Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila

<p><em>Legionella pneumophila</em> is an environmental bacterium and the causative agent of Legionnaires’ disease. Previous genomic studies have shown that recombination accounts for a high proportion (&gt;96%) of diversity within several major disease-associated sequence types...

Popoln opis

Bibliografske podrobnosti
Main Authors: David, S, Sánchez-Busó, L, Harris, SR, Marttinen, P, Rusniok, C, Buchrieser, C, Harrison, TG, Parkhill, J
Format: Journal article
Jezik:English
Izdano: Public Library of Science 2017
_version_ 1826293382725500928
author David, S
Sánchez-Busó, L
Harris, SR
Marttinen, P
Rusniok, C
Buchrieser, C
Harrison, TG
Parkhill, J
author_facet David, S
Sánchez-Busó, L
Harris, SR
Marttinen, P
Rusniok, C
Buchrieser, C
Harrison, TG
Parkhill, J
author_sort David, S
collection OXFORD
description <p><em>Legionella pneumophila</em> is an environmental bacterium and the causative agent of Legionnaires’ disease. Previous genomic studies have shown that recombination accounts for a high proportion (&gt;96%) of diversity within several major disease-associated sequence types (STs) of <em>L</em>. <em>pneumophila</em>. This suggests that recombination represents a potentially important force shaping adaptation and virulence. Despite this, little is known about the biological effects of recombination in <em>L</em>. <em>pneumophila</em>, particularly with regards to homologous recombination (whereby genes are replaced with alternative allelic variants). Using newly available population genomic data, we have disentangled events arising from homologous and non-homologous recombination in six major disease-associated STs of <em>L</em>. <em>pneumophila (subsp</em>. <em>pneumophila)</em>, and subsequently performed a detailed characterisation of the dynamics and impact of homologous recombination. We identified genomic “hotspots” of homologous recombination that include regions containing outer membrane proteins, the lipopolysaccharide (LPS) region and Dot/Icm effectors, which provide interesting clues to the selection pressures faced by <em>L</em>. <em>pneumophila</em>. Inference of the origin of the recombined regions showed that isolates have most frequently imported DNA from isolates belonging to their own clade, but also occasionally from other major clades of the same subspecies. This supports the hypothesis that the possibility for horizontal exchange of new adaptations between major clades of the subspecies may have been a critical factor in the recent emergence of several clinically important STs from diverse genomic backgrounds. However, acquisition of recombined regions from another subspecies, <em>L</em>. <em>pneumophila subsp</em>. <em>fraseri</em>, was rarely observed, suggesting the existence of a recombination barrier and/or the possibility of ongoing speciation between the two subspecies. Finally, we suggest that multi-fragment recombination may occur in <em>L</em>. <em>pneumophila</em>, whereby multiple non-contiguous segments that originate from the same molecule of donor DNA are imported into a recipient genome during a single episode of recombination.</p>
first_indexed 2024-03-07T03:29:15Z
format Journal article
id oxford-uuid:ba1ce467-03ea-4dad-b83c-3b3390ccd4d8
institution University of Oxford
language English
last_indexed 2024-03-07T03:29:15Z
publishDate 2017
publisher Public Library of Science
record_format dspace
spelling oxford-uuid:ba1ce467-03ea-4dad-b83c-3b3390ccd4d82022-03-27T05:07:45ZDynamics and impact of homologous recombination on the evolution of Legionella pneumophilaJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:ba1ce467-03ea-4dad-b83c-3b3390ccd4d8EnglishSymplectic Elements at OxfordPublic Library of Science2017David, SSánchez-Busó, LHarris, SRMarttinen, PRusniok, CBuchrieser, CHarrison, TGParkhill, J<p><em>Legionella pneumophila</em> is an environmental bacterium and the causative agent of Legionnaires’ disease. Previous genomic studies have shown that recombination accounts for a high proportion (&gt;96%) of diversity within several major disease-associated sequence types (STs) of <em>L</em>. <em>pneumophila</em>. This suggests that recombination represents a potentially important force shaping adaptation and virulence. Despite this, little is known about the biological effects of recombination in <em>L</em>. <em>pneumophila</em>, particularly with regards to homologous recombination (whereby genes are replaced with alternative allelic variants). Using newly available population genomic data, we have disentangled events arising from homologous and non-homologous recombination in six major disease-associated STs of <em>L</em>. <em>pneumophila (subsp</em>. <em>pneumophila)</em>, and subsequently performed a detailed characterisation of the dynamics and impact of homologous recombination. We identified genomic “hotspots” of homologous recombination that include regions containing outer membrane proteins, the lipopolysaccharide (LPS) region and Dot/Icm effectors, which provide interesting clues to the selection pressures faced by <em>L</em>. <em>pneumophila</em>. Inference of the origin of the recombined regions showed that isolates have most frequently imported DNA from isolates belonging to their own clade, but also occasionally from other major clades of the same subspecies. This supports the hypothesis that the possibility for horizontal exchange of new adaptations between major clades of the subspecies may have been a critical factor in the recent emergence of several clinically important STs from diverse genomic backgrounds. However, acquisition of recombined regions from another subspecies, <em>L</em>. <em>pneumophila subsp</em>. <em>fraseri</em>, was rarely observed, suggesting the existence of a recombination barrier and/or the possibility of ongoing speciation between the two subspecies. Finally, we suggest that multi-fragment recombination may occur in <em>L</em>. <em>pneumophila</em>, whereby multiple non-contiguous segments that originate from the same molecule of donor DNA are imported into a recipient genome during a single episode of recombination.</p>
spellingShingle David, S
Sánchez-Busó, L
Harris, SR
Marttinen, P
Rusniok, C
Buchrieser, C
Harrison, TG
Parkhill, J
Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title_full Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title_fullStr Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title_full_unstemmed Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title_short Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila
title_sort dynamics and impact of homologous recombination on the evolution of legionella pneumophila
work_keys_str_mv AT davids dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT sanchezbusol dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT harrissr dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT marttinenp dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT rusniokc dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT buchrieserc dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT harrisontg dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila
AT parkhillj dynamicsandimpactofhomologousrecombinationontheevolutionoflegionellapneumophila