Interbacterial signaling via Burkholderia contact-dependent growth inhibition system proteins

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.signal transduction | sociomicrobiology | contact-dependent competition | two-partner secretion | biofilm

Nice or nasty: Protein translocation between bacteria and the different forms of response

“…This finding advances our understanding of the regulation of the system that is known to be activated stochastically (12) and in response to bacterial density (13). The data on the differential expression of genes support the phenotypic changes among bacteria-translocating toxin, described above, and expand our understanding of the collective response beyond the phenotype of agglutination and adhesion that has triggered the interest of Garcia et al (3) in studying the transcriptional profile.…”

“…The activation of an antiprokaryotic mechanism has been reported in response to lysis of clonal bacteria upon an attack (11). The findings described by Garcia et al (3) add two aspects to these reports. First, the authors see a collective response of biofilms and antiprokaryotic mechanisms.…”

“…Garcia et al (3) further investigate that the transcriptional changes are not limited to a response to clonal bacteria. This observation is relevant to our understanding of how bacteria target their behavior toward other cells based on the presence or absence of the gene locus encoding the social behavior.…”

Activation of contact-dependent antibacterial tRNase toxins by translation elongation factors

“…intersibling CDI toxin exchange influences biofilm gene expression in Burkholderia thailandensis (36).…”

Biofilms 2015: Multidisciplinary Approaches Shed Light into Microbial Life on Surfaces

“…Peggy Cotter (University of North Carolina-Chapel Hill, Chapel Hill, NC) discussed the mechanism of interbacterial signal transduction mediated by contact-dependent growth inhibition (CDI) system proteins. Dr. Cotter described how the Burkholderia thailandensis BcpA protein not only inhibits the growth of "nonself" bacteria by mediating CDI (interbacterial killing) but also contributes to community behaviors in "self" bacteria (those producing the same BcpAIOB proteins) by inducing changes in the expression of genes required for the production of pili and EPS and for biofilm formation (63). These results suggest that CDI system proteins con-trol both cooperative and competitive behaviors to build microbial communities composed of only closely related bacteria (49).…”