Interspecies and Intraspecies Signals Synergistically Regulate Lysobacter enzymogenes Twitching Motility

Abstract

The twitching motility of bacteria is closely related to environmental adaptability and pathogenic behaviors. Lysobacter is a good genus in which to study twitching motility because of the complex social activities and distinct movement patterns of its members. Regardless, the mechanism that induces twitching motility is largely unknown. In this study, we found that the interspecies signal indole caused Lysobacter to have irregular, random twitching motility with significantly enhanced speed. Deletion of qseC or qseB from the two-component system for indole signaling perception resulted in the disappearance of rapid, random movements and significantly decreased twitching activity. Indole-induced, rapid, random twitching was achieved through upregulation of expression of gene cluster pilE1-pilY11-pilX1-pilW1-pilV1-fimT1. In addition, under conditions of extremely low bacterial density, individual Lysobacter cells grew and divided in a stable manner in situ without any movement. The intraspecies quorum-sensing signaling factor 13-methyltetradecanoic acid, designated L. enzymogenes diffusible signaling factor (LeDSF), was essential for Lysobacter to produce twitching motility through indirect regulation of gene clusters pilM-pilN-pilO-pilP-pilQ and pilS1-pilR-pilA-pilB-pilC. These results demonstrate that the motility of Lysobacter is induced and regulated by indole and LeDSF, which reveals a novel theory for future studies of the mechanisms of bacterial twitching activities. IMPORTANCE The mechanism underlying bacterial twitching motility is an important research area because it is closely related to social and pathogenic behaviors. The mechanism mediating cell-to-cell perception of twitching motility is largely unknown. Using Lysobacter as a model, we found in this study that the interspecies signal indole caused Lysobacter to exhibit irregular, random twitching motility via activation of gene cluster pilE1-pilY11-pilX1-pilW1-pilV1-fimT1. In addition, population-dependent behavior induced by 13-methyltetradecanoic acid, a quorum-sensing signaling molecule designated LeDSF, was involved in twitching motility by indirectly regulating gene clusters pilM-pilN-pilO-pilP-pilQ and pilS1-pilR-pilA-pilB-pilC. The results demonstrate that the twitching motility of Lysobacter is regulated by these two signaling molecules, offering novel clues for exploring the mechanisms of twitching motility and population-dependent behaviors of bacteria.

The Perception of Rhizosphere Bacterial Communication Signals Leads to Transcriptome Reprogramming in Lysobacter capsici AZ78, a Plant Beneficial Bacterium

“…For instance, twitching motility is required for colonization and infection of phytopathogenic fungi and oomycetes in Lysobacter spp. ( Patel et al, 2011 ; Tomada et al, 2017 ), and it seems to be a DSF-dependent trait in L. brunescens and L. enzymogenes ( Qian et al, 2013 ; Feng et al, 2019 ; Ling et al, 2019b ). Interestingly, upregulation of T4P by GLY and BUT came along with increased antimicrobial activity, suggesting that microbial partners producing this kind of diffusible communication signals might encourage AZ78 to form a stable community and stimulate traits responsible for disease suppressiveness in soils.…”

“…rhizosphere competence and their ability to control plant pathogens. Indeed, it has been shown that DSFs, DFs, and IND regulate the biosynthesis of the heat-stable antifungal factor (HSAF), a potent antifungal compound, and twitching motility in Lysobacter enzymogenes ( Qian et al, 2013 ; Han et al, 2017 ; Su et al, 2017 ; Feng et al, 2019 ). However, with the only exception of the involvement of DSFs and AHLs in Lysobacter brunescens behavior ( Ling et al, 2019a , b ), a complete overview of the overall effect of diffusible communication signals in the ecology of Lysobacter spp.…”

Listening to bacterial Esperanto: transcriptome reprogramming in a plant beneficial rhizobacterium

“…For instance, twitching motility is required for colonization and infection of phytopathogenic fungi and oomycetes in Lysobacter spp. [55, 56] and it seems to be a DSF-dependent trait in L. brunescens and L. enzymogenes [9, 20, 21]. Interestingly, up-regulation of T4P by GLY and BUT came along with increased antimicrobial activity, suggesting that AZ78 might colonize new niches and form a stable community to outcompete other (micro)organisms upon the perception of these DCSs.…”

“…This ability mainly relies on the release of lytic enzymes and antibiotics like the Heat Stable Antifungal Factor (HSAF), which are toxic to phytopathogenic (micro)organisms [16, 17]. In L. enzymogenes DSFs, DFs and IND regulate HSAF biosynthesis [9, 18, 19] and twitching motility [20]. Furthermore, IND reverses the intrinsic antibiotic resistance of L. enzymogenes through the two-component regulatory system QseC/QseB [19, 20].…”

“…In L. enzymogenes DSFs, DFs and IND regulate HSAF biosynthesis [9, 18, 19] and twitching motility [20]. Furthermore, IND reverses the intrinsic antibiotic resistance of L. enzymogenes through the two-component regulatory system QseC/QseB [19, 20]. However, with the only exception of the involvement of DSFs and AHLs in L. brunescens behaviour [21], a complete overview of the overall effect of DCSs in Lysobacter spp.…”