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PubMed2001

Quorum sensing controls the synthesis of virulence factors by modulating rsmA gene expression in Erwinia carotovora subsp. carotovora.

The plant-pathogenic bacterium Erwinia carotovora subsp. carotovora (Ecc) causes disease mainly by means of a number of extracellular plant cell wall-degrading enzymes (PCWDEs), also referred to as virulence factors. The production of PCWDEs is coordinately activated by the diffusible signal molecule N-acyl-homoserine lactone (HSL) in a population density-dependent manner ("quorum sensing"). ExpI is the enzyme responsible for the synthesis of HSL. The Rsm system negatively regulates the production of PCWDEs. It includes three components: RsmA is an RNA-binding protein which promotes mRNA decay; rsmB is a unique regulator RNA, and RsmC regulates expression of rsmA positively and of rsmB negatively. We report here that in an expI knockout mutant of Ecc strain SCC3193, the levels of rsmA and rsmB RNA are remarkably enhanced in comparison to the wild-type strain, while the level of the rsmC transcript is not affected. The increase in transcription of rsmA in the expI strain represses production of PCWDEs, which in turn leads to the avirulent phenotype of this mutant. In the expI- mutant, addition of exogenous HSL caused repression of rsmA and rsmB transcription to the wild-type level, whereas the expression of rsmC was not affected. Taken together, these data suggest that HSL affects the expression of rsmA, and that this effect is not mediated by RsmC. This specific effect and the previous demonstration that HSL is required for PCWDE production in Ecc support the hypothesis that regulation by quorum sensing in Ecc, in contrast to most other systems already described, requires HSL to repress rsmA transcription, which in turn leads to the activation of PCWDE production. A model is presented that explains how HSL controls the production of PCWDEs by modulating the expression of rsmA.

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PubMed2003

Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate.

Rhizobium sp. strain NGR234 forms symbiotic, nitrogen-fixing nodules on a wide range of legumes via functions largely encoded by the plasmid pNGR234a. The pNGR234a sequence revealed a region encoding plasmid replication (rep) and conjugal transfer (tra) functions similar to those encoded by the rep and tra genes from the tumor-inducing (Ti) plasmids of Agrobacterium tumefaciens, including homologues of the Ti plasmid quorum-sensing regulators TraI, TraR, and TraM. In A. tumefaciens, TraI, a LuxI-type protein, catalyzes synthesis of the acylated homoserine lactone (acyl-HSL) N-3-oxo-octanoyl-L-homoserine lactone (3-oxo-C8-HSL). TraR binds 3-oxo-C8-HSL and activates expression of Ti plasmid tra and rep genes, increasing conjugation and copy number at high population densities. TraM prevents this activation under noninducing conditions. Although the pNGR234a TraR, TraI, and TraM appear to function similarly to their A. tumefaciens counterparts, the TraR and TraM orthologues are not cross-functional, and the quorum-sensing systems have differences. NGR234 TraI synthesizes an acyl-HSL likely to be 3-oxo-C8-HSL, but traI mutants and a pNGR234a-cured derivative produce low levels of a similar acyl-HSL and another, more hydrophobic signal molecule. TraR activates expression of several pNGR234a tra operons in response to 3-oxo-C8-HSL and is inhibited by TraM. However, one of the pNGR234a tra operons is not activated by TraR, and conjugal efficiency is not affected by TraR and 3-oxo-C8-HSL. The growth rate of NGR234 is significantly decreased by TraR and 3-oxo-C8-HSL through functions encoded elsewhere in the NGR234 genome.

Bacterial Proteins↗

PubMed2005

Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth.

Candida albicans is a pathogenic fungus able to change morphology in response to variations in its growth environment. Simple inoculation of stationary cells into fresh medium at 37 degrees C, without any other manipulations, appears to be a powerful but transient inducer of hyphal formation; this process also plays a significant role in classical serum induction of hyphal formation. The mechanism appears to involve the release of hyphal repression caused by quorum-sensing molecules in the growth medium of stationary-phase cells, and farnesol has a strong but incomplete role in this process. We used DNA microarray technology to study both the resumption of growth of Candida albicans cells and molecular regulation involving farnesol. Maintaining farnesol in the culture medium during the resumption of growth both delays and reduces the induction of hypha-related genes yet triggers expression of genes encoding drug efflux components. The persistence of farnesol also prevents the repression of histone genes during hyphal growth and affects the expression of putative or demonstrated morphogenesis-regulating cyclin genes, such as HGC1, CLN3, and PCL2. The results suggest a model explaining the triggering of hyphae in the host based on quorum-sensing molecules.

