From Exit to Entry: Long-term Survival and Transmission of Salmonella

Waldner, Landon L.; MacKenzie, Keith D.; Köster, Wolfgang; White, Aaron P.

doi:10.3390/pathogens1020128

Cited by 43 publications

(28 citation statements)

References 147 publications

(192 reference statements)

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“…Biofilms have demonstrated roles in bacterial persistence and virulence [12,13,58,59] and have been 490 anecdotally reported in Clostridia to be composed of cellulose exopolysaccharides [7,8]. Additionally, the 491 loci encoding the molecular machinery for Pel polysaccharide has been recently identified in members of…”

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confidence: 99%

Identification of the Clostridial cellulose synthase and characterization of the cognate glycosyl hydrolase, CcsZ

Scott

Lowrance

Anderson

et al. 2019

Preprint

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1Biofilms are community structures of bacteria enmeshed in a self-produced matrix of exopolysaccharides. 2The biofilm matrix serves numerous roles, including resilience and persistence, making biofilms a subject 3 of research interest among persistent clinical pathogens of global health importance. Our current 4 understanding of the underlying biochemical pathways responsible for biosynthesis of these 5 exopolysaccharides is largely limited to Gram-negative bacteria. Clostridia are a class of Gram-positive, 6 anaerobic and spore-forming bacteria, and include the important human pathogens Clostridium 7 perfringens, Clostridium botulinum, and Clostridioides difficile, among numerous others. Clostridia have 8 been reported to form biofilms composed of cellulose, although the specific loci which encode the 9 cellulose synthase have not been identified. Here, we report the discovery of a gene cluster, which we 10 named ccsABZCD, among selected bacteria within class Clostridia that appears to encode a synthase 11 complex responsible for polymerization, modification, and export of an O-acetylated cellulose 12 exopolysaccharide. To test this hypothesis, we subcloned the putative glycoside hydrolase CcsZ and 13 solved the X-ray crystal structure of both apo-and product-bound CcsZ. Our results demonstrate that 14 CcsZ is in fact an endo-acting cellulase belonging to glycoside hydrolase family 5 . This is in 15 contrast to the Gram-negative cellulose synthase, which instead encodes BcsZ, a structurally distinct GH-16 8. We further show CcsZ is capable of hydrolysis of the soluble mock substrate carboxymethylcellulose 17 (CMC) with a pH optimum of 4.5. The data we present here serves as an entry point to an understanding 18 of biofilm formation among class Clostridia and allowed us to predict a model for Clostridial cellulose 19 synthesis.20 Author summary 21 Biofilms are communities of microorganisms that enmesh themselves in a protective matrix of elf-22 produced polysaccharide materials. Biofilms have demonstrated roles in both virulence and persistence 23 among bacterial pathogens of global health importance. The class Clostridia are a polyphyletic grouping 24 of primarily Gram-positive, anaerobic and spore-forming bacteria which contain the important and well-25 studied human pathogens Clostridioides difficile, Clostridium botulinum, and Clostridium perfringens, 26among others. Bacteria belonging to class Clostridia have been anecdotally reported to form biofilms described. In this work, we identify a gene cluster, which we name ccsABZHI, for the Clostridial cellulose 29 synthase, which bears remarkable similarity to molecular machinery required for the production of 30 cellulose biofilms in other Gram-negative bacteria. We further biochemically characterize one of these 31 enzymes, CcsZ, a predicted endoglucanase which we predicted from our model should cleave cellulose 32 exopolysaccharides. We show that CcsZ is in fact capable of this activity and belongs to a broader family 33 of glycoside hydrolases with unexpected...

