Abstract

BackgroundClassical bacteriological characteristics of Salmonella enterica indicate that the members of this species are unable to utilize lactose as a carbon source. However, lactose-fermenting (Lac+) strains of several Salmonella serovars have been isolated from different foodborne outbreaks as well as different geographical regions worldwide. In the present study, we sequenced the genomes of 13 Lac + S. enterica isolates and characterized the lac region, comparing it to the lac region in other enteric bacterial species.ResultsGenetic analysis of the lac operons in the S. enterica genomes revealed that they all contain intact lacI, lacZ, and lacY genes. However, lacA was truncated in all of the S. enterica subsp. enterica isolates, encoding a 56 amino acid peptide rather than the full length 220 amino acid LacA protein. Molecular analyses of the 13 isolates revealed that the lac operon resided on a plasmid in some strains and in others was integrated into the bacterial chromosome. In most cases, an insertion sequence flanked at least one end of the operon. Interestingly, the S. enterica Montevideo and S. enterica Senftenberg isolates were found to harbor a plasmid with a high degree of sequence similarity to a plasmid from Klebsiella pneumoniae strain NK29 that also harbors the lac operon. In addition, two S. enterica Tennessee isolates carried two copies of the lac operon. Phylogenetic analysis based on lacIZY gene sequences determines distinct clusters, and reveals a greater correlation between lacIZY sequence and flanking organization than with either bacterial species or genomic location.ConclusionsOur results indicate that the lac region is highly mobile among Enterobacteriaceae and demonstrate that the Lac + S. enterica subsp. enterica serovars acquired the lac region through parallel events. The acquisition of the lac operon by several S. enterica serovars may be indicative of environmental adaptation by these bacteria.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-015-0511-8) contains supplementary material, which is available to authorized users.

Highlights

  • Classical bacteriological characteristics of Salmonella enterica indicate that the members of this species are unable to utilize lactose as a carbon source

  • We demonstrated that with the exception of the S. enterica subsp. diarizonae isolates, the lac region is flanked by insertion sequences and that this entire genetic region is itself carried within a mobile genetic element

  • The lactose-fermenting ability exhibited by these isolates is not surprising since 85 % of S. enterica subsp. diarizonae are known to be Lac + [18], a much higher percentage than the 0.8 % reported for S. enterica subsp. enterica [4]

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Summary

Introduction

Classical bacteriological characteristics of Salmonella enterica indicate that the members of this species are unable to utilize lactose as a carbon source. Lactose-fermenting (Lac+) strains of several Salmonella serovars have been isolated from different foodborne outbreaks as well as different geographical regions worldwide. Infrequent, outbreaks caused by lactose-fermenting (Lac+) S. enterica have been reported [5,6,7], including a recent outbreak due to contamination of peanut butter with S. enterica Tennessee that sickened 715 individuals [8]. The lac operon, comprised of the genes lacZ, lacY, and lacA, encodes the proteins responsible for lactose utilization. The lac region includes the lacI gene, located just upstream of lacZ, that encodes a repressor that regulates transcription of the lac operon. While the lac region is located in the E. coli chromosome, it has been reported to be carried on a plasmid in several Enterobacteriaceae including two serovars of S. enterica [12]. Cornelis et al determined that the lacI, lacZ, and lacY genes, along with flanking

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