Quorum sensing control of Type VI secretion factors restricts the proliferation of quorum-sensing mutants

Abstract

Burkholderia thailandensis uses acyl-homoserine lactone-mediated quorum sensing systems to regulate hundreds of genes. Here we show that cell-cell contact-dependent type VI secretion (T6S) toxin-immunity systems are among those activated by quorum sensing in B. thailandensis. We also demonstrate that T6S is required to constrain proliferation of quorum sensing mutants in colony cocultures of a BtaR1 quorum-sensing signal receptor mutant and its parent. However, the BtaR1 mutant is not constrained by and outcompetes its parent in broth coculture, presumably because no cell contact occurs and there is a metabolic cost associated with quorum sensing gene activation. The increased fitness of the wild type over the BtaR1 mutant during agar surface growth is dependent on an intact T6SS-1 apparatus. Thus, quorum sensing activates B. thailandensis T6SS-1 growth inhibition and this control serves to police and constrain quorum-sensing mutants. This work defines a novel role for T6SSs in intraspecies mutant control.DOI: http://dx.doi.org/10.7554/eLife.14712.001

Serine/threonine kinase PpkA coordinates the interplay between T6SS2 activation and quorum sensing in the marine pathogen Vibrio alginolyticus

“…Phosphoproteomics proved a powerful tool to uncover new aspects of T6SS regulation and led to the discovery of the regulatory interplay controlling both QS and T6SS and suggesting the possibility of the coordination between T6S and non-T6SS processes. Ultimately, the complex coordination of QS and T6SS presumably enhances the overall competitive fitness of vibrios for thriving in marine environments (Weber et al, 2009;Borgeaud et al, 2015;Majerczyk et al, 2016). Finally, by additional understanding of the regulation of T6SS activity in V. alginolyticus, we may be able to develop strategies, such as using chemicals that affect T6SS activity or interfere with QS, to reduce the competitive fitness of the bacterium and effectively control the pathogen which plagues the aquaculture industry.…”

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

“…Although we have shown that the genetic architecture of a single trait can constrain cheating, other studies have revealed mechanisms against cheating that are based on the regulatory linkage of multiple traits (Foster et al 2004;Jousset et al 2009;Dandekar et al 2012;Ross-Gillespie et al 2015;Wang et al 2015;Majerczyk et al 2016;Özkaya et al 2018). For instance, Dandekar et al (2012) showed that mutants deficient in the LasIR quorum-sensing (QS) system in P. aeruginosa could cheat on cooperative protease production, but exhibited metabolic insufficiencies in certain media, because this QS system also controls the expression of enzymes required for nutrient degradation.…”

Cell‐cell recognition and social networking in bacteria

“…One example for how policing occurs involves Pseudomonas aeruginosa populations, in which QS cooperators produce cyanide, which inhibits the growth of QS mutants but not of the cooperators (Wang et al, 2015). Similarly, in Burkholderia thailandensis, T6SS expression is induced by QS in cooperators, which renders QS mutants susceptible to T6SS-mediated poisoning (Majerczyk et al, 2016). Whereas these mechanisms keep social mutants from exploiting public goods, they can also be used against siblings that are physiologically different.…”