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confidence: 99%

Identification of the Clostridial cellulose synthase and characterization of the cognate glycosyl hydrolase, CcsZ

Scott

Lowrance

Anderson

et al. 2019

Preprint

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“…Despite their differences, both NTS and typhoidal Salmonella strains rely on type three secretion systems (T3SS) to stimulate invasion, uptake, and survival within human epithelial cells and macrophages (6). While our understanding of pathogenesis is improving, less is known about the strategies that pathogenic Salmonella strains employ to survive outside the host (7,8). It is generally assumed that people become infected with Salmonella through ingestion of contaminated food and water, but there are also numerous examples of sporadic human cases where the causative source is unknown (9).…”

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confidence: 99%

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

MacKenzie

Wang²,

Shivak

et al. 2015

Infect Immun

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f Pathogenic bacteria often need to survive in the host and the environment, and it is not well understood how cells transition between these equally challenging situations. For the human and animal pathogen Salmonella enterica serovar Typhimurium, biofilm formation is correlated with persistence outside a host, but the connection to virulence is unknown. In this study, we analyzed multicellular-aggregate and planktonic-cell subpopulations that coexist when S. Typhimurium is grown under biofilminducing conditions. These cell types arise due to bistable expression of CsgD, the central biofilm regulator. Despite being exposed to the same stresses, the two cell subpopulations had 1,856 genes that were differentially expressed, as determined by transcriptome sequencing (RNA-seq). Aggregated cells displayed the characteristic gene expression of biofilms, whereas planktonic cells had enhanced expression of numerous virulence genes. Increased type three secretion synthesis in planktonic cells correlated with enhanced invasion of a human intestinal cell line and significantly increased virulence in mice compared to the aggregates. However, when the same groups of cells were exposed to desiccation, the aggregates survived better, and the competitive advantage of planktonic cells was lost. We hypothesize that CsgD-based differentiation is a form of bet hedging, with single cells primed for host cell invasion and aggregated cells adapted for persistence in the environment. This allows S. Typhimurium to spread the risks of transmission and ensures a smooth transition between the host and the environment.

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“…Salmonella bacteria can survive for some time without a host; thus, they are frequently found in polluted water, with contamination from the excrement of carrier animals being particularly important (Waldner et al. ).…”

Section: Introductionmentioning

confidence: 99%

“…Some people afflicted with salmonellosis later experience reactive arthritis, which can have long-lasting, disabling effects (Ajene et al 2013). Salmonella bacteria can survive for some time without a host; thus, they are frequently found in polluted water, with contamination from the excrement of carrier animals being particularly important (Waldner et al 2012 Escherichia coli, another bacterium in the family Enterobacteriaceae and a quite similar organism to Salmonella, is commonly referred to as the colon bacillus because of its prevalence in the gastrointestinal tract of humans and other animals. For decades, public health laboratories have used the presence of this and related organisms (coliforms) in sources of drinking water as a sign of fecal contamination and an indication that water is not fit for human consumption.…”

Section: Introductionmentioning

confidence: 99%

Inactivation of Salmonella on tainted foods: using blue light to disinfect cucumbers and processed meat products

Guffey

Payne

Motts

et al. 2016

Food Science & Nutrition

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Foodborne illness resulting from infectious organisms occurring in vegetables and processed meat is a serious health concern in the United States. Improved and cost‐effective techniques for disinfection are needed. Visible light in the blue range (405 nm) was administered to processed meat that had been inoculated with Escherichia coli. One application of light energy at doses of 10, 30, 60, and 100 J/cm2 was applied, in vitro. In the case of vegetables contaminated with Salmonella (cucumbers), 464 nm light was used at 6, 12, and 18 J/cm2. In both cases, after 20 hours of incubation, colony‐forming units were counted and compared to controls to determine whether the light energy inhibited growth of E. coli or Salmonella. E. coli – 405 nm light at doses of 30, 60, and 100 J/cm2 were all effective inhibitors of the organism. Kill rates of 75.61 – 96.34% were achieved. Salmonella – 464 nm light at doses of 6, 12, and 18 J/cm2 produced significant inactivation of the organism. Kill rates of 80.23–100% were obtained. Blue light, delivered in the wavelength/dose combinations used in this study is an effective inhibitor of both E. coli and Salmonella on actual foodstuffs. Blue light should be considered as a potentially effective tool in the effort to protect humans from foodborne illnesses.

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From Exit to Entry: Long-term Survival and Transmission of Salmonella

Cited by 43 publications

References 147 publications

Identification of the Clostridial cellulose synthase and characterization of the cognate glycosyl hydrolase, CcsZ

Identification of the Clostridial cellulose synthase and characterization of the cognate glycosyl hydrolase, CcsZ

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

Inactivation of Salmonella on tainted foods: using blue light to disinfect cucumbers and processed meat products

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