Candida albicans↗

PubMed2003

Proteomic analysis of wild-type Sinorhizobium meliloti responses to N-acyl homoserine lactone quorum-sensing signals and the transition to stationary phase.

Proteome analysis revealed that two long-chain N-acyl homoserine lactones (AHLs) produced by Sinorhizobium meliloti 1021 induced significant differences in the accumulation of more than 100 polypeptides in early-log-phase cultures of the wild type. Fifty-six of the corresponding proteins have been identified by peptide mass fingerprinting. The proteins affected by addition of these two AHLs had diverse functions in carbon and nitrogen metabolism, energy cycles, metabolite transport, DNA synthesis, and protein turnover. Two hours of exposure to 3-oxo-C(16:1)-homoserine lactone (3-oxo-C(16:1)-HL) affected the accumulation of 40 of the 56 identified proteins, whereas comparable exposure to C(14)-HL affected 13 of the 56 proteins. Levels of four proteins were affected by both AHLs. Exposure to 3-oxo-C(16:1)-HL for 8 h affected the accumulation of 17 proteins, 12 of which had reduced accumulation. Of the 80 proteins identified as differing in accumulation between early-log- and early-stationary-phase cultures, only 13 were affected by exposure to 3-oxo-C(16:1)-HL or C(14)-HL. These results provide a foundation for future studies of the functions regulated by AHL quorum sensing in S. meliloti and help to establish proteomic analysis as a powerful global approach to the identification of quorum-sensing regulatory patterns in wild-type bacteria.

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PubMed2006

Immunomodulatory effects of Pseudomonas aeruginosa quorum sensing small molecule probes on mammalian macrophages.

Pseudomonas aeruginosa produces the quorum sensing signalling molecule N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL). This natural product not only coordinates production of virulence factors by the bacterium, but also has immunomodulatory effects on the host organism. Immunomodulatory small molecules are valuable for immunology research and are potential therapeutics for autoimmune diseases such as rheumatoid arthritis, and immunosuppressive drugs following organ transplants. We describe the total synthesis of OdDHL using solid-supported reagents and scavengers, which has the potential to be used for automated analogue synthesis. OdDHL and four analogues were tested for their ability to activate or inhibit release of the pro-inflammatory mediators tumour necrosis factor alpha (TNFalpha) and nitric oxide (NO) from equine or murine macrophages (immune cells). Two of the analogues showed substantial immunomodulatory activity with these macrophages. One analogue showed differing species selectivity, being a potent antagonist in mouse cells, but a partial agonist in horse-derived macrophages. These compounds have the therapeutic potential to be used for protecting animals from bacterial septic shock.

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PubMed2004

Site-directed mutagenesis of a LuxR-type quorum-sensing transcription factor: alteration of autoinducer specificity.

TraR is a quorum-sensing transcription factor from Agrobacterium tumefaciens that regulates replication and conjugation genes of the tumour-inducing (Ti) plasmid. TraR activity requires the autoinducer pheromone N-3-oxooctanoyl-l-homoserine lactone (OOHL). Structural studies of TraR-OOHL-DNA complexes showed that one molecule of OOHL is completely engulfed within the N-terminal domain of each TraR subunit. TraR is thought to bind OOHL via four hydrogen bonds, three of them direct and one water mediated, and by numerous hydrophobic interactions. Here, we show that all residues predicted to hydrogen bond with OOHL are essential for wild-type protein function. Mutants that failed to detect OOHL in vivo invariably failed to sequester exogenous OOHL. We showed previously that TraR is protected from cellular proteases by OOHL, and now show that mutants that failed to detect OOHL were also not protected from proteolysis by OOHL. We also describe several mutants with altered autoinducer specificity. Three mutants (T129V, T129A and T115I) detected 3-oxo-AHLs and 3-unsubstituted AHLs with equal sensitivity, indicating that these mutations perturb the water-mediated hydrogen bond to the 3-oxo moiety of OOHL. Three other mutants (A49I, A49M and Q58L) preferentially detected AHLs containing six or seven carbon atoms rather than eight. The bulkier residues in these mutations appear to have occupied a portion of the OOHL binding site, interfering with binding of the acyl chain of AHLs.

