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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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Location of positively selected sites in OmpF porins of Yersinia.Group VII-Y. enterocolitica WA220; Group XIII-Y. intermedia 1948; Group IX-Y. frederiksenii 4648; Group I-Y. intermedia ATCC 29909; Group X-Y. kristensenii 5868; Group VIII-Y. pseudotuberculosis IP 31758. Sites that show positive selection (P<0.05) are depicted as yellow spheres and (P<0.01)-as red spheres.
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pone-0020546-g005: Location of positively selected sites in OmpF porins of Yersinia.Group VII-Y. enterocolitica WA220; Group XIII-Y. intermedia 1948; Group IX-Y. frederiksenii 4648; Group I-Y. intermedia ATCC 29909; Group X-Y. kristensenii 5868; Group VIII-Y. pseudotuberculosis IP 31758. Sites that show positive selection (P<0.05) are depicted as yellow spheres and (P<0.01)-as red spheres.

Mentions: To determine how the level of selective constraint varies along the ompF gene, we estimated the numbers of synonymous substitutions per synonymous site (dS) and nonsynonymous substitutions per nonsynonymous site (dN) and calculated the dS/dN ratio for the ompF gene. If purifying selection has occurred, a gene has a dS/dN>1. Absence of selection should generate dS/dN = 1. A ratio dS/dN<1 indicates diversifying selection or accelerated evolution [42], [43]. We excluded Yersinia groups with recombination events from analysis and dealt only with six ompF groups of Yersinia (VII, VIII, IX, I, X, XIII). The dS/dN ratio was calculated as an average over all of the codon sites in each ompF group using the Nei-Gojobori method by MEGA 4 of Jukes-Cantor model. Statistical significance was tested by Codon-based Z-test. For all groups we detected approximately identical dS/dN means from 4.224 to 5.748 with p<0.05 of purifying selection. Thus, ompF gene is under strong purifying selection in all six Yersinia groups. Neilsen and Yang method [44], compiled in Sitewise likehood ratio estimation programme [45], was used to identify the sites with the evidence of positive selection in selected ompF groups. The porin protein structures for these groups have been simulated and sites with weak or strong positive selection have been located on the models (Fig. 5).


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)

Location of positively selected sites in OmpF porins of Yersinia.Group VII-Y. enterocolitica WA220; Group XIII-Y. intermedia 1948; Group IX-Y. frederiksenii 4648; Group I-Y. intermedia ATCC 29909; Group X-Y. kristensenii 5868; Group VIII-Y. pseudotuberculosis IP 31758. Sites that show positive selection (P<0.05) are depicted as yellow spheres and (P<0.01)-as red spheres.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020546-g005: Location of positively selected sites in OmpF porins of Yersinia.Group VII-Y. enterocolitica WA220; Group XIII-Y. intermedia 1948; Group IX-Y. frederiksenii 4648; Group I-Y. intermedia ATCC 29909; Group X-Y. kristensenii 5868; Group VIII-Y. pseudotuberculosis IP 31758. Sites that show positive selection (P<0.05) are depicted as yellow spheres and (P<0.01)-as red spheres.
Mentions: To determine how the level of selective constraint varies along the ompF gene, we estimated the numbers of synonymous substitutions per synonymous site (dS) and nonsynonymous substitutions per nonsynonymous site (dN) and calculated the dS/dN ratio for the ompF gene. If purifying selection has occurred, a gene has a dS/dN>1. Absence of selection should generate dS/dN = 1. A ratio dS/dN<1 indicates diversifying selection or accelerated evolution [42], [43]. We excluded Yersinia groups with recombination events from analysis and dealt only with six ompF groups of Yersinia (VII, VIII, IX, I, X, XIII). The dS/dN ratio was calculated as an average over all of the codon sites in each ompF group using the Nei-Gojobori method by MEGA 4 of Jukes-Cantor model. Statistical significance was tested by Codon-based Z-test. For all groups we detected approximately identical dS/dN means from 4.224 to 5.748 with p<0.05 of purifying selection. Thus, ompF gene is under strong purifying selection in all six Yersinia groups. Neilsen and Yang method [44], compiled in Sitewise likehood ratio estimation programme [45], was used to identify the sites with the evidence of positive selection in selected ompF groups. The porin protein structures for these groups have been simulated and sites with weak or strong positive selection have been located on the models (Fig. 5).

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