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Single cell analyses reveal distinct adaptation of typhoidal and non-typhoidal Salmonella enterica serovars to intracellular lifestyle.

ABSTRACT: Salmonella enterica is a common foodborne, facultative intracellular enteropathogen. Human-restricted typhoidal S. enterica serovars Typhi (STY) or Paratyphi A (SPA) cause severe typhoid or paratyphoid fever, while many S. enterica serovar Typhimurium (STM) strains have a broad host range and in human hosts usually lead to a self-limiting gastroenteritis. Due to restriction of STY and SPA to primate hosts, experimental systems for studying the pathogenesis of typhoid and paratyphoid fever are limited. Therefore, STM infection of susceptible mice is commonly considered as model system for studying these diseases. The type III secretion system encoded by Salmonella pathogenicity island 2 (SPI2-T3SS) is a key factor for intracellular survival of Salmonella. Inside host cells, the pathogen resides within the Salmonella-containing vacuole (SCV) and induces tubular structures extending from the SCV, termed Salmonella-induced filaments (SIF). This study applies single cell analyses approaches, which are flow cytometry of Salmonella harboring dual fluorescent protein reporters, effector translocation, and correlative light and electron microscopy to investigate the fate and activities of intracellular STY and SPA. The SPI2-T3SS of STY and SPA is functional in translocation of effector proteins, SCV and SIF formation. However, only a low proportion of intracellular STY and SPA are actively deploying SPI2-T3SS and STY and SPA exhibited a rapid decline of protein biosynthesis upon experimental induction. A role of SPI2-T3SS for proliferation of STY and SPA in epithelial cells was observed, but not for survival or proliferation in phagocytic host cells. Our results indicate that reduced intracellular activities are factors of the stealth strategy of STY and SPA and facilitate systemic spread and persistence of the typhoidal Salmonella.

SUBMITTER: Reuter T

PROVIDER: S-EPMC8244875 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:IntroductionSalmonella is considered one of the most significant pathogens in public health since it is a bacterium that is frequently linked to food-borne illnesses in humans. Some Salmonella serovars are responsible for outbreaks that are connected to the consumption of animal products. Cattle are connected to humans through a shared environment and the food chain as a significant source of animal protein. In Nigeria, antimicrobial medications are easily accessible for use in food-producing animals. Abattoir environments are reservoirs of foodborne bacteria like non-typhoidal Salmonella enterica (NTS), that have become resistant to antibiotics used for prophylaxis or treatment in animals. This study investigated the prevalence and resistance patterns of Salmonella enterica serovars in abattoir employees, beef cattle and abattoir environments in Abuja and Lagos, Nigeria.MethodsA total of 448 samples were collected from healthy personnel, slaughtered cattle, and abattoir environments between May and December 2020. Using Kirby-Bauer disk diffusion method, the resistance profile of NTS isolates were determined. Multidrug resistance (MDR) was considered when NTS was resistant to ≥3 antimicrobial drug classes. We performed phenotypic and genotypic characterizations of all Salmonella isolates including serotyping. Descriptive statistics were used to analyze the data.ResultsTwenty-seven (6%) NTS isolates were obtained. Prevalence of NTS was highest in abattoir environments (15.5%; 9/58), followed by cattle (4.8%;13/272) and abattoir employees (4.2%; 5/118). A high prevalence of resistance was observed for gentamicin (85.2%; 23/27) and tetracycline (77.8%; 21/27). Whole-genome sequencing of 22 NTS showed dissemination of aac(6')-laa (22/22), qnrB19 (1/22), fosA7 (1/22), and tetA (1/22) genes. Serovar diversity of NTS varied with source. S. Anatum, a rare serovar predominated with a prevalence of 18.2% (4/22). Chromosomal point mutations showed ParC T57S substitution in 22 NTS analyzed. Among 22 NTS, 131 mobile genetic elements (MGEs) were detected including insertion sequences (56.5%) and miniature inverted repeats (43.5%). Two integrating MGEs IS6 and IS21 were observed to carry the tetA gene + Incl-1 on the same contig in NTS originating from cattle. Rare serovars namely S. Abony and S. Stormont with MDR phenotypes recovered from cattle and abattoir environments were closely related with a pairwise distance of ≤5 SNPs.ConclusionsFirst report of rare serovars in Nigeria with MDR phenotypes in humans, cattle, and abattoir environments. This study demonstrates the spread of resistance in the abattoir environment possibly by MGEs and emphasizes the importance of genomic surveillance. Beef cattle may be a risk to public health because they spread a variety of rare Salmonella serovars. Therefore, encouraging hand hygiene among abattoir employees while processing beef cattle will further reduce NTS colonization in this population. This requires a One Health collaborative effort among various stakeholders in human health, animal health, and environmental health.

Project description:BackgroundNon-typhoidal Salmonella enterica serovars, associated with different foods including poultry products, are important causes of bacterial gastroenteritis worldwide. The colonization of the chicken gut by S. enterica could result in the contamination of the environment and food chain. The aim of this study was to compare the genomes of 25 S. enterica serovars isolated from broiler chicken farms to assess their intra- and inter-genetic variability, with a focus on virulence and antibiotic resistance characteristics.Methodology/principal findingThe genomes of 25 S. enterica isolates covering five serovars (ten Typhimurium including three monophasic 4,[5],12:i:, four Enteritidis, three Hadar, four Heidelberg and four Kentucky) were sequenced. Most serovars were clustered in strongly supported phylogenetic clades, except for isolates of serovar Enteritidis that were scattered throughout the tree. Plasmids of varying sizes were detected in several isolates independently of serovars. Genes associated with the IncF plasmid and the IncI1 plasmid were identified in twelve and four isolates, respectively, while genes associated with the IncQ plasmid were found in one isolate. The presence of numerous genes associated with Salmonella pathogenicity islands (SPIs) was also confirmed. Components of the type III and IV secretion systems (T3SS and T4SS) varied in different isolates, which could explain in part, differences of their pathogenicity in humans and/or persistence in broilers. Conserved clusters of genes in the T3SS were detected that could be used in designing effective strategies (diagnostic, vaccination or treatments) to combat Salmonella. Antibiotic resistance genes (CMY, aadA, ampC, florR, sul1, sulI, tetAB, and srtA) and class I integrons were detected in resistant isolates while all isolates carried multidrug efflux pump systems regardless of their antibiotic susceptibility profile.Conclusions/significanceThis study showed that the predominant Salmonella serovars in broiler chickens harbor genes encoding adhesins, flagellar proteins, T3SS, iron acquisition systems, and antibiotic and metal resistance genes that may explain their pathogenicity, colonization ability and persistence in chicken. The existence of mobile genetic elements indicates that isolates from a given serovar could acquire and transfer genetic material. Conserved genes in the T3SS and T4SS that we have identified are promising candidates for identification of diagnostic, antimicrobial or vaccine targets for the control of Salmonella in broiler chickens.

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Single cell analyses reveal distinct adaptation of typhoidal and non-typhoidal Salmonella enterica serovars to intracellular lifestyle.

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