N -Acyl- l -Homoserine Lactone Quorum Sensing Controls Butanediol Fermentation in Serratia plymuthica RVH1 and Serratia marcescens MG1

Abstract

Butanediol fermentation in two Serratia species is shown to be affected by N-acyl-L-homoserine lactonedependent quorum sensing. Knockout of quorum-sensing signal production caused a shift towards enhanced acid production, resulting in early growth arrest, which was reversible by the addition of synthetic signal molecules.The Enterobacteriaceae are commonly divided into two groups with different fermentation pathways (4). Members of genera such as Escherichia, Salmonella, and Shigella use the mixed-acid pathway, causing strong acidification of their environment due to the production of large amounts of acids, including acetate, lactate, succinate, and formate. In contrast, members of Klebsiella, Enterobacter, Serratia, and a number of other genera ferment glucose predominantly to 2,3-butanediol (18). In the latter case, the production of acidic products is limited because a significant amount of pyruvate from glycolysis is channeled into the butanediol pathway (6, 9). The production of neutral compounds is ecologically relevant since it allows butanediol fermenters to prevent lethal acidification as cells approach stationary phase. In Klebsiella terrigena, the LysR-type transcriptional activator BudR appears to regulate at least part of the 2,3-butanediol pathway (10). Recently, microarray analysis showed that the production of 2,3-butanediol in Vibrio cholerae is also regulated by the transcriptional activator AphA, in addition to the LysR-type transcriptional activator AlsR (8). The AphA activator is, in turn, regulated by multiple quorum-sensing systems that act in parallel. System 1 uses the CAI-1 autoinducer of unknown structure, while system 2 uses AI-2, a furanosyl borate diester, to trigger a phosphorelay circuit (1,2,7,11,19). These systems are homologues of the Vibrio harveyi systems (11) but differ from the LuxIR paradigm in Vibrio fischeri, in which LuxI synthesizes the Nacyl-L-homoserine lactone (AHL) signaling molecules and the AHL-activated LuxR protein functions as a transcriptional activator triggering a response (5).We recently initiated a study of biofilm-forming bacteria from a food-processing environment (16). One isolate, designated RVH1, was identified as Serratia plymuthica (17), and we recently characterized its LuxIR-homologous quorum-sensing system, SplIR. The SplIR quorum-sensing system regulates the production of an extracellular chitinase, protease, nuclease, and antibacterial compound (R. Van Houdt, P. Moons, A. Aertsen, A. Jansen, K. Vanoirbeek, M. Daykin, P. Williams, and C. W. Michiels, submitted for publication). In the current study, we report that 2,3-butanediol production in this strain is quorum sensing regulated via the same AHL-dependent system. Furthermore, we confirmed our observations in Serratia marcescens MG1 (previously Serratia liquefaciens MG1), the type species of the Serratia genus. The demand and manufacture of 2,3-butanediol are still increasing worldwide (annual rate of 4 to 7%) due to a variety of applications, such as its use as a liquid fuel additive, and t...

Quorum Sensing Regulates Denitrification in Pseudomonas aeruginosa PAO1

“…Quorum sensing has been reported to affect butanediol fermentation in Serratia species (27) and the growth rate in Rhizobium species, although the mechanisms remain obscure (8,30). A study by Wagner et al using DNA microarray analysis (28) reported that exogenous C 4 -HSL and 3-oxo-C 12 -HSL affect the transcription of denitrifying genes in P. aeruginosa PAO1 under aerobic conditions.…”

Core Principles of Bacterial Autoinducer Systems

“…Butanediol fermentation in Serratia plymuthica RVH1 is repressed by an AI system before acidification caused by fermentation impedes population growth (65). Alternatively, in some Burkholderia spp., AI activates the production of oxalate to avoid toxic alkalinization by ammonia (66).…”

Modulation of Quorum Sensing in Acyl-homoserine Lactone-Producing or -Degrading Tobacco Plants Leads to Alteration of Induced Systemic Resistance Elicited by the Rhizobacterium Serratia marcescens 90-166

“…Seed treatment with S. marcescens 90−166 significantly and consistently reduced or delayed symptom development caused by CMV in cucumber and tomato (Raupach et al, 1996). The area under the disease progress curve (AUDPC) was significantly lower for S. marcescens 90−166 than for other Acetoin contents were determined by the Voges-Proskauer described previously (van Houdt et al, 2006). The experiments were repeated three times with similar results.…”

“…Specifically, QS can affect 2,3-butanediol fermentation in S. plymuthica RVH1 and S. marcescens MG1 (Van Houdt et al, 2006;. Among diverse bacterial metabolites, bacterial VOCs such as 2,3-butanediol elicited ISR in Arabidopsis and tobacco (CortesBarco et al, 2010a;2010b;Ryu et al, 2004a).…”

“…Each AHL migrates with a characteristic mobility, and the position and shape of the sample AHL spots can be compared with the spots of different standards in order to identify them. The acetoin production of S. marcescens 90−166 containing pKPE-aiiA and its vector control (pKPEA) that was reported previously (Cho et al, 2007) was determined by the Voges-Proskauer and methyl red assays (van Houdt et al, 2006).…”