Where does Neisseria acquire foreign DNA from

An examination of the source of genomic and pathogenic islands and the evolution of the Neisseria genus

Catherine Putonti, Bogdan Nowicki, Michael Shaffer, Yuriy Fofanov, Stella Nowicki

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Background: Pathogenicity islands (PAIs) or genomic islands (GEIs) are considered to be the result of a recent horizontal transfer. Detecting PAIs/GEIs as well as their putative source can provide insight into the organism's pathogenicity within its host. Previously we introduced a tool called S-plot which provides a visual representation of the variation in compositional properties across and between genomic sequences. Utilizing S-plot and new functionality developed here, we examined 18 publicly available Neisseria genomes, including strains of both pathogenic and non-pathogenic species, in order to identify regions of unusual compositional properties (RUCPs) using both a sliding window as well as a gene-by-gene approach. Results: Numerous GEIs and PAIs were identified including virulence genes previously found within the pathogenic Neisseria species. While some genes were conserved amongst all species, only pathogenic species, or an individual species, a number of genes were detected that are unique to an individual strain. While the majority of such genes have an origin unknown, a number of putative sources including pathogenic and capsule-containing bacteria were determined, indicative of gene exchange between Neisseria spp. and other bacteria within their microhabitat. Furthermore, we uncovered evidence that both N. meningitidis and N. gonorrhoeae have separately acquired DNA from their human host. Data suggests that all three Neisseria species have received horizontally transferred elements post-speciation. Conclusions: Using this approach, we were able to not only find previously identified regions of virulence but also new regions which may be contributing to the virulence of the species. This comparative analysis provides a means for tracing the evolutionary history of the acquisition of foreign DNA within this genus. Looking specifically at the RUCPs present within the 18 genomes considered, a stronger similarity between N. meningitidis and N. lactamica is observed, suggesting that N. meningitidis arose before N. gonorrhoeae.

Original languageEnglish (US)
Article number184
JournalBMC Evolutionary Biology
Volume13
Issue number1
DOIs
StatePublished - 2013
Externally publishedYes

Fingerprint

Neisseria
Genomic Islands
genomics
DNA
pathogenicity
genomic islands
gene
pathogenicity islands
Virulence
Genes
virulence
genes
Gonorrhea
genome
Neisseria gonorrhoeae
Genome
Bacteria
Neisseria meningitidis
bacterium
bacteria

Keywords

  • Horizontal gene transfer
  • Neisseria
  • Pathogen-host DNA transfer
  • Pathogenicity islands

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Medicine(all)

Cite this

Where does Neisseria acquire foreign DNA from : An examination of the source of genomic and pathogenic islands and the evolution of the Neisseria genus. / Putonti, Catherine; Nowicki, Bogdan; Shaffer, Michael; Fofanov, Yuriy; Nowicki, Stella.

In: BMC Evolutionary Biology, Vol. 13, No. 1, 184, 2013.

Research output: Contribution to journalArticle

@article{19842beda834444da97a663fb4fcf9e8,
title = "Where does Neisseria acquire foreign DNA from: An examination of the source of genomic and pathogenic islands and the evolution of the Neisseria genus",
abstract = "Background: Pathogenicity islands (PAIs) or genomic islands (GEIs) are considered to be the result of a recent horizontal transfer. Detecting PAIs/GEIs as well as their putative source can provide insight into the organism's pathogenicity within its host. Previously we introduced a tool called S-plot which provides a visual representation of the variation in compositional properties across and between genomic sequences. Utilizing S-plot and new functionality developed here, we examined 18 publicly available Neisseria genomes, including strains of both pathogenic and non-pathogenic species, in order to identify regions of unusual compositional properties (RUCPs) using both a sliding window as well as a gene-by-gene approach. Results: Numerous GEIs and PAIs were identified including virulence genes previously found within the pathogenic Neisseria species. While some genes were conserved amongst all species, only pathogenic species, or an individual species, a number of genes were detected that are unique to an individual strain. While the majority of such genes have an origin unknown, a number of putative sources including pathogenic and capsule-containing bacteria were determined, indicative of gene exchange between Neisseria spp. and other bacteria within their microhabitat. Furthermore, we uncovered evidence that both N. meningitidis and N. gonorrhoeae have separately acquired DNA from their human host. Data suggests that all three Neisseria species have received horizontally transferred elements post-speciation. Conclusions: Using this approach, we were able to not only find previously identified regions of virulence but also new regions which may be contributing to the virulence of the species. This comparative analysis provides a means for tracing the evolutionary history of the acquisition of foreign DNA within this genus. Looking specifically at the RUCPs present within the 18 genomes considered, a stronger similarity between N. meningitidis and N. lactamica is observed, suggesting that N. meningitidis arose before N. gonorrhoeae.",
keywords = "Horizontal gene transfer, Neisseria, Pathogen-host DNA transfer, Pathogenicity islands",
author = "Catherine Putonti and Bogdan Nowicki and Michael Shaffer and Yuriy Fofanov and Stella Nowicki",
year = "2013",
doi = "10.1186/1471-2148-13-184",
language = "English (US)",
volume = "13",
journal = "BMC Evolutionary Biology",
issn = "1471-2148",
publisher = "BioMed Central",
number = "1",

