Role of trehalose biosynthesis in environmental survival and virulence of Salmonella enterica serovar typhimurium

Howells, Angela M.; Bullifent, Helen L.; Dhaliwal, K. G.; Griffin, Kate F.; Castro, Arcadio García de; Frith, Graeme; Tunnacliffe, Alan; Titball, Richard W.

doi:10.1016/s0923-2508(02)01321-9

Cited by 33 publications

(24 citation statements)

References 22 publications

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“…A recent study by Fong and Wang (13) also showed the upregulation of otsB in S. enterica cells after a 6-day desiccation in peanut oil. Howells et al (36) observed that after incubation at 50°C for 7 min, the number of viable cells of an S. Typhimurium ΔotsA mutant decreased to 0.6% of the initial population, whereas the wild type had an 8% survival rate. Conversely, we did not identify the upregulation of the otsA or otsB gene previously reported to be involved in the desiccation tolerance of Salmonella.…”

Section: Discussionmentioning

confidence: 99%

Thermal Resistance and Gene Expression of both Desiccation-Adapted and Rehydrated Salmonella enterica Serovar Typhimurium Cells in Aged Broiler Litter

Zhao

Jiang

2017

Appl Environ Microbiol

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The objective of this study was to investigate the thermal resistance and gene expression of both desiccation-adapted and rehydrated Salmonella enterica serovar Typhimurium cells in aged broiler litter. S. Typhimurium was desiccation adapted in aged broiler litter with a 20% moisture content (water activity [a w ], 0.81) for 1, 2, 3, 12, or 24 h at room temperature and then rehydrated for 3 h. As analyzed by quantitative real-time reverse transcriptase PCR (qRT-PCR), the rpoS, proV, dnaK, and grpE genes were upregulated (P Ͻ 0.05) under desiccation stress and could be induced after 1 h but in less than 2 h. Following rehydration, fold changes in the levels of these four genes became significantly lower (P Ͻ 0.05). The desiccation-adapted ΔrpoS mutant was less heat resistant at 75°C than was the desiccation-adapted wild type (P Ͻ 0.05), whereas there were no differences in heat resistance between desiccation-adapted mutants in two nonregulated genes (otsA and PagfD) and the desiccation-adapted wild type (P Ͼ 0.05). Survival characteristics of the desiccation-adapted ΔPagfD (rdar [red, dry, and rough] morphotype) and ΔagfD (saw [smooth and white] morphotype) mutants were similar (P Ͼ 0.05). Trehalose synthesis in the desiccation-adapted wild type was not induced compared to a nonadapted control (P Ͼ 0.05). Our results demonstrated the importance of the rpoS, proV, dnaK, and grpE genes in the desiccation survival of S. Typhimurium. By using an ΔrpoS mutant, we found that the rpoS gene was involved in the crossprotection of desiccation-adapted S. Typhimurium against high temperatures, while trehalose synthesis or rdar morphology did not play a significant role in this phenomenon. In summary, S. Typhimurium could respond rapidly to low-a w conditions in aged broiler litter while developing cross-protection against high temperatures, but this process could be reversed upon rehydration.IMPORTANCE Physical heat treatment is effective in eliminating human pathogens from poultry litter used as biological soil amendments. However, prior to physical heat treatment, some populations of microorganisms may be adapted to the stressful conditions in poultry litter during composting or stockpiling, which may cross-protect them against subsequent high temperatures. Our previous study demonstrated that desiccation-adapted S. enterica cells in aged broiler litter exhibited enhanced thermal resistance. However, there is limited research on the underlying mechanisms of the extended survival of pathogens under desiccation conditions in animal wastes and cross-tolerance to subsequent heat treatment. Moreover, no information is available about the thermal resistance of desiccationadapted microorganisms in response to rehydration. Therefore, in the present study, we investigated the gene expression and thermal resistance of both desiccationadapted and rehydrated S. Typhimurium in aged broiler litter. This work will guide future research efforts to control human pathogens in animal wastes used as biological soil amendments.

