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Trends of the major porin gene (ompF) evolution: insight from the genus Yersinia.

Stenkova AM, Isaeva MP, Shubin FN, Rasskazov VA, Rakin AV - PLoS ONE (2011)

Bottom Line: Very high congruence in the tree topologies was observed for Y. enterocolitica, Y. kristensenii, Y. ruckeri, indicating that intragenic recombination in these species had no effect on the ompF gene.A significant level of intra- and interspecies recombination was found for Y. aleksiciae, Y. intermedia and Y. mollaretii.To our knowledge, this is a first investigation of diversity of the porin gene covering the whole genus of the family Enterobacteriaceae.

View Article: PubMed Central - PubMed

Affiliation: Pacific Institute of Bioorganic Chemistry, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russian Federation. stenkova@gmail.com

ABSTRACT
OmpF is one of the major general porins of Enterobacteriaceae that belongs to the first line of bacterial defense and interactions with the biotic as well as abiotic environments. Porins are surface exposed and their structures strongly reflect the history of multiple interactions with the environmental challenges. Unfortunately, little is known on diversity of porin genes of Enterobacteriaceae and the genus Yersinia especially. We analyzed the sequences of the ompF gene from 73 Yersinia strains covering 14 known species. The phylogenetic analysis placed most of the Yersinia strains in the same line assigned by 16S rDNA-gyrB tree. Very high congruence in the tree topologies was observed for Y. enterocolitica, Y. kristensenii, Y. ruckeri, indicating that intragenic recombination in these species had no effect on the ompF gene. A significant level of intra- and interspecies recombination was found for Y. aleksiciae, Y. intermedia and Y. mollaretii. Our analysis shows that the ompF gene of Yersinia has evolved with nonrandom mutational rate under purifying selection. However, several surface loops in the OmpF porin contain positively selected sites, which very likely reflect adaptive diversification Yersinia to their ecological niches. To our knowledge, this is a first investigation of diversity of the porin gene covering the whole genus of the family Enterobacteriaceae. This study demonstrates that recombination and positive selection both contribute to evolution of ompF, but the relative contribution of these evolutionary forces are different among Yersinia species.

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Phylogenetic relationships among ompF sequences of Yersinia.The unrooted dendrogram was generated using neighbour-joining algorithm. The evolutionary distances were computed using the Kimura 2-parameter method and are expressed in number of base substitutions per site. The percentages of replicate trees in which the associated taxa clustered together in the bootstrap test are shown in nodes.
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pone-0020546-g002: Phylogenetic relationships among ompF sequences of Yersinia.The unrooted dendrogram was generated using neighbour-joining algorithm. The evolutionary distances were computed using the Kimura 2-parameter method and are expressed in number of base substitutions per site. The percentages of replicate trees in which the associated taxa clustered together in the bootstrap test are shown in nodes.

Mentions: We investigated phylogenetic relationships and recombination of the ompF gene from all Yersinia strains (Table 1). The ompF gene was amplified, using primers, derived from a CLUSTALX alignment of the published ompF nucleotide sequences. 73 complete coding nucleotide sequences of the ompF gene were aligned to infer ompF phylogenetic tree. We found 62 unique nucleotide alleles of the ompF gene (table 1), which clustered into 18 groups on the tree (Fig. 2). Though different algorithms and clustering methods produced similar topologies of the ompF tree, phylogenetic clustering of the strains performed by neighbor-joining method with Kimura 2-parameter algorithm gave the highest bootstrap values. With the exception of five species, Y. similis, Y. intermedia, Y. mollaretii, Y. frederiksenii and Y. aleksiciae, all strains that belong to the same Yersinia species were clustered in one group. Five strains of Y. ruckeri clustered together in a distinct group V and showed the intragroup distance mean by 0.002 and the largest intergroup genetic distance means from 0.166 to 0.197. It reaffirmed that Y. ruckeri has been fairly clonal and genetically the most distant species within the genus [26], [29]. For Y. enterocolitica (group VII) the intraspecies genetic distance mean was 0.029, and the groups means of 0.097–0.166. Phylogenetic grouping of Y. enterocolitica ompF genes exactly replicated that of 16S rDNA-gyrB sequences with division in two subspecies, Y. enterocolitica subsp. palearctica (Y11, 1234, 2974/81, 6579, 1245, 2720/87, and 1215) and Y. enterocolitica subsp. enterocolitica (WA220 and ATCC 8081), supported by a high bootstrap value (100%). Interestingly, in both phylogenetic trees, Y. enterocolitica subsp. palearctica clearly splits into two lines (bootstrap value 100%), one of them was only formed by Y. enterocolitica strains (1215, 1234, and 1245) isolated in Russian Far-East. Strains of Y. kristensenii formed group X with intragroup distance mean 0.020, and intergroup distance means 0.072–0.183. The Y. bercovieri (group VI), Y. rohdei (group XIV) and Y. aldovae (group IV) were represented by only two strains and the within and between group distance means were up to 0.009 and 0.068–0.188, respectively. The strains of Y. pestis, Y. pseudotuberculosis and Y. similis grouped together (group VIII) with intragroup distance mean of 0.037, and between group distance means being 0.138–0.196. The VIII group splits into two subgroups with bootstrap value of 100%. One of these subgroups included two Y. pseudotuberculosis strains IP32953, IP31758 and Y. similis Y239, while the other-all Y. pestis strains and Y. pseudotuberculosis YPIII. This ompF tree topology did not correlate with the 16S rDNA-gyrB tree branching, possibly indicating interspecies recombination between Y. pseudotuberculosis and Y. similis, or/and diversification of the ompF gene of Y. pseudotuberculosis before emergence of Y. pestis by adaptive evolution.


