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Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius. PLoS One 2008;3(10):e3541 PMID: 18958153 PMCID: PMC2568817

Pubmed ID

18958153

Abstract

BACKGROUND: 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.

METHODOLOGY/PRINCIPAL FINDINGS: 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.

CONCLUSIONS/SIGNIFICANCE: 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.

Author List

Pontes MH, Babst M, Lochhead R, Oakeson K, Smith K, Dale C

Author

Robert Lochhead PhD Assistant Professor in the Microbiology and Immunology department at Medical College of Wisconsin




Scopus

2-s2.0-56149106746   21 Citations

MESH terms used to index this publication - Major topics in bold

Animals
Enterobacteriaceae
Gene Expression Profiling
Gene Expression Regulation, Bacterial
Host-Pathogen Interactions
Insecta
Models, Biological
Oligonucleotide Array Sequence Analysis
Oxidative Stress
Quorum Sensing
Symbiosis
Tsetse Flies
jenkins-FCD Prod-256 97250b83e4554f37bec91ca291f44ff4aedcc508