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Section: Discussionmentioning

confidence: 99%

Thermal Resistance and Gene Expression of both Desiccation-Adapted and Rehydrated Salmonella enterica Serovar Typhimurium Cells in Aged Broiler Litter

Zhao

Jiang

2017

Appl Environ Microbiol

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“…This would fit with a model where the bacteria in the lumen are growing slowly or are under stress, as the trehalose operon is induced under these conditions in an RpoS-dependent manner (76,84). Trehalose has been demonstrated to play a role in cell protection against stressful environmental conditions, such as osmotic stress and heat shock, and was proposed to have a role in survival but not virulence (39).…”

Section: Discussionmentioning

confidence: 99%

Salmonella enterica Serovar Typhimurium Colonizing the Lumen of the Chicken Intestine Grows Slowly and Upregulates a Unique Set of Virulence and Metabolism Genes

Harvey¹,

Watson²,

Hulme

et al. 2011

Infect Immun

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The pattern of global gene expression in Salmonella enterica serovar Typhimurium bacteria harvested from the chicken intestinal lumen (cecum) was compared with that of a late-log-phase LB broth culture using a whole-genome microarray. Levels of transcription, translation, and cell division in vivo were lower than those in vitro. S. Typhimurium appeared to be using carbon sources, such as propionate, 1,2-propanediol, and ethanolamine, in addition to melibiose and ascorbate, the latter possibly transformed to D-xylulose. Amino acid starvation appeared to be a factor during colonization. Bacteria in the lumen were non-or weakly motile and nonchemotactic but showed upregulation of a number of fimbrial and Salmonella pathogenicity island 3 (SPI-3) and 5 genes, suggesting a close physical association with the host during colonization. S. Typhimurium bacteria harvested from the cecal mucosa showed an expression profile similar to that of bacteria from the intestinal lumen, except that levels of transcription, translation, and cell division were higher and glucose may also have been used as a carbon source.

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“…On the other hand, glycine-betaine, carnitine, ectoine, proline and trehalose have emerged as the principal compatible solutes (Csonka & Epstein, 1996;Bremer & Krämer, 2000;Howells et al, 2002;Sleator & Hill, 2002;García-Estepa et al, 2006). The genetic loci responsible for the synthesis or uptake of compatible solutes and potassium are highlighted in Fig.…”

Section: D Gel Electrophoresis Analyses By Vanmentioning

confidence: 99%

Salmonella spp. survival strategies within the host gastrointestinal tract

et al. 2011

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Human salmonellosis infections are usually acquired via the food chain as a result of the ability of Salmonella serovars to colonize and persist within the gastrointestinal tract of their hosts. In addition, after food ingestion and in order to cause foodborne disease in humans, Salmonella must be able to resist several deleterious stress conditions which are part of the host defence against infections. This review gives an overview of the main defensive mechanisms involved in the Salmonella response to the extreme acid conditions of the stomach, and the elevated concentrations of bile salts, osmolytes and commensal bacterial metabolites, and the low oxygen tension conditions of the mammalian and avian gastrointestinal tracts.

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Role of trehalose biosynthesis in environmental survival and virulence of Salmonella enterica serovar typhimurium

Cited by 33 publications

References 22 publications

Thermal Resistance and Gene Expression of both Desiccation-Adapted and Rehydrated Salmonella enterica Serovar Typhimurium Cells in Aged Broiler Litter

Thermal Resistance and Gene Expression of both Desiccation-Adapted and Rehydrated Salmonella enterica Serovar Typhimurium Cells in Aged Broiler Litter

Salmonella enterica Serovar Typhimurium Colonizing the Lumen of the Chicken Intestine Grows Slowly and Upregulates a Unique Set of Virulence and Metabolism Genes

Salmonella spp. survival strategies within the host gastrointestinal tract

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