Interbacterial signaling via Burkholderia contact dependent growth inhibition system proteins

Erin C. Garcia, Andrew I. Perault, Sara A. Marlatt, Peggy A. Cotter

Research output: Contribution to journalArticlepeer-review

74 Scopus citations

Abstract

In prokaryotes and eukaryotes, cell-cell communication and recognition of self are critical to coordinate multicellular functions. Although kin and kind discrimination are increasingly appreciated to shape naturally occurring microbe populations, the underlying mechanisms that govern these interbacterial interactions are insufficiently understood. Here, we identify a mechanism of interbacterial signal transduction that is mediated by contact-dependent growth inhibition (CDI) system proteins. CDI systems have been characterized by their ability to deliver a polymorphic protein toxin into the cytoplasm of a neighboring bacterium, resulting in growth inhibition or death unless the recipient bacterium produces a corresponding immunity protein. Using the model organism Burkholderia thailandensis, we show that delivery of a catalytically active CDI system toxin to immune (self) bacteria results in gene expression and phenotypic changes within the recipient cells. Termed contact-dependent signaling (CDS), this response promotes biofilm formation and other community-associated behaviors. Engineered strains that are isogenic with B. thailandensis, except the DNA region encoding the toxin and immunity proteins, did not display CDS, whereas a strain of Burkholderia dolosa producing a nearly identical toxin-immunity pair induced signaling in B. thailandensis. Our data indicate that bcpAIOB loci confer dual benefits; they direct antagonism toward non-self bacteria and promote cooperation between self bacteria, with self being defined by the bcpAIOB allele and not by genealogic relatedness.

Original languageEnglish
Pages (from-to)8296-8301
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number29
DOIs
StatePublished - Jul 19 2016

Bibliographical note

Funding Information:
We thank the University of North Carolina Microscopy Services Laboratory for microscopy assistance; John LiPuma (University of Michigan) for providing Burkholderia dolosa AU0158; Joan Mecsas (Tufts University) for a method suggestion; Eric Garcia for RNA isolation expertise and reagents; Eliza Mason for pGFlipCm construction; and Alecia Septer and members of the P.A.C. laboratory for insightful discussion. RNA sequencing was performed by the staff at the University of North Carolina High Throughput Sequencing Facility. This work was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Awards R21 AI093154 and R21 AI112764 (to P.A.C.) and F32 AI096728 (to E.C.G.). S.A.M. was supported by Grant K12GM00678 from the Training, Workforce Development, and Diversity division of the National Institute of General Medical Sciences of the NIH.

Keywords

  • Biofilm
  • Contact-dependent competition
  • Signal transduction
  • Sociomicrobiology
  • Two-partner secretion

ASJC Scopus subject areas

  • General

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