik M. C., Gambino L. F., Miller P. F. The MarR repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli: prototypic member of a family of bacterial regulatory proteins involved in sensing phenolic compounds. Mol Med. 1995 May;1(4):436–446. [PMC free article] [PubMed] [Google Scholar]
  63. Sutton J. M., Lea E. J., Downie J. A. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9990–9994. doi: 10.1073/pnas.91.21.9990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Szabo M., Bronner D., Whitfield C. Relationships between rfb gene clusters required for biosynthesis of identical D-galactose-containing O antigens in Klebsiella pneumoniae serotype O1 and Serratia marcescens serotype O16. J Bacteriol. 1995 Mar;177(6):1544–1553. doi: 10.1128/jb.177.6.1544-1553.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Uttaro A. D., Ugalde R. A. A chromosomal cluster of genes encoding ADP-glucose synthetase, glycogen synthase and phosphoglucomutase in Agrobacterium tumefaciens. Gene. 1994 Dec 2;150(1):117–122. doi: 10.1016/0378-1119(94)90869-9. [DOI] [PubMed] [Google Scholar]
  66. Vieira J., Messing J. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene. 1991 Apr;100:189–194. doi: 10.1016/0378-1119(91)90365-i. [DOI] [PubMed] [Google Scholar]
  67. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wang A. Y., Grogan D. W., Cronan J. E., Jr Cyclopropane fatty acid synthase of Escherichia coli: deduced amino acid sequence, purification, and studies of the enzyme active site. Biochemistry. 1992 Nov 17;31(45):11020–11028. doi: 10.1021/bi00160a011. [DOI] [PubMed] [Google Scholar]
  69. Welch R. A. Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol. 1991 Mar;5(3):521–528. doi: 10.1111/j.1365-2958.1991.tb00723.x. [DOI] [PubMed] [Google Scholar]
  70. Yazdi M. A., Moir A. Characterization and cloning of the gerC locus of Bacillus subtilis 168. J Gen Microbiol. 1990 Jul;136(7):1335–1342. doi: 10.1099/00221287-136-7-1335. [DOI] [PubMed] [Google Scholar]
  71. Yin Y., Zhang F., Ling V., Arrowsmith C. H. Structural analysis and comparison of the C-terminal transport signal domains of hemolysin A and leukotoxin A. FEBS Lett. 1995 Jun 5;366(1):1–5. doi: 10.1016/0014-5793(95)00454-h. [DOI] [PubMed] [Google Scholar]
  72. Zhan H. J., Lee C. C., Leigh J. A. Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations. J Bacteriol. 1991 Nov;173(22):7391–7394. doi: 10.1128/jb.173.22.7391-7394.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Zhan H. J., Levery S. B., Lee C. C., Leigh J. A. A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion. Proc Natl Acad Sci U S A. 1989 May;86(9):3055–3059. doi: 10.1073/pnas.86.9.3055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zhang L., al-Hendy A., Toivanen P., Skurnik M. Genetic organization and sequence of the rfb gene cluster of Yersinia enterocolitica serotype O:3: similarities to the dTDP-L-rhamnose biosynthesis pathway of Salmonella and to the bacterial polysaccharide transport systems. Mol Microbiol. 1993 Jul;9(2):309–321. doi: 10.1111/j.1365-2958.1993.tb01692.x. [DOI] [PubMed] [Google Scholar]
  75. Zimmermann J., Voss H., Schwager C., Stegemann J., Erfle H., Stucky K., Kristensen T., Ansorge W. A simplified protocol for fast plasmid DNA sequencing. Nucleic Acids Res. 1990 Feb 25;18(4):1067–1067. doi: 10.1093/nar/18.4.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. del Castillo I., González-Pastor J. E., San Millán J. L., Moreno F. Nucleotide sequence of the Escherichia coli regulatory gene mprA and construction and characterization of mprA-deficient mutants. J Bacteriol. 1991 Jun;173(12):3924–3929. doi: 10.1128/jb.173.12.3924-3929.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. van Rhijn P., Luyten E., Vlassak K., Vanderleyden J. Isolation and characterization of a pSym locus of Rhizobium sp. BR816 that extends nodulation ability of narrow host range Phaseolus vulgaris symbionts to Leucaena leucocephala. Mol Plant Microbe Interact. 1996 Jan;9(1):74–77. doi: 10.1094/mpmi-9-0074. [DOI] [PubMed] [Google Scholar]
  78. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES