Characterization of genes required for the pathogenicity of Pectobacterium carotovorum subsp. carotovorum Pcc21 in Chinese cabbage

Lee, Dong Hwan; Lim, Joong‐Soo; Lee, Juneok; Roh, Eunjung; Jung, Kyu-Suk; Choi, Mansoo; Oh, Chang‐Sik; Ryu, Sangryeol; Yun, Jong-Chul; Heu, Sunggi

doi:10.1099/mic.0.067280-0

Cited by 68 publications

(75 citation statements)

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“…After finding that Salmonella metabolic requirements for proliferation within tomatoes differed from the requirements for the systemic infection of mice, we explored whether these requirements are similar to the metabolic requirements of bacterial phytopathogens during plant infection. To test the hypothesis that Salmonella behavior in tomatoes is similar to the behavior of plant pathogens, we extracted the information identified in mutant screens of Pectobacterium carotovorum in Chinese cabbage (39), Ralstonia solanacearum in Arabidopsis thaliana and tomatoes (40), Xanthomonas citri in grapefruit (41), Xanthomonas oryzae pv. oryzicola in rice and tobacco (42), Pseudomonas tolaasii in A. thaliana (43), Pseudomonas syringae pv.…”

Section: Resultsmentioning

confidence: 99%

Salmonella Persistence in Tomatoes Requires a Distinct Set of Metabolic Functions Identified by Transposon Insertion Sequencing

Moraes

Desai

Porwollik

et al. 2017

Appl Environ Microbiol

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Human enteric pathogens, such as Salmonella spp. and verotoxigenic Escherichia coli, are increasingly recognized as causes of gastroenteritis outbreaks associated with the consumption of fruits and vegetables. Persistence in plants represents an important part of the life cycle of these pathogens. The identification of the full complement of Salmonella genes involved in the colonization of the model plant (tomato) was carried out using transposon insertion sequencing analysis. With this approach, 230,000 transposon insertions were screened in tomato pericarps to identify loci with reduction in fitness, followed by validation of the screen results using competition assays of the isogenic mutants against the wild type. A comparison with studies in animals revealed a distinct plant-associated set of genes, which only partially overlaps with the genes required to elicit disease in animals. De novo biosynthesis of amino acids was critical to persistence within tomatoes, while amino acid scavenging was prevalent in animal infections. Fitness reduction of the Salmonella amino acid synthesis mutants was generally more severe in the tomato rin mutant, which hyperaccumulates certain amino acids, suggesting that these nutrients remain unavailable to Salmonella spp. within plants. Salmonella lipopolysaccharide (LPS) was required for persistence in both animals and plants, exemplifying some shared pathogenesis-related mechanisms in animal and plant hosts. Similarly to phytopathogens, Salmonella spp. required biosynthesis of amino acids, LPS, and nucleotides to colonize tomatoes. Overall, however, it appears that while Salmonella shares some strategies with phytopathogens and taps into its animal virulence-related functions, colonization of tomatoes represents a distinct strategy, highlighting this pathogen's flexible metabolism.IMPORTANCE Outbreaks of gastroenteritis caused by human pathogens have been increasingly associated with foods of plant origin, with tomatoes being one of the common culprits. Recent studies also suggest that these human pathogens can use plants as alternate hosts as a part of their life cycle. While dual (animal/plant) lifestyles of other members of the Enterobacteriaceae family are well known, the strategies with which Salmonella colonizes plants are only partially understood. Therefore, we undertook a high-throughput characterization of the functions required for Salmonella persistence within tomatoes. The results of this study were compared with what is known about genes required for Salmonella virulence in animals and interactions of plant pathogens with their hosts to determine whether Salmonella repurposes its virulence repertoire inside plants or whether it behaves more as a phytopathogen during plant colonization. Even though Salmonella utilized some of its virulence-related genes in tomatoes, plant colonization required a distinct set of functions.KEYWORDS Salmonella, foodborne pathogens, plant-microbe interactions

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Section: Resultsmentioning

confidence: 99%

Salmonella Persistence in Tomatoes Requires a Distinct Set of Metabolic Functions Identified by Transposon Insertion Sequencing

Moraes

Desai

Porwollik

et al. 2017

Appl Environ Microbiol

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“…The production of these enzymes is dependent on cell density and regulated by quorum sensing through N-acetylhomoserine lactone (5) and intracellular regulators (6, 7). Motility and nutrient uptake are also factors influencing phytopathogenicity (4,(8)(9)(10). Besides these general pathogenicity factors, phytopathogens have to overcome the toxicity of plant allelochemicals.…”

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confidence: 99%

“…have been found during the last decades (2)(3)(4). Of these, plant cell wall-degrading enzymes produced by Pectobacterium spp.…”

