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Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11.

ABSTRACT: Lysobacter enzymogenes is a bacterial biological control agent emerging as a new source of antibiotic metabolites, such as heat-stable antifungal factor (HSAF) and the antibacterial factor WAP-8294A2. The regulatory mechanism(s) for antibiotic metabolite biosynthesis remains largely unknown in L. enzymogenes. Clp, a cyclic adenosine monophosphate (cAMP)-receptor-like protein, is shown to function as a global regulator in modulating biocontrol-associated traits in L. enzymogenes. However, the genetic basis of Clp signaling remains unclear. Here, we utilized transcriptome/microarray analysis to determine the Clp regulon in L. enzymogenes. We showed that Clp is a global regulator in gene expression, as the transcription of 775 genes belonging to 19 functional groups was differentially controlled by Clp signaling. Analysis of the Clp regulon detected previously characterized Clp-modulated functions as well as novel loci. These include novel loci involved in antibiotic metabolite biosynthesis and surface motility in L. enzymogenes. We further showed experimentally that Clp signaling played a positive role in regulating the biosynthesis of HSAF and WAP-8294A2, as well as surface motility which is a type-IV-pilus-dependent trait. The regulation by Clp signaling of antibiotic (HSAF and WAP-8294A2) biosynthesis and surface motility was found to be independent. Importantly, we identified a factor Lysobacter acetyltransferase (Lat), a homologue of histone acetyltransferase Hpa2, which was regulated by Clp and involved in HSAF biosynthesis, but not associated with WAP-8294A2 production and surface motility. Overall, our study provided new insights into the regulatory role and molecular mechanism of Clp signaling in L. enzymogenes.

SUBMITTER: Wang Y

PROVIDER: S-EPMC4207120 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Project description: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.

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Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11.

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