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Genomic Characterization of a Nalidixic Acid-Resistant Salmonella Enteritidis Strain Causing Persistent Infections in Broiler Chickens.

ABSTRACT: Virulent strains of Salmonella enterica subsp. enterica serovar Enteritidis (SE) harbored by poultry can cause disease in poultry flocks and potentially result in human foodborne illness. Two broiler flocks grown a year apart on the same premises experienced mortality throughout the growing period due to septicemic disease caused by SE. Gross lesions predominantly consisted of polyserositis followed by yolk sacculitis, arthritis, osteomyelitis, and spondylitis. Tissues with lesions were cultured yielding 59 SE isolates. These were genotyped by Rep-PCR followed by whole-genome sequencing (WGS) of 15 isolates which were clonal. The strain, SE_TAU19, was further characterized for antimicrobial susceptibility and virulence in a broiler embryo lethality assay. SE_TAU19 was resistant to nalidixic acid and sulfadimethoxine and was virulent to embryos with 100% mortality of all challenged broiler embryos within 3.5 days. Screening the SE_TAU19 whole-genome sequence revealed seven antimicrobial resistance (AMR) genes, 120 virulence genes, and two IncF plasmid replicons corresponding to a single, serovar-specific pSEV virulence plasmid. The pef, spv, and rck virulence genes localized to the plasmid sequence assembly. We report phenotypic and genomic features of a virulent SE strain from persistently infected broiler flocks and present a workflow for SE characterization from isolate collection to genome assembly and sequence analysis. Further SE surveillance and investigation of SE virulence in broiler chickens is warranted.

SUBMITTER: Walker GK

PROVIDER: S-EPMC8440904 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:Restrictions of in-feed antibiotics use in poultry has pushed research toward finding appropriate alternatives such as Direct-Fed Microbials (DFM). In this study, previously tested Bacillus isolates (B. subtilis and B. amyloliquefaciens) were used to evaluate their therapeutic and prophylactic effects against Salmonella enterica serovar Enteritidis (S. Enteritidis) in broiler chickens. For this purpose, initial antibacterial activity of Bacillus-DFM (104 spores/g or 106 spores/g) against S. Enteritidis colonization in crop, proventriculus and intestine was investigated using an in vitro digestive model. Furthermore, to evaluate therapeutic and prophylactic effects of Bacillus-DFM (104 spores/g) against S. Enteritidis colonization, altogether 60 (n = 30/group) and 30 (n = 15/group) 1-day-old broiler chickens were randomly allocated to either DFM or control group (without Bacillus-DFM), respectively. Chickens were orally gavaged with 104 cfu of S. Enteritidis per chicken at 1-day old, and cecal tonsils (CT) and crop were collected 3 and 10 days later during the therapeutic study, whereas they were orally gavaged with 107 cfu of S. Enteritidis per chicken at 6-day-old, and CT and crop were collected 24 h later from two independent trials during the prophylactic study. Serum superoxide dismutase (SOD), FITC-d and intestinal IgA levels were reported for both chicken studies, in addition cecal microbiota analysis was performed during the therapeutic study. DFM significantly reduced S. Enteritidis concentration in the intestine compartment, and in both proventriculus and intestine compartments as compared to the control when used at 104 spores/g and 106 spores/g, respectively (p < 0.05). DFM significantly reduced FITC-d and IgA as well as SOD and IgA levels (p < 0.05) compared to the control in therapeutic and prophylactic studies, respectively. Interestingly, in the therapeutic study, there were significant differences in bacterial community structure and predicted metabolic pathways between DFM and control. Likewise, phylum Actinobacteria and the genera Bifidobacterium, Roseburia, Proteus, and cc_115 were decreased, while the genus Streptococcus was enriched significantly in the DFM group as compared to the control (MetagenomeSeq, p < 0.05). Thus, the overall results suggest that the Bacillus-DFM can reduce S. Enteritidis colonization and improve the intestinal health in chickens through mechanism(s) that might involve the modulation of gut microbiota and their metabolic pathways.

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Genomic Characterization of a Nalidixic Acid-Resistant Salmonella Enteritidis Strain Causing Persistent Infections in Broiler Chickens.

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