The shdA Gene Is Restricted to Serotypes ofSalmonella enterica Subspecies I and Contributes to Efficient and Prolonged Fecal Shedding

ABSTRACT Little is known about factors which enable Salmonellaserotypes to circulate within populations of livestock and domestic fowl. We have identified a DNA region which is present inSalmonella serotypes commonly isolated from livestock and domestic fowl (S. enterica subspecies I) but absent from reptile-associated Salmonella serotypes (S. bongori and S. enterica subspecies II to VII). This DNA region was cloned from Salmonella serotype Typhimurium and sequence analysis revealed the presence of a 6,105-bp open reading frame, designated shdA, whose product's deduced amino acid sequence displayed homology to that of AIDA-I from diarrheagenicEscherichia coli, MisL of serotype Typhimurium, and IcsA ofShigella flexneri. The shdA gene was located adjacent to xseA at 52 min, in a 30-kb DNA region which is not present in Escherichia coli K-12. A serotype Typhimurium shdA mutant was shed with the feces in reduced numbers and for a shorter period of time compared to its isogenic parent. A possible role for the shdA gene during the expansion in host range of S. enterica subspecies I to include warm-blooded vertebrates is discussed.

[1]  P. R. Edwards,et al.  The Arizona group of enterobacteriaceae in animals and man; occurrence and distribution. , 1956, Bulletin of the World Health Organization.

[2]  S. Aleksić,et al.  Human infection caused by Salmonellae of subspecies II to VI in Germany, 1977-1992. , 1996, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[3]  V. L. Miller,et al.  Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R-M+ mutant. , 1993, Gene.

[4]  H. Grønstøl,et al.  Experimental Salmonella infection in calves. 1. The effect of stress factors on the carrier state , 1974, Journal of Hygiene.

[5]  S. Schroeder,et al.  Salmonellosis in the United States--a five-year review. , 1970, American journal of epidemiology.

[6]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[7]  F. Heffron,et al.  Multiple Fimbrial Adhesins Are Required for Full Virulence of Salmonella typhimurium in Mice , 1998, Infection and Immunity.

[8]  S. Brunak,et al.  SHORT COMMUNICATION Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites , 1997 .

[9]  B. Rowe,et al.  Salmonella arizonae in the United Kingdom from 1966 to 1990 , 1992, Epidemiology and Infection.

[10]  D. Hartl,et al.  Salmonella virulence plasmid. Modular acquisition of the spv virulence region by an F-plasmid in Salmonella enterica subspecies I and insertion into the chromosome of subspecies II, IIIa, IV and VII isolates. , 1998, Genetics.

[11]  R. Anderson,et al.  Evolutionary pressures in the spread and persistence of infectious agents in vertebrate populations , 1995, Parasitology.

[12]  M. Schmidt,et al.  AIDA‐I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule , 1992, Molecular microbiology.

[13]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[14]  F. Heffron,et al.  The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Pühler,et al.  A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria , 1983, Bio/Technology.

[16]  J. H. Mccoy Trends in salmonella food poisoning in England and Wales 1941–72 , 1975, Journal of Hygiene.

[17]  F. Heffron,et al.  Fur regulon of Salmonella typhimurium: identification of new iron-regulated genes , 1995, Journal of bacteriology.

[18]  B. Plikaytis,et al.  Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov , 1989, Journal of clinical microbiology.

[19]  D. Hanahan,et al.  Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Sundberg,et al.  Salmonellosis in reptiles: a review. , 1981, American journal of epidemiology.

[21]  J. Samuel,et al.  Salmonella in the intestinal tract and associated lymph nodes of sheep and cattle , 1981, Journal of Hygiene.

[22]  Eduardo A. Groisman,et al.  The SPI-3 Pathogenicity Island ofSalmonella enterica , 1999, Journal of bacteriology.

[23]  M. Roggendorf,et al.  Enterobacteria of reptiles. , 1976 .

[24]  F. Heffron,et al.  The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse , 1996, Infection and immunity.

[25]  J H Lee,et al.  Prevalence of fecal shedding of Salmonella organisms among captive green iguanas and potential public health implications. , 1998, Journal of the American Veterinary Medical Association.

[26]  G. Noskin,et al.  Salmonella arizonae bacteremia as the presenting manifestation of human immunodeficiency virus infection following rattlesnake meat ingestion. , 1990, Reviews of infectious diseases.

[27]  W. Johnson,et al.  Human salmonellosis associated with exotic pets , 1997, Journal of clinical microbiology.

[28]  H. Ochman,et al.  Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Velden,et al.  Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes , 1997, Journal of bacteriology.

[30]  F. Blattner,et al.  Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12 , 1997, Journal of bacteriology.

[31]  C. Wray,et al.  Incidence of salmonella infection in animals in England and Wales, 1968–1974 , 1977, Journal of Hygiene.

[32]  W. Goebel,et al.  A cytolysin encoded by Salmonella is required for survival within macrophages. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Galán,et al.  Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. M. Mackay‐Scollay,et al.  Salmonella and Arizona in reptiles and man in Western Australia , 1969, Journal of Hygiene.

[35]  B. Bochner Curing bacterial cells of lysogenic viruses by using ucb indicator plates , 1984 .

[36]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[37]  S. Makino,et al.  virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence , 1989, Journal of bacteriology.

[38]  J. Musser,et al.  Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers , 1990, Infection and immunity.

[39]  T. Whittam,et al.  Molecular genetic relationships of the salmonellae , 1996, Applied and environmental microbiology.

[40]  M. Popoff Antigenic formulas of the Salmonella serovars , 1997 .

[41]  F. Heffron,et al.  Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid , 1997, Infection and immunity.

[42]  J. Koopman,et al.  The occurrence of salmonellas and lactose-negative Arizonas in reptiles in The Netherlands, and a comparison of three enrichment methods used in their isolation , 1973, Journal of Hygiene.

[43]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[44]  F. Heffron,et al.  Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster , 1995, Journal of bacteriology.

[45]  W. Huse,et al.  Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. , 1988, Nucleic acids research.

[46]  S. Falkow What is a pathogen , 1997 .

[47]  P. Sansonetti,et al.  Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Boyd,et al.  Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. , 1993, Journal of general microbiology.

[49]  M. Thurmond,et al.  Prevalence of salmonellae in cattle and in the environment on California dairies. , 1994, Journal of the American Veterinary Medical Association.

[50]  T. Ficht,et al.  Evolution of Host Adaptation inSalmonella enterica , 1998, Infection and Immunity.