Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.

<h4>Background</h4>Sodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse flies (Glossina spp.), uses an acylated homoserine lactone (AHL)-based quorum sensing system to modulate gene expression in accordance with bacterial cell density. The S. glossinidius quoru...

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Main Authors: Mauricio H Pontes, Markus Babst, Robert Lochhead, Kelly Oakeson, Kari Smith, Colin Dale
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2008-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18958153/?tool=EBI
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spelling doaj-e35ceb136d9e4359b1d557bcacf7e0512021-03-03T22:44:45ZengPublic Library of Science (PLoS)PLoS ONE1932-62032008-01-01310e354110.1371/journal.pone.0003541Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.Mauricio H PontesMarkus BabstRobert LochheadKelly OakesonKari SmithColin Dale<h4>Background</h4>Sodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse flies (Glossina spp.), uses an acylated homoserine lactone (AHL)-based quorum sensing system to modulate gene expression in accordance with bacterial cell density. The S. glossinidius quorum sensing system relies on the function of two regulatory proteins; SogI (a LuxI homolog) synthesizes a signaling molecule, characterized as N-(3-oxohexanoyl) homoserine lactone (OHHL), and SogR1 (a LuxR homolog) interacts with OHHL to modulate transcription of specific target genes.<h4>Methodology/principal findings</h4>We used a tiling microarray to analyze the S. glossinidius transcriptome in the presence and absence of exogenous OHHL. The major finding is that OHHL increases transcription of a large number of genes that are known to be involved in the oxidative stress response. We also show that the obligate symbiont of the rice weevil, Sitophilus oryzae (SOPE), maintains copies of the quorum sensing regulatory genes that are found in S. glossinidius. Molecular evolutionary analyses indicate that these sequences are evolving under stabilizing selection, consistent with the maintenance of their functions in the SOPE symbiosis. Finally, the expression studies in S. glossinidius also reveal that quorum sensing regulates the expression of a cryptic, degenerate gene (carA) that arose from an ancient deletion in the last common ancestor of S. glossinidius and SOPE.<h4>Conclusions/significance</h4>This oxidative stress response is likely mandated under conditions of dense intracellular symbiont infection, when intense metabolic activity is expected to generate a heavy oxidative burden. Such conditions are known to arise in the bacteriocytes of grain weevils, which harbor dense intracellular infections of symbiotic bacteria that are closely related to S. glossinidius. The presence of a degenerate carA sequence in S. glossinidius and SOPE indicates the potential for neofunctionalization to occur during the process of genome degeneration.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18958153/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Mauricio H Pontes
Markus Babst
Robert Lochhead
Kelly Oakeson
Kari Smith
Colin Dale
spellingShingle Mauricio H Pontes
Markus Babst
Robert Lochhead
Kelly Oakeson
Kari Smith
Colin Dale
Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
PLoS ONE
author_facet Mauricio H Pontes
Markus Babst
Robert Lochhead
Kelly Oakeson
Kari Smith
Colin Dale
author_sort Mauricio H Pontes
title Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
title_short Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
title_full Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
title_fullStr Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
title_full_unstemmed Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius.
title_sort quorum sensing primes the oxidative stress response in the insect endosymbiont, sodalis glossinidius.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2008-01-01
description <h4>Background</h4>Sodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse flies (Glossina spp.), uses an acylated homoserine lactone (AHL)-based quorum sensing system to modulate gene expression in accordance with bacterial cell density. The S. glossinidius quorum sensing system relies on the function of two regulatory proteins; SogI (a LuxI homolog) synthesizes a signaling molecule, characterized as N-(3-oxohexanoyl) homoserine lactone (OHHL), and SogR1 (a LuxR homolog) interacts with OHHL to modulate transcription of specific target genes.<h4>Methodology/principal findings</h4>We used a tiling microarray to analyze the S. glossinidius transcriptome in the presence and absence of exogenous OHHL. The major finding is that OHHL increases transcription of a large number of genes that are known to be involved in the oxidative stress response. We also show that the obligate symbiont of the rice weevil, Sitophilus oryzae (SOPE), maintains copies of the quorum sensing regulatory genes that are found in S. glossinidius. Molecular evolutionary analyses indicate that these sequences are evolving under stabilizing selection, consistent with the maintenance of their functions in the SOPE symbiosis. Finally, the expression studies in S. glossinidius also reveal that quorum sensing regulates the expression of a cryptic, degenerate gene (carA) that arose from an ancient deletion in the last common ancestor of S. glossinidius and SOPE.<h4>Conclusions/significance</h4>This oxidative stress response is likely mandated under conditions of dense intracellular symbiont infection, when intense metabolic activity is expected to generate a heavy oxidative burden. Such conditions are known to arise in the bacteriocytes of grain weevils, which harbor dense intracellular infections of symbiotic bacteria that are closely related to S. glossinidius. The presence of a degenerate carA sequence in S. glossinidius and SOPE indicates the potential for neofunctionalization to occur during the process of genome degeneration.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18958153/?tool=EBI
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