Transposition of the Heat-Stable ToxinastAGene into a Gifsy-2-Related Prophage ofSalmonella entericaSerovar Abortusovis

Abstract

The horizontal transfer and acquisition of virulence genes via mobile genetic elements have been a major driving force in the evolution of Salmonella pathogenicity. Serovars of Salmonella enterica carry variable assortments of phage-encoded virulence genes, suggesting that temperate phages play a pivotal role in this process. Epidemic isolates of S. enterica serovar Typhimurium are consistently lysogenic for two lambdoid phages, Gifsy-1 and Gifsy-2, carrying known virulence genes. Other serovars of S. enterica, including serovars Dublin, Gallinarum, Enteritidis, and Hadar, carry distinct prophages with similarity to the Gifsy phages. In this study, we analyzed Gifsy-related loci from S. enterica serovar Abortusovis, a pathogen associated exclusively with ovine infection. A cryptic prophage, closely related to serovar Typhimurium phage Gifsy-2, was identified. This element, named Gifsy-2AO, was shown to contribute to serovar Abortusovis systemic infection in lambs. Sequence analysis of the prophage b region showed a large deletion which covers genes encoding phage tail fiber proteins and putative virulence factors, including type III secreted effector protein SseI (GtgB, SrfH). This deletion was identified in most of the serovar Abortusovis isolates tested and might be dependent on the replicative transposition of an adjacent insertion sequence, IS1414, previously identified in pathogenic Escherichia coli strains. IS1414 encodes heat-stable toxin EAST1 (astA) and showed multiple genomic copies in isolates of serovar Abortusovis. To our knowledge, this is the first evidence of intergeneric transfer of virulence genes via insertion sequence elements in Salmonella. The acquisition of IS1414 (EAST1) and its frequent transposition within the chromosome might improve the fitness of serovar Abortusovis within its narrow ecological niche.

Presence of Escherichia coli carrying the EAST1 toxin gene in farm animals

“…Yet, there is no evidence of EAST1-dependent fluid secretion in animal studies or of an association of EAST1 with epidemic strains of E. coli with high diarrheagenic potential [2].…”

“…A study of Bacciu et al [2] indicated that an intergeneric transfer of virulence genes (involving the astA gene) via an insertion sequence (IS1414, encoding a transposase (tnpA) and astA in Salmonella) from E. coli together with studies reporting the presence of astA in bacterial genera besides E. coli, like Salmonella Agona [32] and Klebsiella pneumoniae [29] clearly indicate that horizontal transfer of virulence factors, including the astA gene, between bacterial genera occurs in nature and can account for the considerable distribution of the EAST1 gene in E. coli besides EAEC. Yet, there is no evidence of EAST1-dependent fluid secretion in animal studies or of an association of EAST1 with epidemic strains of E. coli with high diarrheagenic potential [2].…”

Species-specific supercoil dynamics of the bacterial nucleoid

“…More significant are the four plaque-forming prophage, Gifsy-1, Gifsy-2, Fels-1, and Fels-2. These viruses are under selection because they include multiple genes and operons that increase the ability of Salmonella to infect and reside in mammalian hosts (Bacciu et al 2004;Coombes et al 2005;Figueroa-Bossi and Bossi 1999;Ho et al 2002). These elements are also potentially lethal if and when spontaneous induction leads to viral replication and cell lysis.…”

Characterization of virulence factors in the newly described Salmonella enterica serotype Keurmassar emerging in Senegal (sub-Saharan Africa)

“…Detection of Gifsy-1 and Gifsy-2 phages was performed as previously described [3]. S. Typhimurium strain ATCC 14028s was used as positive control.…”

“…Multiple virulence factors are involved in the pathogenesis of Salmonella. These virulence genes act together in a complex virulence function, and have been found on horizontally acquired DNA regions, such as pathogenicity islands, plasmids, transposons, and bacteriophages [3,4].…”