A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.

Legionella encodes multiple classes of Type IV Secretion Systems (T4SSs), including the Dot/Icm protein secretion system that is essential for intracellular multiplication in amoebal and human hosts. Other T4SSs not essential for virulence are thought to facilitate the acquisition of niche-specific...

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Main Authors: Bryan A Wee, Megan Woolfit, Scott A Beatson, Nicola K Petty
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3864950?pdf=render
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spelling doaj-fac9558d607947f2abde74163b07d0ae2020-11-25T01:53:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-01812e8222110.1371/journal.pone.0082221A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.Bryan A WeeMegan WoolfitScott A BeatsonNicola K PettyLegionella encodes multiple classes of Type IV Secretion Systems (T4SSs), including the Dot/Icm protein secretion system that is essential for intracellular multiplication in amoebal and human hosts. Other T4SSs not essential for virulence are thought to facilitate the acquisition of niche-specific adaptation genes including the numerous effector genes that are a hallmark of this genus. Previously, we identified two novel gene clusters in the draft genome of Legionella pneumophila strain 130b that encode homologues of a subtype of T4SS, the genomic island-associated T4SS (GI-T4SS), usually associated with integrative and conjugative elements (ICE). In this study, we performed genomic analyses of 14 homologous GI-T4SS clusters found in eight publicly available Legionella genomes and show that this cluster is unusually well conserved in a region of high plasticity. Phylogenetic analyses show that Legionella GI-T4SSs are substantially divergent from other members of this subtype of T4SS and represent a novel clade of GI-T4SSs only found in this genus. The GI-T4SS was found to be under purifying selection, suggesting it is functional and may play an important role in the evolution and adaptation of Legionella. Like other GI-T4SSs, the Legionella clusters are also associated with ICEs, but lack the typical integration and replication modules of related ICEs. The absence of complete replication and DNA pre-processing modules, together with the presence of Legionella-specific regulatory elements, suggest the Legionella GI-T4SS-associated ICE is unique and may employ novel mechanisms of regulation, maintenance and excision. The Legionella GI-T4SS cluster was found to be associated with several cargo genes, including numerous antibiotic resistance and virulence factors, which may confer a fitness benefit to the organism. The in-silico characterisation of this new T4SS furthers our understanding of the diversity of secretion systems involved in the frequent horizontal gene transfers that allow Legionella to adapt to and exploit diverse environmental niches.http://europepmc.org/articles/PMC3864950?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Bryan A Wee
Megan Woolfit
Scott A Beatson
Nicola K Petty
spellingShingle Bryan A Wee
Megan Woolfit
Scott A Beatson
Nicola K Petty
A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
PLoS ONE
author_facet Bryan A Wee
Megan Woolfit
Scott A Beatson
Nicola K Petty
author_sort Bryan A Wee
title A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
title_short A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
title_full A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
title_fullStr A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
title_full_unstemmed A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella.
title_sort distinct and divergent lineage of genomic island-associated type iv secretion systems in legionella.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Legionella encodes multiple classes of Type IV Secretion Systems (T4SSs), including the Dot/Icm protein secretion system that is essential for intracellular multiplication in amoebal and human hosts. Other T4SSs not essential for virulence are thought to facilitate the acquisition of niche-specific adaptation genes including the numerous effector genes that are a hallmark of this genus. Previously, we identified two novel gene clusters in the draft genome of Legionella pneumophila strain 130b that encode homologues of a subtype of T4SS, the genomic island-associated T4SS (GI-T4SS), usually associated with integrative and conjugative elements (ICE). In this study, we performed genomic analyses of 14 homologous GI-T4SS clusters found in eight publicly available Legionella genomes and show that this cluster is unusually well conserved in a region of high plasticity. Phylogenetic analyses show that Legionella GI-T4SSs are substantially divergent from other members of this subtype of T4SS and represent a novel clade of GI-T4SSs only found in this genus. The GI-T4SS was found to be under purifying selection, suggesting it is functional and may play an important role in the evolution and adaptation of Legionella. Like other GI-T4SSs, the Legionella clusters are also associated with ICEs, but lack the typical integration and replication modules of related ICEs. The absence of complete replication and DNA pre-processing modules, together with the presence of Legionella-specific regulatory elements, suggest the Legionella GI-T4SS-associated ICE is unique and may employ novel mechanisms of regulation, maintenance and excision. The Legionella GI-T4SS cluster was found to be associated with several cargo genes, including numerous antibiotic resistance and virulence factors, which may confer a fitness benefit to the organism. The in-silico characterisation of this new T4SS furthers our understanding of the diversity of secretion systems involved in the frequent horizontal gene transfers that allow Legionella to adapt to and exploit diverse environmental niches.
url http://europepmc.org/articles/PMC3864950?pdf=render
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