Campylobacter fetus surface layer proteins are transported by a type I secretion system

Stuart A Thompson, Omer L. Shedd, Kevin C. Ray, Michael H. Beins, Jesse P. Jorgensen, Martin J. Blaser

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

The virulence of Campylobacter fetus, a bacterial pathogen of ungulates and humans, is mediated in part by the presence of a paracrystalline surface layer (S-layer) that confers serum resistance. The subunits of the S-layer are S-layer proteins (SLPs) that are secreted in the absence of an N- terminal signal sequence and attach to either type A or B C. fetus lipopolysaccharide in a serospecific manner. Antigenic variation of multiple SLPs (encoded by sapA homologs) of type A strain 23D occurs by inversion of a promoter-containing DNA element flanked by two sapA homologs. Cloning and sequencing of the entire 6.2-kh invertible region from C. fetus 23D revealed a probable 5.6-kb operon of four overlapping genes (sapCDEF, with sizes of 1,035, 1,752, 1,284, and 1,302 bp, respectively) transcribed in the opposite direction from sapA. The four genes also were present in the invertible region of type B strain 84-107 and were virtually identical to their counterparts in the type A strain. Although SapC had no database homologies, SapD, SapE, and SapF had predicted amino acid homologies with type I protein secretion systems (typified by Escherichia coli HlyBD/TolC or Erwinia chrysanthemi PrtDEF) that utilize C-terminal secretion signals to mediate the secretion of hemolysins, leukotoxins, or proteases from other bacterial species. Analysis of the C termini of four C. fetus SLPs revealed conserved structures that are potential secretion signals. A C. fetus sapD mutant neither produced nor secreted SLPs. E. coli expressing C. fetus sapA and sapCDEF secreted SapA, indicating that the sapCDEF genes are sufficient for SLP secretion. C. fetus SLPs therefore are transported to the cell surface by a type I secretion system.

Original languageEnglish (US)
Pages (from-to)6450-6458
Number of pages9
JournalJournal of Bacteriology
Volume180
Issue number24
StatePublished - Dec 1 1998
Externally publishedYes

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Campylobacter fetus
Pectobacterium chrysanthemi
Overlapping Genes
Escherichia coli
Antigenic Variation
Hemolysin Proteins
Operon
Protein Sorting Signals
S-layer proteins
Type I Secretion Systems
Genes
Virulence
Lipopolysaccharides
Organism Cloning
Peptide Hydrolases
Databases
Amino Acids
DNA

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Thompson, S. A., Shedd, O. L., Ray, K. C., Beins, M. H., Jorgensen, J. P., & Blaser, M. J. (1998). Campylobacter fetus surface layer proteins are transported by a type I secretion system. Journal of Bacteriology, 180(24), 6450-6458.

Campylobacter fetus surface layer proteins are transported by a type I secretion system. / Thompson, Stuart A; Shedd, Omer L.; Ray, Kevin C.; Beins, Michael H.; Jorgensen, Jesse P.; Blaser, Martin J.

In: Journal of Bacteriology, Vol. 180, No. 24, 01.12.1998, p. 6450-6458.

Research output: Contribution to journalArticle

Thompson, SA, Shedd, OL, Ray, KC, Beins, MH, Jorgensen, JP & Blaser, MJ 1998, 'Campylobacter fetus surface layer proteins are transported by a type I secretion system', Journal of Bacteriology, vol. 180, no. 24, pp. 6450-6458.
Thompson SA, Shedd OL, Ray KC, Beins MH, Jorgensen JP, Blaser MJ. Campylobacter fetus surface layer proteins are transported by a type I secretion system. Journal of Bacteriology. 1998 Dec 1;180(24):6450-6458.
Thompson, Stuart A ; Shedd, Omer L. ; Ray, Kevin C. ; Beins, Michael H. ; Jorgensen, Jesse P. ; Blaser, Martin J. / Campylobacter fetus surface layer proteins are transported by a type I secretion system. In: Journal of Bacteriology. 1998 ; Vol. 180, No. 24. pp. 6450-6458.
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abstract = "The virulence of Campylobacter fetus, a bacterial pathogen of ungulates and humans, is mediated in part by the presence of a paracrystalline surface layer (S-layer) that confers serum resistance. The subunits of the S-layer are S-layer proteins (SLPs) that are secreted in the absence of an N- terminal signal sequence and attach to either type A or B C. fetus lipopolysaccharide in a serospecific manner. Antigenic variation of multiple SLPs (encoded by sapA homologs) of type A strain 23D occurs by inversion of a promoter-containing DNA element flanked by two sapA homologs. Cloning and sequencing of the entire 6.2-kh invertible region from C. fetus 23D revealed a probable 5.6-kb operon of four overlapping genes (sapCDEF, with sizes of 1,035, 1,752, 1,284, and 1,302 bp, respectively) transcribed in the opposite direction from sapA. The four genes also were present in the invertible region of type B strain 84-107 and were virtually identical to their counterparts in the type A strain. Although SapC had no database homologies, SapD, SapE, and SapF had predicted amino acid homologies with type I protein secretion systems (typified by Escherichia coli HlyBD/TolC or Erwinia chrysanthemi PrtDEF) that utilize C-terminal secretion signals to mediate the secretion of hemolysins, leukotoxins, or proteases from other bacterial species. Analysis of the C termini of four C. fetus SLPs revealed conserved structures that are potential secretion signals. A C. fetus sapD mutant neither produced nor secreted SLPs. E. coli expressing C. fetus sapA and sapCDEF secreted SapA, indicating that the sapCDEF genes are sufficient for SLP secretion. C. fetus SLPs therefore are transported to the cell surface by a type I secretion system.",
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