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PubMed2001

Distribution of quorum-sensing genes in the Burkholderia cepacia complex.

The distribution of quorum-sensing genes among strains from seven genomovars of the Burkholderia cepacia complex was examined by PCR. cepR and cepI were amplified from B. cepacia genomovars I and III, B. stabilis, and B. vietnamiensis. cepR was also amplified from B. multivorans and B. cepacia genomovar VI. bviIR were amplified from B. vietnamiensis. All genomovars produced N-octanoyl-L-homoserine lactone and N-hexanoyl-L-homoserine lactone. B. vietnamiensis and B. cepacia genomovar VII produced additional N-acyl-L-homoserine lactones.

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PubMed2003

Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa.

Quorum sensing (QS)-based transcriptional responses in Pseudomonas aeruginosa have been defined on the basis of increases in transcript levels of QS-controlled genes such as lasB and aprA following the hierarchical transcriptional increases of central controllers such as the lasR gene. These increases occur at high bacterial concentrations such as early-stationary-phase growth in vitro. However, the extent to which the increases occur in a variety of clinical and environmental isolates has not been determined nor is there extensive information on allelic variation in lasR genes. An analysis of the sequences of the lasR gene among 66 clinical and environmental isolates showed that 81% have a sequence either identical to that of strain PAO1 or with a silent mutation, 15% have nucleotide changes resulting in amino acid changes, and 5% have an insertion sequence in the lasR gene. Using real-time PCR to quantify transcript levels of lasR, lasB, and aprA in the early log and early stationary phases among 35 isolates from bacteremia and pneumonia cases and the environment, we found most (33 of 35) strains had increases in lasR transcripts in early stationary phase but with a very wide range of final transcript levels per cell. There was a strong correlation (r(2) = 0.84) between early-log- and early-stationary-phase transcript levels in all strains, but this finding remained true only for the 50% of strains above the median level of lasR found in early log phase. There were significant (P < 0.05) but weak-to-modest correlations of lasR transcript levels with aprA (r(2) = 0.2) and lasB (r(2) = 0.5) transcript levels, but again this correlation occurred only in the 50% of P. aeruginosa strains with the highest levels of lasR transcripts in early stationary phase. There were no differences in distribution of lasR alleles among the bacteremia, pneumonia, or environmental isolates. Overall, only about 50% of P. aeruginosa strains from clinical and environmental sources show a lasR-dependent increase in the transcription of aprA and lasB genes, indicating that for about 50% of clinical isolates this regulatory system may not play a significant role in pathogenesis.

Bacterial Proteins↗

PubMed2003

Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment.

Bacterial communication via quorum sensing (QS) has been reported to be important in the production of virulence factors, antibiotic sensitivity, and biofilm development. Two QS systems, known as the las and rhl systems, have been identified previously in the opportunistic pathogen Pseudomonas aeruginosa. High-density oligonucleotide microarrays for the P. aeruginosa PAO1 genome were used to investigate global gene expression patterns modulated by QS regulons. In the initial experiments we focused on identifying las and/or rhl QS-regulated genes using a QS signal generation-deficient mutant (PAO-JP2) that was cultured with and without added exogenous autoinducers [N-(3-oxododecanoyl) homoserine lactone and N-butyryl homoserine lactone]. Conservatively, 616 genes showed statistically significant differential expression (P </= 0.05) in response to the exogenous autoinducers and were classified as QS regulated. A total of 244 genes were identified as being QS regulated at the mid-logarithmic phase, and 450 genes were identified as being QS regulated at the early stationary phase. Most of the previously reported QS-promoted genes were confirmed, and a large number of additional QS-promoted genes were identified. Importantly, 222 genes were identified as being QS repressed. Environmental factors, such as medium composition and oxygen availability, eliminated detection of transcripts of many genes that were identified as being QS regulated.

