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Acquisition of the lac operon by Salmonella enterica.

Leonard SR, Lacher DW, Lampel KA - BMC Microbiol. (2015)

Bottom Line: 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.Our 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.

View Article: PubMed Central - PubMed

Affiliation: Division of Molecular Biology, Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD, USA. susan.leonard@fda.hhs.gov.

ABSTRACT

Background: Classical 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.

Results: Genetic 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.

Conclusions: Our 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.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic relationships of lacIZY for Salmonella isolates and other Enterobacteriaceae. This neighbor-joining tree was constructed using the Kimura two-parameter model of nucleotide substitution. Bootstrap values based on 500 replications are given at the internal nodes. Salmonella isolates are indicated by the black circles and bold text. The branch connecting the S. enterica subsp. arizonae/diarizonae cluster with the rest of the isolates was shortened to improve the clarity of the relationships and its actual length is given above the dashed line
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Fig1: Phylogenetic relationships of lacIZY for Salmonella isolates and other Enterobacteriaceae. This neighbor-joining tree was constructed using the Kimura two-parameter model of nucleotide substitution. Bootstrap values based on 500 replications are given at the internal nodes. Salmonella isolates are indicated by the black circles and bold text. The branch connecting the S. enterica subsp. arizonae/diarizonae cluster with the rest of the isolates was shortened to improve the clarity of the relationships and its actual length is given above the dashed line

Mentions: Along with characterizing the lac regions and flanking sequence in the genomes, we determined the sequence similarity of the concatenated lacI, lacZ, and lacY genes of the S. enterica isolates and other enteric bacterial species (Fig. 1). As expected, the lac genes carried by the Senftenberg and Montevideo isolates (50262-50265, 50270-50272) displayed a high degree of similarity (99.98 %) with those found on the K. pneumoniae plasmid pK29 (Additional file 1 Figure S1). In general, similar lac region flanking organization corresponds to highest lac gene sequence identity. One notable exception is the lac2 region in the Tennessee isolates 50260 and 50261 where the flanking IS elements, as well as the lengths of the gene upstream of lacI and the lacA remnant, are similar to the K. pneumoniae plasmid pKP007, but the lacIZY gene sequences share only 98 % identity. The S. enterica subsp. diarizonae lac gene sequences share low (73 %) homology with those of the S. enterica subsp. enterica serovars and other Enterobacteriaceae. Clearly, the lac gene sequences do not cluster according to plasmid or chromosomal location (Table 1, Fig. 1).Fig. 1


Acquisition of the lac operon by Salmonella enterica.

Leonard SR, Lacher DW, Lampel KA - BMC Microbiol. (2015)

Phylogenetic relationships of lacIZY for Salmonella isolates and other Enterobacteriaceae. This neighbor-joining tree was constructed using the Kimura two-parameter model of nucleotide substitution. Bootstrap values based on 500 replications are given at the internal nodes. Salmonella isolates are indicated by the black circles and bold text. The branch connecting the S. enterica subsp. arizonae/diarizonae cluster with the rest of the isolates was shortened to improve the clarity of the relationships and its actual length is given above the dashed line
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4549013&req=5

Fig1: Phylogenetic relationships of lacIZY for Salmonella isolates and other Enterobacteriaceae. This neighbor-joining tree was constructed using the Kimura two-parameter model of nucleotide substitution. Bootstrap values based on 500 replications are given at the internal nodes. Salmonella isolates are indicated by the black circles and bold text. The branch connecting the S. enterica subsp. arizonae/diarizonae cluster with the rest of the isolates was shortened to improve the clarity of the relationships and its actual length is given above the dashed line
Mentions: Along with characterizing the lac regions and flanking sequence in the genomes, we determined the sequence similarity of the concatenated lacI, lacZ, and lacY genes of the S. enterica isolates and other enteric bacterial species (Fig. 1). As expected, the lac genes carried by the Senftenberg and Montevideo isolates (50262-50265, 50270-50272) displayed a high degree of similarity (99.98 %) with those found on the K. pneumoniae plasmid pK29 (Additional file 1 Figure S1). In general, similar lac region flanking organization corresponds to highest lac gene sequence identity. One notable exception is the lac2 region in the Tennessee isolates 50260 and 50261 where the flanking IS elements, as well as the lengths of the gene upstream of lacI and the lacA remnant, are similar to the K. pneumoniae plasmid pKP007, but the lacIZY gene sequences share only 98 % identity. The S. enterica subsp. diarizonae lac gene sequences share low (73 %) homology with those of the S. enterica subsp. enterica serovars and other Enterobacteriaceae. Clearly, the lac gene sequences do not cluster according to plasmid or chromosomal location (Table 1, Fig. 1).Fig. 1

Bottom Line: 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.Our 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.

View Article: PubMed Central - PubMed

Affiliation: Division of Molecular Biology, Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD, USA. susan.leonard@fda.hhs.gov.

ABSTRACT

Background: Classical 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.

Results: Genetic 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.

Conclusions: Our 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.

No MeSH data available.


Related in: MedlinePlus