Elevated Temperature Enhances Virulence ofErwinia carotovorasubsp.carotovoraStrain EC153 to Plants and Stimulates Production of the Quorum Sensing Signal,N-Acyl Homoserine Lactone, and Extracellular Proteins

Abstract

Erwinia carotovora subsp. atroseptica, E. carotovora subsp. betavasculorum, and E. carotovora subsp. carotovora produce high levels of extracellular enzymes, such as pectate lyase (Pel), polygalacturonase (Peh), cellulase (Cel), and protease (Prt), and the quorum-sensing signal N-acyl-homoserine lactone (AHL) at 28°C. However, the production of these enzymes and AHL by these bacteria is severely inhibited during growth at elevated temperatures (31.2°C for E. carotovora subsp. atroseptica and 34.5°C for E. carotovora subsp. betavasculorum and most E. carotovora subsp. carotovora strains). At elevated temperatures these bacteria produce high levels of RsmA, an RNA binding protein that promotes RNA decay. E. carotovora subsp. carotovora strain EC153 is an exception in that it produces higher levels of Pel, Peh, Cel, and Prt at 34.5°C than at 28°C. EC153 also causes extensive maceration of celery petioles and Chinese cabbage leaves at 34.5°C, which correlates with a higher growth rate and higher levels of rRNA and AHL. The lack of pectinase production by E. carotovora subsp. carotovora strain Ecc71 at 34.5°C limits the growth of this organism in plant tissues and consequently impairs its ability to cause tissue maceration. Comparative studies with ahlI (the gene encoding a putative AHL synthase), pel-1, and peh-1 transcripts documented that at 34.5°C the RNAs are more stable in EC153 than in Ecc71. Our data reveal that overall metabolic activity, AHL levels, and mRNA stability are responsible for the higher levels of extracellular protein production and the enhanced virulence of EC153 at 34.5°C compared to 28°C.Genes for virulence and pathogenicity in bacteria are subject to regulation by transcriptional factors, posttranscriptional mechanisms, indigenous signals, and signals of host origin, as well as environmental factors. One of the latter factors, temperature, has been found to play a critical role in numerous instances. For example, virulence genes of human-pathogenic Yersinia species are activated at 37°C (44). Toxin production by several plant-pathogenic bacteria (for example, production of phaseolotoxin by Pseudomonas syringae pv. phaseolicola and production of coronatine by P. syringae pv. coronafasciens), on the other hand, is highly susceptible to high temperatures since little or no toxin production results from growth at 20°C or a higher temperature (4,35,36,40). Recently, Weingart et al. (51) reported that in P. syringae pv. glycinea, coronatine production in minimal medium and the expression of a cma::egfp fusion in minimal medium and in plant tissue were much higher at 18°C than at 28°C.Many gram-negative bacteria produce the diffusible metabolite N-acyl-homoserine lactone (AHL) or analogs of this compound, which serve as quorum-sensing signals (reviewed in references 14, 27, 37, 46, 49, and 52). AHL controls secondary metabolite production, bacterial interactions with eukaryotic hosts, and diverse phenotypes that are regulated in a cell density-dependent manner. AHL production appears to be favored ...

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

“…Temperature has recently been shown to affect QS mechanisms (Tait et al, 2010). For example, V. mediterranei produces four N-Acyl homoserine lactone at 18 1C compared with only two at 25 1C and 30 1C (Tait et al, 2010), and there is evidence that temperature can affect the level of AHL production positively (Hasegawa et al, 2005;Latour et al, 2007) and negatively (Tait et al, 2010). The Vc450 genome possesses three (AI-1/LuxMN, AI-2/LuxSPQ and CAI-1/CqsAS) two-component histidine kinase QS pathways ( Figure 5) and three small RNAs (Supplementary Figure 7), characteristic of those identified in the regulation of other Vibrio species QS (Lenz et al, 2004).…”

BpiB05, a novel metagenome-derived hydrolase acting on N-acylhomoserine lactones

“…Through the accumulation of bacterially produced signal molecules, autoinducers, the bacterial population is able to sense increases in cell density and alter gene expression accordingly (Waters and Bassler, 2005). This enables coordinated expression of genes at the population level which are most effective at higher cell densities, such as pathogenicity, biofilm formation and production of extracellular proteins (de Kievit and Iglewski, 2000;Hasegawa et al, 2005;Rasmussen and Givskov, 2006a;Ulrich et al, 2004). Many quorum sensing mechanisms involve N-AHLs in gram-negative bacteria.…”

Thermoregulation of N -Acyl Homoserine Lactone-Based Quorum Sensing in the Soft Rot Bacterium Pectobacterium atrosepticum

“…Besides, our results show that one of the mechanisms involved in the QS thermoregulation consists of controlling HSL synthase production by modulating the amounts of expI transcripts. This temperature-dependent regulation could occur at the level of transcription initiation involving temperature-sensitive sigma factors or by production of small RNAs which would act as thermosensors (9,10). In contrast, the QS thermoregulation differs from that one of the main virulence factors studied in the soft rot bacterium Pectobacterium.…”