Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes

Abstract

Only certain serotypes of Salmonella represent 99% of all human clinical isolates. We determined whether the phylogenetic distribution of fimbrial operons would account for the host adaptations observed for Salmonella serotypes. We found that three fimbrial operons, fim, lpf, and agf, were present in a lineage ancestral to Salmonella. While the fim and agf fimbrial operons were highly conserved among all Salmonella serotypes, sequence analysis suggested that the lpf operon was lost from many distantly related lineages. As a consequence, the distribution of the lpf operon cannot be explained easily and may be a consequence of positive and negative selection in different hosts for the presence of these genes. Two other fimbrial operons, sef and pef, each entered two distantly related Salmonella lineages and each is present only in a small number of serotypes. These results show that horizontal gene transfer and deletion events have created unique combinations of fimbrial operons among Salmonella serotypes. The presence of sef and pef correlated with serotypes frequently isolated from common domesticated animals.The genus Salmonella and the species Escherichia coli are phylogenetically closely related, diverging from a common ancestor between 100 and 160 million years ago (21, 40). The gene order on the chromosome has been highly conserved between these two organisms (45), and corresponding genes have an average of 84% sequence identity (50). These properties make E. coli and the genus Salmonella a unique pair with which to identify evolutionary changes in genomes. A comparison of the genetic map of E. coli K-12 with that of serotype Salmonella typhimurium, which identified some 30 large DNA segments present only in one of these organisms, provided the first evidence that horizontal gene transfer mediated by plasmids or phage was a major driving force during the evolution of these bacteria (45). The genetic material received by the genus Salmonella by way of horizontal gene transfer includes several segments encoding virulence factors. The transferred DNA may vary in size from large genetic elements, such as the pathogenicity islands SPI 1 (34) and SPI 2 (51), phage (38), and virulence plasmids (27), to fimbrial operons located on the chromosome (5), or even single genes inserted in a housekeeping operon (52). Although acquisition of these virulence genes has significantly influenced the evolution of Salmonella serotypes, little is known about their ancestry. The first step in understanding how these virulence factors contributed to shape this successful pathogen is to determine the point in evolution when they were acquired.The classification of the genus Salmonella into serotypes according to the Kauffmann and White scheme is not particularly useful for evolutionary studies since it is based on three surface markers and therefore does not provide a good basis for estimating genetic relatedness among strains (43). The inherent weakness of this system was pointed out by Selander and coworkers, who showed by multilo...

Detection of virulence-associated genes in Salmonella Enteritidis isolates from chicken in South of Brazil

“…Studies concerning the frequency of these genes are important in tracking the adaptation of different serovars of Salmonella spp. to an increasing number of hosts because the acquisition and loss of fimbrial genes are involved in this process (Bäumler et al 1997). The high frequency of sefA is consistent with previous findings (Amini et al 2010, Craciunas et al 2012, and it can be considered a target gene to identify the serovar S. Enteritidis by PCR (Amini et al 2010).…”

“…The highest frequency of P1 profile demonstrate that these genes are widely distributed in the population of Salmonella spp. The presence of more than one genetic profile may suggest acquisitions or deletions of genes in different clones, which could promote different levels of strain adaptation to the host (Bäumler et al 1997, Prager et al 2000, Moussa et al 2013.…”

“…isolates lost and acquire new virulence factors over time in order to adapt to new hosts or to the environment (Bäumler et al 1997, Suez et al 2013. Currently, the foremost challenges are determining how Salmonella acquires virulence factors and what the most important genetic traits conferring virulence to Salmonella spp.…”

Comparative Genetics of the rdar Morphotype inSalmonella

“…For pathogenic Salmonella spp., genome sequencing efforts have identified over 15 distinct fimbrial types (Salmonella enterica serovars Typhimurium [42], Typhi [44], and Paratyphi [41]). Pioneering work by Baumler et al (5) and subsequent genomic comparisons (14,45,61) revealed that most fimbrial operons have a scattered distribution throughout the salmonellae. Early hypotheses that fimbriae were involved in adherence to host cells suggested that numerous fimbrial types would contribute to the host specificities and tissue tropisms of different Salmonella spp.…”

“…The divergent agfDEFG/BAC (csgDEFG/BAC) operons coding for Tafi biosynthesis have been detected in almost all Salmonella isolates tested to date (5,18). Virtually identical operons have also been identified in Escherichia coli and other enterobacterial species (8,49,69).…”