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PubMed2001

Quorum-sensing in Gram-negative bacteria.

It has become increasingly and widely recognised that bacteria do not exist as solitary cells, but are colonial organisms that exploit elaborate systems of intercellular communication to facilitate their adaptation to changing environmental conditions. The languages by which bacteria communicate take the form of chemical signals, excreted from the cells, which can elicit profound physiological changes. Many types of signalling molecules, which regulate diverse phenotypes across distant genera, have been described. The most common signalling molecules found in Gram-negative bacteria are N-acyl derivatives of homoserine lactone (acyl HSLs). Modulation of the physiological processes controlled by acyl HSLs (and, indeed, many of the non-acyl HSL-mediated systems) occurs in a cell density- and growth phase-dependent manner. Therefore, the term 'quorum-sensing' has been coined to describe this ability of bacteria to monitor cell density before expressing a phenotype. In this paper, we review the current state of research concerning acyl HSL-mediated quorum-sensing. We also describe two non-acyl HSL-based systems utilised by the phytopathogens Ralstonia solanacearum and Xanthomonas campestris.

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PubMed2003

Quorum sensing and expression of virulence in Escherichia coli O157:H7.

Enterohaemorrhagic Escherichia coli O157:H7 causes a characteristic histopathology in intestinal cells known as attaching and effacing lesion. The genes for the lesion are encoded by the Locus of Enterocyte Effacement (LEE) pathogenicity island, that encodes a type III secretion system, the intimin intestinal colonization factor, and the translocated intimin receptor protein that is translocated from the bacterium to the host epithelial cells. Expression of the operons encoded within LEE is complex, but recent studies have demonstrated that quorum sensing influences transcription from four of the LEE operon promoters. A transcriptional regulator (LuxR homologue), signal synthase (LuxI homologue), and autoinducer (acylhomoserine lactone) are indispensable for this system in most gram-negative bacteria. Vibrio harveyi, a gram-negative bioluminescent marine bacterium, regulates light production in response to two autoinducers (AI-1 and AI-2). AI-1 is a homoserine lactone produced by most gram-negative bacteria. The structure of AI-2 is not known, but many species of gram positive and gram-negative bacteria, including E. coli and more specifically O157:H7, have been shown to produce AI-2 depending on the function encoded by the luxS gene. The LuxS acts as an AI-2 synthase and the AI-2 is produced from S-adenosylmethionine in three enzymatic steps. The substrate for LuxS is S-ribosylhomocysteine, which is cleaved to form two products, one of which is homocysteine, and the other is AI-2. The biosynthetic pathways and the biochemical intermediates in AI-2 biosynthesis have been observed to be identical in several gram-negative bacteria, such as E. coli, Salmonella typhimurium, V. harveyi, Vibrio cholerae, and Enterococcus faecalis. Thus, unlike quorum sensing via the family of related homoserine autoinducers, AI-2 is a universal signal, which may be used by a variety of bacteria for communication among and between species and may be responsible for regulation of virulence genes in E. coli O157:H7.

Escherichia coli O157↗

PubMed2006

Discovery of potent inhibitors of pseudomonal quorum sensing via pharmacophore modeling and in silico screening.

HipHop-Refine was employed to derive a binding hypothesis for pseudomonal quorum sensing (QS) antagonists. The model was employed as 3D search query to screen the National Cancer Institute (NCI) database. One of the hits illustrated nanomolar QS inhibitory activity. The fact that this compound contained tetravalent lead (Pb) prompted us to evaluate the activities of phenyl mercuric nitrate and thimerosal, both fit the binding pharmacophore. The two mercurials illustrated nanomolar to low micromolar IC50 inhibitory values against pseudomonal QS. The three compounds represent a new class of QS inhibitors.

Algorithms↗

PubMed2006

Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures.