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confidence: 99%

“…In microorganisms, general allelochemical defense systems are efflux pumps that decrease the intracellular concentration of toxic substances. Several studies identified TolC as a pathogenicity factor related to the extrusion of phytochemicals (4,15,16). TolC is an outer membrane protein that interacts with efflux pumps of the cytoplasmic membrane (17,18).…”

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confidence: 99%

“…TolC is an outer membrane protein that interacts with efflux pumps of the cytoplasmic membrane (17,18). Although several phytochemicals have been tested as substrates of Pectobacterium TolC (4,15,16), none of the substrates tested included isothiocyanates. In addition to this, a transposon mutagenesis study of Pseudomonas syringae pv.…”

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confidence: 99%

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SaxA-Mediated Isothiocyanate Metabolism in Phytopathogenic Pectobacteria

Welte

Rosengarten

Graaf

et al. 2016

Appl Environ Microbiol

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Pectobacteria are devastating plant pathogens that infect a large variety of crops, including members of the family Brassicaceae. To infect cabbage crops, these plant pathogens need to overcome the plant's antibacterial defense mechanisms, where isothiocyanates are liberated by hydrolysis of glucosinolates. Here, we found that a Pectobacterium isolate from the gut of cabbage root fly larvae was particularly resistant to isothiocyanate and even seemed to benefit from the abundant Brassica root metabolite 2-phenylethyl isothiocyanate as a nitrogen source in an ecosystem where nitrogen is scarce. The Pectobacterium isolate harbored a naturally occurring mobile plasmid that contained a sax operon. We hypothesized that SaxA was the enzyme responsible for the breakdown of 2-phenylethyl isothiocyanate. Subsequently, we heterologously produced and purified the SaxA protein and characterized the recombinant enzyme. It hydrolyzed 2-phenylethyl isothiocyanate to yield the products carbonyl sulfide and phenylethylamine. It was also active toward another aromatic isothiocyanate but hardly toward aliphatic isothiocyanates. It belongs to the class B metal-dependent beta-lactamase fold protein family but was not, however, able to hydrolyze beta-lactam antibiotics. We discovered that several copies of the saxA gene are widespread in full and draft Pectobacterium genomes and therefore hypothesize that SaxA might be a new pathogenicity factor of the genus Pectobacterium, possibly compromising food preservation strategies using isothiocyanates. P ectobacteria are phytopathogens that cause tuber soft rot and blackleg (stem rot) in many horticulturally and economically important crops during cultivation, transport, or storage. Most Pectobacterium spp., e.g., Pectobacterium carotovorum or P. wasabiae, can be detrimental to many different plants, such as potato, sugar beet, cabbage, wasabi, chicory, and Ornithogalum plants, whereas other Pectobacterium spp., e.g., P. atrosepticum and P. betavasulorum, have a more narrow host range of potato and sugar beet plants, respectively (1).Several pathogenicity factors of soft-rot-causing Pectobacterium spp. have been found during the last decades (2-4). Of these, plant cell wall-degrading enzymes produced by Pectobacterium spp. have a large impact on the progress of the disease, as their production leads to the degradation of invaded plant tissue (2, 3). The production of these enzymes is dependent on cell density and regulated by quorum sensing through N-acetylhomoserine lactone (5) and intracellular regulators (6, 7). Motility and nutrient uptake are also factors influencing phytopathogenicity (4,(8)(9)(10). Besides these general pathogenicity factors, phytopathogens have to overcome the toxicity of plant allelochemicals. Important allelochemicals of members of the family Brassicaceae (cabbages and mustards) are isothiocyanates that are liberated by the glucosinolate-myrosinase defense system (11-13). The antimicrobial effect of isothiocyanates has been mainly attributed to their reactivity w...

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Biochemical and Molecular Mechanisms in Biofilm Formation of Plant‐Associated Bacteria

Padmavathi

Bakkiyaraj

Pandian

2017

Biofilms in Plant and Soil Health

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Characterization of genes required for the pathogenicity of Pectobacterium carotovorum subsp. carotovorum Pcc21 in Chinese cabbage

Cited by 68 publications

References 54 publications

Salmonella Persistence in Tomatoes Requires a Distinct Set of Metabolic Functions Identified by Transposon Insertion Sequencing

Salmonella Persistence in Tomatoes Requires a Distinct Set of Metabolic Functions Identified by Transposon Insertion Sequencing

SaxA-Mediated Isothiocyanate Metabolism in Phytopathogenic Pectobacteria

Biochemical and Molecular Mechanisms in Biofilm Formation of Plant‐Associated Bacteria

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