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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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Schematic representation of recombination events with brake-points location in the ompF gene of Yersinia.
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pone-0020546-g003: Schematic representation of recombination events with brake-points location in the ompF gene of Yersinia.

Mentions: As mentioned above, some species produced incongruent 16S rDNA-gyrB and ompF phylogenies. A mix branching pattern can be a sign of recombination, whereas in the case of mutation the gene trees look the same [33]. To verify this assumption, we used four tests (RDP, MaxChi, Chimera, and Geneconv) in the RDP3.34 package for investigation of the ompF gene of all Yersinia groups. We detected four recombination events with brake-points involving three species, Y. intermedia (groups I, II, XIII), Y. aleksiciae (groups XVI and XVII) and Y. mollaretii (groups XVIII and XV) (Fig. 3). From the ompF tree, one can suppose that a recombination event between ompFs of Y. aleksiciae and Y. mollaretii occurred twice. In the first case ompF of Y. mollaretii group XV served as a donor and ompF of Y. aleksiciae group XVII was a recipient, producing a recombinant ompF allele of Y. aleksiciae group XVI. And vice versa, ompF of Y. aleksiciae group XVII served as a donor and ompF of Y. mollaretii group XV was a recipient, giving a recombinant ompF allele of Y. mollaretii group XVIII. This explanation comes from comparison of the branch length and sequence diversity of the group members. To our data, interspecies intragenic recombination was detected for the first time in the genus Yersinia. We observed a complex pattern of recombination in Y. intermedia ompF (groups I, II, XIII). Group I mainly played a parental role in different recombination events, giving ompF variants of Y. intermedia groups II and XIII; other players of the events were not identified in this analysis. It should be noted, that group I strains are most numerous and widely geographically distributed. So it can be supposed, that this ompF variant is more spread and successful in coexistence with mammals including evolutionary newcomers, humans. Acquisition of regions of a successful allele by recombination can be preferred for minor variants (groups II and XIII) when bacterium get into a new niche such as mammals. Interestingly, an extraordinary position of the XIII group on the phylogenetic tree indicates a new origin of the ompF gene not represented by any known Yersinia species. The fact, that this group includes a human isolate (Nr13/84) may be an evidence of occurrence in new niche, human. Noteworthy, it was extremely difficult to reconstruct a scenario of recombination events for all Y. intermedia ompF. This might be a subject of further research, as well as investigation of associations within a specific niche.


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)

Schematic representation of recombination events with brake-points location in the ompF gene of Yersinia.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020546-g003: Schematic representation of recombination events with brake-points location in the ompF gene of Yersinia.
Mentions: As mentioned above, some species produced incongruent 16S rDNA-gyrB and ompF phylogenies. A mix branching pattern can be a sign of recombination, whereas in the case of mutation the gene trees look the same [33]. To verify this assumption, we used four tests (RDP, MaxChi, Chimera, and Geneconv) in the RDP3.34 package for investigation of the ompF gene of all Yersinia groups. We detected four recombination events with brake-points involving three species, Y. intermedia (groups I, II, XIII), Y. aleksiciae (groups XVI and XVII) and Y. mollaretii (groups XVIII and XV) (Fig. 3). From the ompF tree, one can suppose that a recombination event between ompFs of Y. aleksiciae and Y. mollaretii occurred twice. In the first case ompF of Y. mollaretii group XV served as a donor and ompF of Y. aleksiciae group XVII was a recipient, producing a recombinant ompF allele of Y. aleksiciae group XVI. And vice versa, ompF of Y. aleksiciae group XVII served as a donor and ompF of Y. mollaretii group XV was a recipient, giving a recombinant ompF allele of Y. mollaretii group XVIII. This explanation comes from comparison of the branch length and sequence diversity of the group members. To our data, interspecies intragenic recombination was detected for the first time in the genus Yersinia. We observed a complex pattern of recombination in Y. intermedia ompF (groups I, II, XIII). Group I mainly played a parental role in different recombination events, giving ompF variants of Y. intermedia groups II and XIII; other players of the events were not identified in this analysis. It should be noted, that group I strains are most numerous and widely geographically distributed. So it can be supposed, that this ompF variant is more spread and successful in coexistence with mammals including evolutionary newcomers, humans. Acquisition of regions of a successful allele by recombination can be preferred for minor variants (groups II and XIII) when bacterium get into a new niche such as mammals. Interestingly, an extraordinary position of the XIII group on the phylogenetic tree indicates a new origin of the ompF gene not represented by any known Yersinia species. The fact, that this group includes a human isolate (Nr13/84) may be an evidence of occurrence in new niche, human. Noteworthy, it was extremely difficult to reconstruct a scenario of recombination events for all Y. intermedia ompF. This might be a subject of further research, as well as investigation of associations within a specific niche.

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