Trends of the major porin gene (ompF) evolution: insight from the genus Yersinia.

Stenkova AM, Isaeva MP, Shubin FN, Rasskazov VA, Rakin AV - PLoS ONE (2011)

Phylogenetic relationships among ompF sequences of Yersinia.The unrooted dendrogram was generated using neighbour-joining algorithm. The evolutionary distances were computed using the Kimura 2-parameter method and are expressed in number of base substitutions per site. The percentages of replicate trees in which the associated taxa clustered together in the bootstrap test are shown in nodes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105102&req=5

pone-0020546-g002: Phylogenetic relationships among ompF sequences of Yersinia.The unrooted dendrogram was generated using neighbour-joining algorithm. The evolutionary distances were computed using the Kimura 2-parameter method and are expressed in number of base substitutions per site. The percentages of replicate trees in which the associated taxa clustered together in the bootstrap test are shown in nodes.
Mentions: We investigated phylogenetic relationships and recombination of the ompF gene from all Yersinia strains (Table 1). The ompF gene was amplified, using primers, derived from a CLUSTALX alignment of the published ompF nucleotide sequences. 73 complete coding nucleotide sequences of the ompF gene were aligned to infer ompF phylogenetic tree. We found 62 unique nucleotide alleles of the ompF gene (table 1), which clustered into 18 groups on the tree (Fig. 2). Though different algorithms and clustering methods produced similar topologies of the ompF tree, phylogenetic clustering of the strains performed by neighbor-joining method with Kimura 2-parameter algorithm gave the highest bootstrap values. With the exception of five species, Y. similis, Y. intermedia, Y. mollaretii, Y. frederiksenii and Y. aleksiciae, all strains that belong to the same Yersinia species were clustered in one group. Five strains of Y. ruckeri clustered together in a distinct group V and showed the intragroup distance mean by 0.002 and the largest intergroup genetic distance means from 0.166 to 0.197. It reaffirmed that Y. ruckeri has been fairly clonal and genetically the most distant species within the genus [26], [29]. For Y. enterocolitica (group VII) the intraspecies genetic distance mean was 0.029, and the groups means of 0.097–0.166. Phylogenetic grouping of Y. enterocolitica ompF genes exactly replicated that of 16S rDNA-gyrB sequences with division in two subspecies, Y. enterocolitica subsp. palearctica (Y11, 1234, 2974/81, 6579, 1245, 2720/87, and 1215) and Y. enterocolitica subsp. enterocolitica (WA220 and ATCC 8081), supported by a high bootstrap value (100%). Interestingly, in both phylogenetic trees, Y. enterocolitica subsp. palearctica clearly splits into two lines (bootstrap value 100%), one of them was only formed by Y. enterocolitica strains (1215, 1234, and 1245) isolated in Russian Far-East. Strains of Y. kristensenii formed group X with intragroup distance mean 0.020, and intergroup distance means 0.072–0.183. The Y. bercovieri (group VI), Y. rohdei (group XIV) and Y. aldovae (group IV) were represented by only two strains and the within and between group distance means were up to 0.009 and 0.068–0.188, respectively. The strains of Y. pestis, Y. pseudotuberculosis and Y. similis grouped together (group VIII) with intragroup distance mean of 0.037, and between group distance means being 0.138–0.196. The VIII group splits into two subgroups with bootstrap value of 100%. One of these subgroups included two Y. pseudotuberculosis strains IP32953, IP31758 and Y. similis Y239, while the other-all Y. pestis strains and Y. pseudotuberculosis YPIII. This ompF tree topology did not correlate with the 16S rDNA-gyrB tree branching, possibly indicating interspecies recombination between Y. pseudotuberculosis and Y. similis, or/and diversification of the ompF gene of Y. pseudotuberculosis before emergence of Y. pestis by adaptive evolution.

Bottom Line: Very high congruence in the tree topologies was observed for Y. enterocolitica, Y. kristensenii, Y. ruckeri, indicating that intragenic recombination in these species had no effect on the ompF gene.A significant level of intra- and interspecies recombination was found for Y. aleksiciae, Y. intermedia and Y. mollaretii.To our knowledge, this is a first investigation of diversity of the porin gene covering the whole genus of the family Enterobacteriaceae.

View Article: PubMed Central - PubMed

Affiliation: Pacific Institute of Bioorganic Chemistry, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russian Federation. stenkova@gmail.com

ABSTRACT
OmpF is one of the major general porins of Enterobacteriaceae that belongs to the first line of bacterial defense and interactions with the biotic as well as abiotic environments. Porins are surface exposed and their structures strongly reflect the history of multiple interactions with the environmental challenges. Unfortunately, little is known on diversity of porin genes of Enterobacteriaceae and the genus Yersinia especially. We analyzed the sequences of the ompF gene from 73 Yersinia strains covering 14 known species. The phylogenetic analysis placed most of the Yersinia strains in the same line assigned by 16S rDNA-gyrB tree. Very high congruence in the tree topologies was observed for Y. enterocolitica, Y. kristensenii, Y. ruckeri, indicating that intragenic recombination in these species had no effect on the ompF gene. A significant level of intra- and interspecies recombination was found for Y. aleksiciae, Y. intermedia and Y. mollaretii. Our analysis shows that the ompF gene of Yersinia has evolved with nonrandom mutational rate under purifying selection. However, several surface loops in the OmpF porin contain positively selected sites, which very likely reflect adaptive diversification Yersinia to their ecological niches. To our knowledge, this is a first investigation of diversity of the porin gene covering the whole genus of the family Enterobacteriaceae. This study demonstrates that recombination and positive selection both contribute to evolution of ompF, but the relative contribution of these evolutionary forces are different among Yersinia species.

Show MeSH
Related in: MedlinePlus