Characterization of two-component system CitB family in Salmonella enterica serovar Gallinarum biovar Gallinarum

Chen, Jiaqi; Zhou, Xiao Hua; Tang, Yanting; Jiang, Zhijie; Kang, Xiamei; Wang, Jianfeng; Yue, Min

doi:10.1016/j.vetmic.2023.109659

Cited by 6 publications

(5 citation statements)

References 28 publications

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“…The targeted deletion mutants were constructed by homologous recombination via the CRISPR/Cas9-mediated genome-editing system ( 18 , 43 , 68 , 69 ), with minor changes. The sgRNA was designed through the online web server CHOPCHOP ( http://chopchop.cbu.uib.no ) and amplified with the primers gene-sgRNA-F/sgRNA-R.…”

Section: Methodsmentioning

confidence: 99%

Integrated OMICs approach reveals energy metabolism pathway is vital for Salmonella Pullorum survival within the egg white

Kang,

An,

Wang

et al. 2024

mSphere

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Eggs, an important part of a healthy daily diet, can protect chicken embryo development due to the shell barrier and various antibacterial components within the egg white. Our previous study demonstrated that Salmonella Pullorum, highly adapted to chickens, can survive in the egg white and, therefore, be passed to newly hatched chicks. However, the survival strategy of Salmonella Pullorum in antibacterial conditions remains unknown. The overall transcripts in the egg white showed a large-scale shift compared to LB broth. The expression of common response genes and pathways, such as those involved in iron uptake, biotin biosynthesis, and virulence, was significantly changed, consistent with the other transovarial transmission serovar Enteritidis. Notably, membrane stress response, amino acid metabolism, and carbohydrate metabolism were specifically affected. Additional upregulated functionally relevant genes (JI728_13095, JI728_13100, JI728_17960, JI728_10085, JI728_15605, and nhaA ) as mutants confirmed the susceptible phenotype. Furthermore, fim deletion resulted in an increased survival capacity in the egg white, consistent with the downregulated expression. The second-round RNA-Seq analysis of the Δ fim mutant in the egg white revealed significantly upregulated genes compared with the wild type in the egg white responsible for energy metabolism located on the hyc and hyp operons regulated by FhlA, indicating the Δ fim mutant cannot receive enough oxygen and switched to fermentative growth due to its inability to attach to the albumen surface. Together, this study provides a first estimate of the global transcriptional response of Salmonella Pullorum under antibacterial egg white and highlights the new potential role of fim deletion in optimizing energy metabolism pathways that may assist vertical transmission. IMPORTANCE Pullorum disease, causing serious embryo death and chick mortality, results in substantial economic losses worldwide due to transovarial transmission. Egg-borne outbreaks are frequently reported in many countries. The present study has filled the knowledge gap regarding how the specific chicken-adapted pathogen Salmonella Pullorum behaves within the challenging environment of egg white. The deletion of the fim fimbrial system can increase survival in the albumen, possibly by reprogramming metabolism-related gene products, which reveals a new adaptive strategy of pathogens. Moreover, the comparison, including previous research on Salmonella Enteritidis, capable of vertical transmission, aims to provide diversified data sets in the field and further help to implement reasonable and effective measures to improve both food safety and animal health.

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Section: Methodsmentioning

confidence: 99%

Integrated OMICs approach reveals energy metabolism pathway is vital for Salmonella Pullorum survival within the egg white

Kang,

An,

Wang

et al. 2024

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“…The plates were incubated at 22°C and 37°C for three days. The following steps were the same as reported previously (Chen et al 2023) except for measuring the absorbance value at OD 590nm . Three independent experiments were conducted for each strain.…”

Section: Biofilm Formation Assaymentioning

confidence: 99%

“…Salmonella contains various virulence factors, including pathogenicity islands, flagella, and fimbriae, which play essential roles in different stages during infection (Chen et al 2023;Kang et al 2022;Klasa et al 2020;Kolenda et al 2019;Li et al 2022b). Fimbriae, especially type I fimbriae, enable Salmonella to adhere and colonize various host cells and abiotic surfaces (Kolenda et al 2019;Xu et al 2021).…”

