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Comparative genomics reveals an SNP potentially leading to phenotypic diversity of Salmonella enterica serovar Enteritidis.

ABSTRACT: An SNP is a spontaneous genetic change having a potential to modify the functions of the original genes and to lead to phenotypic diversity of bacteria in nature. In this study, a phylogenetic analysis of Salmonella enterica serovar Enteritidis, a major food-borne pathogen, showed that eight strains of S. Enteritidis isolated in South Korea, including FORC_075 and FORC_078, have almost identical genome sequences. Interestingly, however, the abilities of FORC_075 to form biofilms and red, dry and rough (RDAR) colonies were significantly impaired, resulting in phenotypic differences among the eight strains. Comparative genomic analyses revealed that one of the non-synonymous SNPs unique to FORC_075 has occurred in envZ, which encodes a sensor kinase of the EnvZ/OmpR two-component system. The SNP in envZ leads to an amino acid change from Pro248 (CCG) in other strains including FORC_078 to Leu248 (CTG) in FORC_075. Allelic exchange of envZ between FORC_075 and FORC_078 identified that the SNP in envZ is responsible for the impaired biofilm- and RDAR colony-forming abilities of S. Enteritidis. Biochemical analyses demonstrated that the SNP in envZ significantly increases the phosphorylated status of OmpR in S. Enteritidis and alters the expression of the OmpR regulon. Phenotypic analyses further identified that the SNP in envZ decreases motility of S. Enteritidis but increases its adhesion and invasion to both human epithelial cells and murine macrophage cells. In addition to an enhancement of infectivity to the host cells, survival under acid stress was also elevated by the SNP in envZ. Together, these results suggest that the natural occurrence of the SNP in envZ could contribute to phenotypic diversity of S. Enteritidis, possibly improving its fitness and pathogenesis.

SUBMITTER: Ko D

PROVIDER: S-EPMC8209725 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Salmonella enterica serovar Enteritidis (S. Enteritidis) has caused major epidemics of gastrointestinal infection in many different countries. In this study we investigate genome divergence and pathogenic potential in S. Enteritidis isolated before, during and after an epidemic in Uruguay.266 S. Enteritidis isolates were genotyped using RAPD-PCR and a selection were subjected to PFGE analysis. From these, 29 isolates spanning different periods, genetic profiles and sources of isolation were assayed for their ability to infect human epithelial cells and subjected to comparative genomic hybridization using a Salmonella pan-array and the sequenced strain S. Enteritidis PT4 P125109 as reference. Six other isolates from distant countries were included as external comparators.Two hundred and thirty three chromosomal genes as well as the virulence plasmid were found as variable among S. Enteritidis isolates. Ten out of the 16 chromosomal regions that varied between different isolates correspond to phage-like regions. The 2 oldest pre-epidemic isolates lack phage SE20 and harbour other phage encoded genes that are absent in the sequenced strain. Besides variation in prophage, we found variation in genes involved in metabolism and bacterial fitness. Five epidemic strains lack the complete Salmonella virulence plasmid. Significantly, strains with indistinguishable genetic patterns still showed major differences in their ability to infect epithelial cells, indicating that the approach used was insufficient to detect the genetic basis of this differential behaviour.The recent epidemic of S. Enteritidis infection in Uruguay has been driven by the introduction of closely related strains of phage type 4 lineage. Our results confirm previous reports demonstrating a high degree of genetic homogeneity among S. Enteritidis isolates. However, 10 of the regions of variability described here are for the first time reported as being variable in S. Enteritidis. In particular, the oldest pre-epidemic isolates carry phage-associated genetic regions not previously reported in S. Enteritidis. Overall, our results support the view that phages play a crucial role in the generation of genetic diversity in S. Enteritidis and that phage SE20 may be a key marker for the emergence of particular isolates capable of causing epidemics.

Project description:Salmonella enterica serovar Enteritidis has emerged as a significant foodborne pathogen throughout the world and is commonly characterized by phage typing. In Canada phage types (PT) 4, 8 and 13 predominate and in 2005 a large foodborne PT13 outbreak occurred in the province of Ontario. The ability to link strains during this outbreak was difficult due to the apparent clonality of PT13 isolates in Canada, as there was a single dominant pulsed-field gel electrophoresis (PFGE) profile amongst epidemiologically linked human and food isolates as well as concurrent sporadic strains. The aim of this study was to perform comparative genomic hybridization (CGH), DNA sequence-based typing (SBT) genomic analyses, plasmid analyses, and automated repetitive sequence-based PCR (rep-PCR) to identify epidemiologically significant traits capable of subtyping S. Enteritidis PT13.CGH using an oligonucleotide array based upon chromosomal coding sequences of S. enterica serovar Typhimurium strain LT2 and the Salmonella genomic island 1 successfully determined major genetic differences between S. Typhimurium and S. Enteritidis PT13, but no significant strain-to-strain differences were observed between S. Enteritidis PT13 isolates. Individual loci (safA and fliC) that were identified as potentially divergent in the CGH data set were sequenced in a panel of S. Enteritidis strains, and no differences were detected between the PT13 strains. Additional sequence-based typing was performed at the fimA, mdh, manB, cyaA, citT, caiC, dmsA, ratA and STM0660 loci. Similarly, no diversity was observed amongst PT13 strains. Variation in plasmid content between PT13 strains was observed, but macrorestriction with BglII did not identify further differences. Automated rep-PCR patterns were variable between serovars, but S. Enteritidis PT13 strains could not be differentiated.None of the methods identified any significant variation between PT13 strains. Greater than 11,300 base pairs of sequence for each of seven S. Enteritidis PT13 strains were analyzed without detecting a single polymorphic site, although diversity between different phage types of S. Enteritidis was observed. These data suggest that Canadian S. Enteritidis PT13 strains are highly related genetically.

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Comparative genomics reveals an SNP potentially leading to phenotypic diversity of Salmonella enterica serovar Enteritidis.

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