Cross-species activation of hydrogen cyanide production by a promiscuous quorum-sensing receptor promotesChromobacterium subtsugaecompetition in a dual-species model

Many saprophytic bacteria have LuxR-I-type acyl-homoserine lactone (AHL) quorum-sensing systems that may be important for competing with other bacteria in complex soil communities. LuxR AHL receptors specifically interact with cognate AHLs to cause changes in expression of target genes. Some LuxR-type AHL receptors have relaxed specificity and are responsive to non-cognate AHLs. These promiscuous receptors might be used to sense and respond to AHLs produced by other bacteria by eavesdropping. We are interested in understanding the role of eavesdropping during interspecies competition. The soil saprophyteChromobacterium subtsugaehas a single AHL circuit, CviR-I, which produces and responds toN-hexanoyl-HSL (C6-HSL). The AHL receptor CviR can respond to a variety of AHLs in addition to C6-HSL. In prior studies we have utilized a coculture model withC. subtsugaeand another soil saprophyteBurkholderia thailandensis. Using this model, we previously showed that promiscuous activation of CviR byB. thailandensisAHLs provides a competitive advantage toC. subtsugae. Here, we show thatB. thailandensisAHLs activate transcription of dozens of genes inC. subtsugae, including thehcnABCgenes coding for production of hydrogen cyanide. We show that hydrogen cyanide production is population density-dependent and demonstrate that the cross-induction of hydrogen cyanide byB. thailandensisAHLs provides a competitive advantage toC. subtsugae. Our results provide new information onC. subtsugaequorum sensing and are the basis for future studies aimed at understanding the role of eavesdropping in interspecies competition.IMPACT STATEMENTIn quorum sensing, population density-dependent changes in gene regulation are the result of a cytoplasmic transcription regulator binding to a quorum sensing signal. The signal-receptor interaction is considered to be specific to ensure fidelity of the system. However, some quorum-sensing receptor proteins have relaxed specificity and can recognize and respond to a range of signals. These promiscuous receptors might provide some benefit by enabling interspecies activation of quorum sensing by “eavesdropping,” although the potential benefits of eavesdropping are not well studied. The current study utilizes a dual-species laboratory competition model, where one species has a promiscuous signal receptor and can respond to signals produced by the other species. In our study, we identify the signals that enable quorum sensing cross talk and show that cross talk promotes competition by inducing hydrogen cyanide production. Our results highlight how quorum sensing-enabled interspecies cross talk might provide an advantage during competition and provide a new basis for understanding how receptor-signal pairs might evolve in natural environments.DATA SUMMARYThe authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files.