Section: Introductionmentioning

confidence: 99%

Allelic functional variation of FimH among Salmonella enterica subspecies

Kang,

Chen,

Zhou

et al. 2023

Animal Diseases

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Salmonella enterica has a wide diversity, with numerous serovars belonging to six different subspecies with dynamic animal-host tropism. The FimH protein is the adhesin mediating binding to various cells, and slight amino acid discrepancy significantly affects the adherence capacities. To date, the general function of FimH variability across different subspecies of Salmonella enterica has not been addressed. To investigate the biological functions of FimH among the six Salmonella enterica subspecies, the present study performed several assays to determine biofilm formation, Caenorhabditis elegans killing, and intestinal porcine enterocyte cell IPEC-J2 adhesion by using various FimH allele mutants. In general, allelic mutations in both the lectin and pilin domains of FimH could cause changes in binding affinity, such as the N79S mutation. We also observed that the N79S variation in Salmonella Dublin increased the adhesive ability of IPEC-J2 cells. Moreover, a new amino acid substitution, T260M, within the pilin domain in one subspecies IIIb strain beneficial to binding to cells was highlighted in this study, even though the biofilm-forming and Caenorhabditis elegans-killing abilities exhibited no significant differences in variants. Combined with point mutations being a natural tendency due to positive selection in harsh environments, we speculate that allelic variation T260M probably contributes to pathoadaptive evolution in Salmonella enterica subspecies IIIb.

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“…Salmonella enterica serovar Gallinarum, an avian-restricted serovar, includes two common variants or biovars, Pullorum (causing Pullorum disease) and Gallinarum (causing fowl typhoid), resulting in devastating damage and economic loss in developing countries, including China [ 25–29 ], where increasing antimicrobial resistance (AMR) in these strains has become a significant concern [ 30–34 ]. Notably, Salmonella enterica serovar Gallinarum biovar Pullorum (bvSP) has a strong preference for affecting newly hatched chicks; in contrast, biovar Gallinarum (bvSG) mainly causes lethal diseases in adult birds [ 35 ]. Additionally, bvSP is very poor at colonization and survival in the gastrointestinal tract, and it can further develop transovarial transmission during industrialized breeding, where the underlying evolutionary driver remains obscure.…”

Section: Introductionmentioning

confidence: 99%

Genome degradation promotes Salmonella pathoadaptation by remodeling fimbriae-mediated proinflammatory response

Zhou,

Kang,

Chen

et al. 2023

National Science Review

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Understanding changes in pathogen behavior (e.g. increased virulence, a shift in transmission channel) constitutes a significant barrier to the public health management of emerging infectious diseases. Genome degradation via gene depletion or inactivation is recognized as a pathoadaptive feature of the pathogen evolving with the host. However, little is known about the exact role of genome degradation in affecting pathogenic behavior, and the underlying molecular detail has yet to be examined. Using large-scale global avian-restricted Salmonella genomes spanning more than a century, we projected the genetic diversity of Salmonella Pullorum (bvSP) with increasingly antimicrobial-resistant ST92 prevalent in Chinese flocks. The phylogenomic analysis identified three lineages in bvSP, with virulent enhancement in the recently emerged two lineages (L2/L3), as evidenced in chicken and embryo infection assays. Notably, the ancestor L1 lineage resembles the Salmonella serovars with higher metabolic flexibilities and more robust environmental tolerance, indicating stepwise evolutionary trajectories towards avian-restricted lineages. Pan-genome analysis pinpointed fimbrial degradation from a virulent lineage. Later engineered fim-deletion mutant, and all other five fimbrial systems, revealed behavior switching that restricted horizontal fecal-oral transmission but boosted virulence in chicks. By depleting fimbrial appendages, bvSP established persistent replication with less pro-inflammation in chick macrophages and adopted vertical transovarial transmission, accompanied by ever-increasing intensification in the poultry industry. Together, we uncovered a previously unseen paradigm for remodeling bacterial surface appendages that supplements virulence-enhanced evolution with increased vertical transmission.

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Characterization of two-component system CitB family in Salmonella enterica serovar Gallinarum biovar Gallinarum

Cited by 6 publications

References 28 publications

Integrated OMICs approach reveals energy metabolism pathway is vital for Salmonella Pullorum survival within the egg white

Integrated OMICs approach reveals energy metabolism pathway is vital for Salmonella Pullorum survival within the egg white

Allelic functional variation of FimH among Salmonella enterica subspecies

Genome degradation promotes Salmonella pathoadaptation by remodeling fimbriae-mediated proinflammatory response

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