Signal Integration in Quorum Sensing Enables Cross-Species Induction of Virulence in Pectobacterium wasabiae

Abstract

Bacterial communities can sense their neighbors, regulating group behaviors in response to cell density and environmental changes. The diversity of signaling networks in a single species has been postulated to allow custom responses to different stimuli; however, little is known about how multiple signals are integrated and the implications of this integration in different ecological contexts. In the plant pathogen Pectobacterium wasabiae (formerly Erwinia carotovora), two signaling networks—the N-acyl homoserine lactone (AHL) quorum-sensing system and the Gac/Rsm signal transduction pathway—control the expression of secreted plant cell wall-degrading enzymes, its major virulence determinants. We show that the AHL system controls the Gac/Rsm system by affecting the expression of the regulatory RNA RsmB. This regulation is mediated by ExpR2, the quorum-sensing receptor that responds to the P. wasabiae cognate AHL but also to AHLs produced by other bacterial species. As a consequence, this level of regulation allows P. wasabiae to bypass the Gac-dependent regulation of RsmB in the presence of exogenous AHLs or AHL-producing bacteria. We provide in vivo evidence that this pivotal role of RsmB in signal transduction is important for the ability of P. wasabiae to induce virulence in response to other AHL-producing bacteria in multispecies plant lesions. Our results suggest that the signaling architecture in P. wasabiae was coopted to prime the bacteria to eavesdrop on other bacteria and quickly join the efforts of other species, which are already exploiting host resources.

Quorum Sensing Signal Selectivity and the Potential for Interspecies Cross Talk

“…AHL QS has long been recognized as a form of intraspecies bacterial communication. There are, however, examples of “promiscuous” AHL signal receptors, which are able to respond to signals other than their self-produced cognate AHL (8, 9). Existing data on QS selectivity are limited and often generated by E.…”

“…For example, Chromobacterium violaceum is frequently used as a tool for AHL detection due to its receptor’s promiscuous response to multiple AHLs (7). Furthermore, “eavesdropping” through promiscuous receptors has been shown to affect both interspecies competition (8) and cooperation (9) in laboratory experiments. In in vivo settings, interspecies cross talk via degenerate signals and/or promiscuous receptors have both been shown to modulate bacterial virulence to the benefit or detriment of a plant host (9–11), and similar interactions have been hypothesized to occur during human infections (12).…”

“…Furthermore, “eavesdropping” through promiscuous receptors has been shown to affect both interspecies competition (8) and cooperation (9) in laboratory experiments. In in vivo settings, interspecies cross talk via degenerate signals and/or promiscuous receptors have both been shown to modulate bacterial virulence to the benefit or detriment of a plant host (9–11), and similar interactions have been hypothesized to occur during human infections (12). Given that most bacteria are found in mixed polymicrobial communities, it is tempting to speculate that cross talk between QS systems mediates numerous interspecies interactions (13, 14).…”

A Rhodococcal Transcriptional Regulatory Mechanism Detects the Common Lactone Ring of AHL Quorum-Sensing Signals and Triggers the Quorum-Quenching Response

“…Among the top 10 phytopathogens, Pectobacterium spp. employs QS that can also harbor a high degree of complexity to integrate several AHL signaling networks ( Barnard and Salmond, 2007 ; Mansfield et al, 2012 ; Valente et al, 2017 ). Pectobacterial QS ensures the synchronized production of massive amounts of lytic enzymes involved in plant tissues degradation ( Barnard and Salmond, 2007 ; Põllumaa et al, 2012 ).…”

Horizontally acquired quorum sensing regulators recruited by the PhoP regulatory network expand host-adaptation repertoire in the phytopathogenPectobacterium carotovorum

“…In this context, one of the best-characterized mechanism of PCWDE regulation in SRP pathogens is the quorum-sensing (QS) (21). This is a crucial regulatory circuit controlling population density-based behaviour in SRP, as well as in a large spectrum of bacteria (22, 23). Quorum sensing networks in gram-negative bacteria rely on recognition of autoinducer molecules, such as acyl-homoserine lactones (AHL) and other products synthesized using S-adenosylmethionine, by specialized receptors such as ExpR/LuxR homologs (24, 25).…”