}

TY - JOUR

T1 - Where does Neisseria acquire foreign DNA from

T2 - An examination of the source of genomic and pathogenic islands and the evolution of the Neisseria genus

AU - Putonti, Catherine

AU - Nowicki, Bogdan

AU - Shaffer, Michael

AU - Fofanov, Yuriy

AU - Nowicki, Stella

PY - 2013

Y1 - 2013

N2 - Background: Pathogenicity islands (PAIs) or genomic islands (GEIs) are considered to be the result of a recent horizontal transfer. Detecting PAIs/GEIs as well as their putative source can provide insight into the organism's pathogenicity within its host. Previously we introduced a tool called S-plot which provides a visual representation of the variation in compositional properties across and between genomic sequences. Utilizing S-plot and new functionality developed here, we examined 18 publicly available Neisseria genomes, including strains of both pathogenic and non-pathogenic species, in order to identify regions of unusual compositional properties (RUCPs) using both a sliding window as well as a gene-by-gene approach. Results: Numerous GEIs and PAIs were identified including virulence genes previously found within the pathogenic Neisseria species. While some genes were conserved amongst all species, only pathogenic species, or an individual species, a number of genes were detected that are unique to an individual strain. While the majority of such genes have an origin unknown, a number of putative sources including pathogenic and capsule-containing bacteria were determined, indicative of gene exchange between Neisseria spp. and other bacteria within their microhabitat. Furthermore, we uncovered evidence that both N. meningitidis and N. gonorrhoeae have separately acquired DNA from their human host. Data suggests that all three Neisseria species have received horizontally transferred elements post-speciation. Conclusions: Using this approach, we were able to not only find previously identified regions of virulence but also new regions which may be contributing to the virulence of the species. This comparative analysis provides a means for tracing the evolutionary history of the acquisition of foreign DNA within this genus. Looking specifically at the RUCPs present within the 18 genomes considered, a stronger similarity between N. meningitidis and N. lactamica is observed, suggesting that N. meningitidis arose before N. gonorrhoeae.

AB - Background: Pathogenicity islands (PAIs) or genomic islands (GEIs) are considered to be the result of a recent horizontal transfer. Detecting PAIs/GEIs as well as their putative source can provide insight into the organism's pathogenicity within its host. Previously we introduced a tool called S-plot which provides a visual representation of the variation in compositional properties across and between genomic sequences. Utilizing S-plot and new functionality developed here, we examined 18 publicly available Neisseria genomes, including strains of both pathogenic and non-pathogenic species, in order to identify regions of unusual compositional properties (RUCPs) using both a sliding window as well as a gene-by-gene approach. Results: Numerous GEIs and PAIs were identified including virulence genes previously found within the pathogenic Neisseria species. While some genes were conserved amongst all species, only pathogenic species, or an individual species, a number of genes were detected that are unique to an individual strain. While the majority of such genes have an origin unknown, a number of putative sources including pathogenic and capsule-containing bacteria were determined, indicative of gene exchange between Neisseria spp. and other bacteria within their microhabitat. Furthermore, we uncovered evidence that both N. meningitidis and N. gonorrhoeae have separately acquired DNA from their human host. Data suggests that all three Neisseria species have received horizontally transferred elements post-speciation. Conclusions: Using this approach, we were able to not only find previously identified regions of virulence but also new regions which may be contributing to the virulence of the species. This comparative analysis provides a means for tracing the evolutionary history of the acquisition of foreign DNA within this genus. Looking specifically at the RUCPs present within the 18 genomes considered, a stronger similarity between N. meningitidis and N. lactamica is observed, suggesting that N. meningitidis arose before N. gonorrhoeae.

KW - Horizontal gene transfer

KW - Neisseria

KW - Pathogen-host DNA transfer

KW - Pathogenicity islands

UR - http://www.scopus.com/inward/record.url?scp=84883267833&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84883267833&partnerID=8YFLogxK

U2 - 10.1186/1471-2148-13-184

DO - 10.1186/1471-2148-13-184

M3 - Article

VL - 13

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

IS - 1

M1 - 184

ER -