In the environment, multiple microbial taxa typically coexist as communities, competing for resources and, often, physically associated within biofilms. A dual-species cocultivation model has been developed by using two ubiquitous and well studied microbes Pseudomonas aeruginosa (P.a.) and Agrobacterium tumefaciens (A.t.) as a tractable system to identify molecular mechanisms that underlie multispecies microbial associations. Several factors were found to influence coculture interactions. P.a. had a distinct growth-rate advantage in cocultures, increasing its relative abundance during planktonic and biofilm growth. P.a. also demonstrated a slight quorum-sensing-dependent increase in growth yield in liquid cocultures. P.a. dominated coculture biofilms, "blanketing" or burying immature A.t. microcolonies. P.a. flagellar and type IV pili mutant strains exhibited deficient blanketing and impaired competition in coculture biofilms, whereas, in planktonic coculture, these mutations had no effect on competition. In contrast, A.t. used motility to emigrate from coculture biofilms. In both planktonic and biofilm cocultures, A.t. remained viable for extended periods of time, coexisting with its more numerous competitor. These findings reveal that quorum-sensing-regulated functions and surface motility are important microbial competition factors for P.a. and that the outcome of competition and the relative contribution of different factors to competition are strongly influenced by the environment in which they occur.

Agrobacterium tumefaciens↗

PubMed2004

The PmlI-PmlR quorum-sensing system in Burkholderia pseudomallei plays a key role in virulence and modulates production of the MprA protease.

Burkholderia pseudomallei is the causative agent of melioidosis, an often fatal infection of humans and animals. The virulence of this pathogen is thought to depend on a number of secreted proteins, including the MprA metalloprotease. We observed that MprA is produced upon entry into the stationary phase, when the cell density is high, and this prompted us to study cell density-dependent regulation in B. pseudomallei. A search of the B. pseudomallei genome led to identification of a quorum-sensing system involving the LuxI-LuxR homologs PmlI-PmlR. PmlI directed the synthesis of an N-acylhomoserine lactone identified as N-decanoylhomoserine lactone. A B. pseudomallei pmlI mutant was significantly less virulent than the parental strain in a murine model of infection by the intraperitoneal, subcutaneous, and intranasal routes. Inactivation of pmlI resulted in overproduction of MprA at the onset of the stationary phase. A wild-type phenotype was restored following complementation with pmlI or addition of cell-free culture supernatant. In contrast, there was no significant difference between the virulence of a B. pseudomallei mprA mutant and the virulence of the wild-type strain. These results suggest that the PmlI-PmlR quorum-sensing system of B. pseudomallei is essential for full virulence in a mouse model and downregulates the production of MprA at a high cell density.

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PubMed2006

Identification of genes regulated by the cepIR quorum-sensing system in Burkholderia cenocepacia by high-throughput screening of a random promoter library.

The Burkholderia cenocepacia cepIR quorum-sensing system regulates expression of extracellular proteases, chitinase, and genes involved in ornibactin biosynthesis, biofilm formation, and motility. In a genome-wide screen we identified cepIR-regulated genes by screening a random promoter library of B. cenocepacia K56-2 constructed in a luminescence reporter detection plasmid for differential expression in response to N-octanoyl-l-homoserine lactone (OHL). Eighty-nine clones were identified; in 58 of these clones expression was positively regulated by cepIR, and in 31 expression was negatively regulated by cepIR. The expression profiles of the 89 promoter clones were compared in the cepI mutant K56-dI2 in medium supplemented with 30 pM OHL and K56-2 to confirm that the presence of OHL restored expression to wild-type levels. To validate the promoter library observations and to determine the effect of a cepR mutation on expression of selected genes, the mRNA levels of nine genes whose promoters were predicted to be regulated by cepR were quantitated by quantitative reverse transcription-PCR in the wild type and cepI and cepR mutants. The expression levels of all nine genes were similar in the cepI and cepR mutants and consistent with the promoter-lux reporter activity. The expression of four selected cepIR-regulated gene promoters was examined in a cciIR mutant, and two of these promoters were also regulated by cciIR. This study extends our understanding of genes whose expression is influenced by cepIR and indicates the global regulatory effect of the cepIR system in B. cenocepacia.

Bacterial Proteins↗

PubMed2005

Involvement of bacterial quorum-sensing signals in spoilage of bean sprouts.

