Home LiteratureArticle Details
PMID: 8626338 Published · ppublish English Journal Article

Linkage of genes essential for synthesis of a polysaccharide capsule in Sphingomonas strain S88.

Journal of bacteriology ·Vol. 178 ·No. 9 ·1996-05-00 ·Pages 2676-87

Yamazaki M, Thorne L, Mikolajczak M, Armentrout RW, Pollock TJ

Abstract

Several structurally related capsular polysaccharides that are secreted by members of the genus Sphingomonas are being developed as aqueous rheological control agents for diverse industrial and food applications. They include gellan (S-60), welan (S-130), rhamsan (S-194), S-657, S-88, S-198, S-7, and NW-11. We refer to these polysaccharides as sphingans, after the genus name. This paper characterizes the first gene cluster isolated from a Sphingomonas species (S88) that is required for capsule synthesis. Overlapping DNA segments which spanned about 50 kbp of S88 DNA restored the synthesis of sphingan S-88 in capsule-negative mutants. The mutations were mapped into functional complementation groups, and the contiguous nucleotide sequence for the 29-kbp cluster was determined. The genetic complementation map and the DNA sequences were interpreted as an extended multicistronic locus containing genes essential for the assembly and secretion of polysaccharide S-88. Many of the deduced amino acid sequences were similar to gene products from other polysaccharide-secreting bacteria such as Rhizobium meliloti (succinoglycan), Xanthomonas campestris (xanthan gum), and Salmonella enterica (O antigen). The S88 locus contained a four-gene operon for the biosynthesis of dTDP-L-rhamnose, an essential precursor for the sphingans. Unexpectedly, there were also two genes for secretion of a lytic or toxin-like protein nested within the polysaccharide cluster. The conservation and linkage of genes that code for a defensive capsule and genes for secretion of an offensive lysin or toxin suggest a heretofore unknown pathogenic life history for Sphingomonas strain S88.

