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

Mauricio H. Pontes, Markus Babst, Robert Lochhead, Kelly Oakeson, Kari Smith, Colin Dale

Research output: Contribution to journalArticlepeer-review

29 Scopus citations

Abstract

Background: Sodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse files (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.

Original languageEnglish (US)
Article numbere3541
JournalPloS one
Volume3
Issue number10
DOIs
StatePublished - Oct 28 2008

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

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