Bacterial communication signals, acylated homoserine lactones (AHLs), were extracted from samples of commercial bean sprouts undergoing soft-rot spoilage. Bean sprouts produced in the laboratory did not undergo soft-rot spoilage and did not contain AHLs or AHL-producing bacteria, although the bacterial population reached levels similar to those in the commercial sprouts, 10(8) to 10(9) CFU/g. AHL-producing bacteria (Enterobacteriaceae and pseudomonads) were isolated from commercial sprouts, and strains that were both proteolytic and pectinolytic were capable of causing soft-rot spoilage in bean sprouts. Thin-layer chromatography and liquid chromatography-high-resolution mass spectrometry revealed the presence of N-3-oxo-hexanoyl-l-homoserine lactone in spoiled bean sprouts and in extracts from pure cultures of bacteria. During normal spoilage, the pH of the sprouts increased due to proteolytic activity, and the higher pH probably facilitated the activity of pectate lyase. The AHL synthetase gene (I gene) from a spoilage Pectobacterium was cloned, sequenced, and inactivated in the parent strain. The predicted amino acid sequence showed 97% homology to HslI and CarI in Erwinia carotovora. Spoilage of laboratory bean sprouts inoculated with the AHL-negative mutant was delayed compared to sprouts inoculated with the wild type, and the AHL-negative mutant did not cause the pH to rise. Compared to the wild-type strain, the AHL-negative mutant had significantly reduced protease and pectinase activities and was negative in an iron chelation (siderophore) assay. This is the first study demonstrating AHL regulation of iron chelation in Enterobacteriaceae. The present study clearly demonstrates that the bacterial spoilage of some food products is influenced by quorum-sensing-regulated phenotypes, and understanding these processes may be useful in the development of novel food preservation additives that specifically block the quorum-sensing systems.

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PubMed2005

Effect of quorum sensing agents on the growth kinetics of Pseudomonas spp. of raw milk origin.

Psychrotrophs, particularly strains of Pseudomonas fluorescens, dominate the microflora of refrigerated raw milk and secrete heat-stable extracellular enzymes (proteases and lipases) which survive pasteurisation and even UHT heat treatments and degrade the casein and fat components of raw milk causing a reduction in cheese yield, gelation of UHT milk and off flavours in many dairy products. These enzymes are usually produced in the late log/early stationary growth phases when the cell density is high. This fact indicated that induction of these enzymes may be a candidate for quorum sensing, a phenomenon by which bacteria can sense and respond to cell population size by means of chemical signals based on the homoserine lactone molecule. It is assumed that the production of these enzymes contributes to the selective advantage of psychrotrophs and hence have a significant effect on their growth kinetics. In the work reported here nine proprietary homoserine lactone compounds were screened, using water as a control, for their effect on the lag phase duration (LPD) and exponential growth rate (EGR) of three strains of Pseudomonas fluorescens isolated from refrigerated raw milk after 1, 3 and 5 days storage. Two compounds viz. N-benzoyloxycarbonyl-L-homoserine lactone and N-3-oxyhexanoyl-DL-homoserine lactone were found to significantly (P < 0.001) reduce the LPD and increase the EGR of the three strains. Further work with these compounds is warranted, monitoring growth in parallel with enzyme production, to determine the extent to which extracellular enzyme production is mediated by the quorum sensing phenomenon in this species.

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PubMed2005

Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway.

Two-dimensional polyacrylamide gel electrophoresis of the secreted proteins of Erwinia carotovora subsp. atroseptica revealed a low-abundance protein that was identified by mass spectrometry as a homologue of a Xanthomonas campestris avirulence protein with unknown function. The predicted Svx protein has an N-terminal signal sequence and zinc binding-region signature, and the mature protein is post-translationally modified. A 2D difference gel electrophoresis (DIGE) showed that the protein is secreted by the type II (out) secretion apparatus, which is also responsible for the secretion of the major known virulence factors, PelC and CelV. Transcription of the svx gene is under N-acyl-homoserine lactone-mediated quorum-sensing control. The svx gene was inactivated by transposon insertion. The mutant showed a decrease in virulence in potato plant assays, demonstrating a role for Svx in the pathogenicity of E. carotovora subsp. atroseptica. These results show that Svx is a previously unidentified virulence determinant which is secreted by the out machinery and is regulated by quorum sensing, two systems employed by several other virulence factors. Thus, the type II secretory machine is a conduit for virulence factors other than the main pectinnases and cellulase in E. carotovora subsp. atroseptica.

Bacterial Proteins↗