MeSH Terms
ATP-Binding Cassette Transporters/genetics Amino Acid Sequence Bacterial Capsules/biosynthesis Base Composition Base Sequence Carbohydrate Sequence Cloning, Molecular Codon Genes, Bacterial/genetics Genetic Complementation Test Gram-Negative Aerobic Bacteria/genetics,metabolism Molecular Sequence Data Multigene Family/genetics Operon/genetics Peptide Chain Initiation, Translational/genetics Sequence Alignment Sequence Analysis, DNA Sequence Deletion
Chemicals
ATP-Binding Cassette Transporters Codon
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Yamazaki M
Shin-Etsu Bio, Inc., San Diego, California 92121, USA.
Thorne L
Mikolajczak M
Armentrout R W
Pollock T J
References (49)
49 references, click to expand
  1. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347-51 PMID: 7012838
  2. Uses of transposons with emphasis on Tn10.
    Methods Enzymol. 1991;204:139-80 PMID: 1658561
  3. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  4. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers.
    Gene. 1982 Oct;19(3):259-68 PMID: 6295879
  5. Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti.
    Cell. 1993 Jul 30;74(2):269-80 PMID: 8343955
  6. Cloning and sequence analysis of a hemolysin-encoding gene from Pseudomonas paucimobilis.
    Gene. 1993 Aug 16;130(1):57-63 PMID: 8344528
  7. Identification of cpsD, a gene essential for type III capsule expression in group B streptococci.
    Mol Microbiol. 1993 May;8(5):843-55 PMID: 8355611
  8. Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti.
    J Bacteriol. 1993 Nov;175(21):7033-44 PMID: 8226645
  9. 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):7045-55 PMID: 8226646
  10. 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):7786-92 PMID: 8253667
  11. Nucleotide sequence and mutational analysis of the gene encoding KpsD, a periplasmic protein involved in transport of polysialic acid in Escherichia coli K1.
    J Bacteriol. 1994 Jul;176(13):4025-33 PMID: 8021185
  12. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster.
    J Bacteriol. 1994 Jul;176(13):4144-56 PMID: 7517391
  13. Mechanism of bacitracin resistance in gram-negative bacteria that synthesize exopolysaccharides.
    J Bacteriol. 1994 Oct;176(20):6229-37 PMID: 7928993
  14. Transferases of O-antigen biosynthesis in Salmonella enterica: dideoxyhexosyltransferases of groups B and C2 and acetyltransferase of group C2.
    J Bacteriol. 1995 Jul;177(14):4084-8 PMID: 7541787
  15. Aromatic-degrading Sphingomonas isolates from the deep subsurface.
    Appl Environ Microbiol. 1995 May;61(5):1917-22 PMID: 7544095
  16. 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 PMID: 7565082
  17. Chemical structure of glycosphingolipids isolated from Sphingomonas paucimobilis.
    FEBS Lett. 1991 Nov 4;292(1-2):107-10 PMID: 1959589
  18. Cloning and sequencing of the gene for a Pseudomonas paucimobilis enzyme that cleaves beta-aryl ether.
    J Bacteriol. 1991 Dec;173(24):7950-5 PMID: 1744051
  19. Infections with Pseudomonas paucimobilis: report of four cases and review.
    Rev Infect Dis. 1991 Nov-Dec;13(6):1072-6 PMID: 1775840
  20. Location of the O-acetyl group in welan by the reductive-cleavage method.
    Carbohydr Res. 1992 Feb 7;224:337-41 PMID: 1591770
  21. A rapid method for cosmid cloning.
    Biotechniques. 1992 Feb;12(2):172, 174, 176 PMID: 1616703
  22. DNA cassettes containing the origin of transfer (oriT) of two broad-host-range transfer systems.
    Biotechniques. 1992 Jul;13(1):56-8, 60, 62 PMID: 1503776
  23. 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 PMID: 8439670
  24. Sequential assembly and polymerization of the polyprenol-linked pentasaccharide repeating unit of the xanthan polysaccharide in Xanthomonas campestris.
    J Bacteriol. 1993 May;175(9):2490-500 PMID: 7683019
  25. Biosynthesis of cell wall lipopolysaccharide in mutants of Salmonella. V. A mutant of Salmonella typhimurium defective in the synthesis of cytidine diphosphoabequose.
    J Bacteriol. 1969 Oct;100(1):433-44 PMID: 4899003
  26. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites.
    Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342-6 PMID: 4598299
  27. Structure of extracellular polysaccharide from Xanthomonas campestris.
    Carbohydr Res. 1975 Dec;45:275-82 PMID: 1212669
  28. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  29. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648-52 PMID: 377280
  30. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  31. Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression.
    Plasmid. 1985 Mar;13(2):149-53 PMID: 2987994
  32. Nucleotide sequence of an Escherichia coli chromosomal hemolysin.
    J Bacteriol. 1985 Jul;163(1):94-105 PMID: 3891743
  33. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector.
    Gene. 1986;48(1):119-31 PMID: 3549457
  34. Genetic and physical analyses of a cluster of genes essential for xanthan gum biosynthesis in Xanthomonas campestris.
    J Bacteriol. 1987 Jun;169(6):2854-61 PMID: 3034868
  35. Clustering of mutations blocking synthesis of xanthan gum by Xanthomonas campestris.
    J Bacteriol. 1987 Aug;169(8):3593-600 PMID: 3038845
  36. The ndvA gene product of Rhizobium meliloti is required for beta-(1----2)glucan production and has homology to the ATP-binding export protein HlyB.
    J Bacteriol. 1988 Aug;170(8):3523-30 PMID: 3042754
  37. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis.
    EMBO J. 1988 Dec 1;7(12):3997-4004 PMID: 2905265
  38. Cloning, nucleotide sequence, and characterization of genes encoding the secretion function of the Pasteurella haemolytica leukotoxin determinant.
    J Bacteriol. 1989 Feb;171(2):916-28 PMID: 2914876
  39. 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. 1988 Jul;213(1):155-62 PMID: 2851702
  40. Two genes that regulate exopolysaccharide production in Rhizobium sp. strain NGR234: DNA sequences and resultant phenotypes.
    J Bacteriol. 1990 Jan;172(1):193-203 PMID: 2152899
  41. Genomic organization of the human multidrug resistance (MDR1) gene and origin of P-glycoproteins.
    J Biol Chem. 1990 Jan 5;265(1):506-14 PMID: 1967175
  42. Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb. nov., and two genospecies of the genus Sphingomonas.
    Microbiol Immunol. 1990;34(2):99-119 PMID: 2111872
  43. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  44. Structural analysis of an acidic polysaccharide secreted by Xanthobacter sp. (ATCC 53272).
    Carbohydr Res. 1990 Oct 10;206(2):289-96 PMID: 2073637
  45. The bex locus in encapsulated Haemophilus influenzae: a chromosomal region involved in capsule polysaccharide export.
    Mol Microbiol. 1990 Nov;4(11):1853-62 PMID: 2082145
  46. Molecular analysis of the Escherichia coli K5 kps locus: identification and characterization of an inner-membrane capsular polysaccharide transport system.
    Mol Microbiol. 1990 Nov;4(11):1863-9 PMID: 2082146
  47. Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2).
    Mol Microbiol. 1991 Mar;5(3):695-713 PMID: 1710759
  48. Rhizobium meliloti exoG and exoJ mutations affect the exoX-exoY system for modulation of exopolysaccharide production.
    J Bacteriol. 1991 Jun;173(12):3776-88 PMID: 2050634
  49. Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance.
    J Bacteriol. 1982 May;150(2):815-25 PMID: 6950931
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-05-00
Pages
2676-87
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC177995
Subset
IM
Databases
GENBANK
U51197
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]