Characterization of Two-Component System CitB Family in Salmonella Pullorum

Salmonella enterica, serovar Gallinarum, biovar Pullorum, is an avian-specific pathogen which has caused considerable economic losses to the poultry industry worldwide. Two-component systems (TCSs) play an essential role in obtaining nutrients, detecting the presence of neighboring bacteria and regulating the expression of virulence factors. The genome analysis of S. Pullorum strain S06004 suggesting the carriage of 22 pairs of TCSs, which belong to five families named CitB, OmpR, NarL, Chemotaxis and LuxR. In the CitB family, three pairs of TCSs, namely CitA-CitB, DcuS-DcuR and DpiB-DpiA, remain unaddressed in S. Pullorum. To systematically investigate the function of the CitB family in S. Pullorum, four mutants, ΔcitAB (abbreviated as Δcit), ΔdcuSR (Δdcu), ΔdpiBA (Δdpi) and ΔcitABΔdcuSRΔdpiBA (Δ3), were made using the CRISPR/Cas9 system. The results demonstrated that the CitB family did not affect the growth of bacteria, the results of biochemical tests, invasion and proliferation in chicken macrophage HD-11 cells and the expression of fimbrial protein. But the mutants showed thicker biofilm formation, higher resistance to antimicrobial agents, enhanced tolerance to inhibition by egg albumen and increased virulence in chicken embryos. Moreover, the deletion of Dpi TCS was detrimental to survival after exposure to hyperosmotic and oxidative environments, as well as the long-term colonization of the small intestine of chickens. Collectively, we provided new knowledge regarding the possible role of the CitB family involved in the pathogenic processes of S. Pullorum.

[1]  Xiaoping Zhou,et al.  A global dataset for prevalence of Salmonella Gallinarum between 1945 and 2021 , 2022, Scientific data.

[2]  Biao Tang,et al.  Higher tolerance of predominant Salmonella serovars circulating in the antibiotic-free feed farms to environmental stresses. , 2022, Journal of hazardous materials.

[3]  J. Gunn,et al.  The Abundance and Organization of Salmonella Extracellular Polymeric Substances in Gallbladder-Mimicking Environments and In Vivo , 2021, Infection and immunity.

[4]  E. Groisman,et al.  How the PhoP/PhoQ System Controls Virulence and Mg2+ Homeostasis: Lessons in Signal Transduction, Pathogenesis, Physiology, and Evolution , 2021, Microbiology and molecular biology reviews : MMBR.

[5]  R. Ferreira,et al.  The role of two-component regulatory systems in environmental sensing and virulence in Salmonella , 2021, Critical reviews in microbiology.

[6]  K. Schat,et al.  Pullorum Disease: Evolution of the Eradication Strategy , 2021, Avian Diseases.

[7]  X. Niu,et al.  Establishment and evaluation of an indirect ELISA for detection of antibodies to goat Klebsiella pneumonia , 2020, BMC Veterinary Research.

[8]  M. Hess,et al.  Bacterial Infection in Chicken Embryos and Consequences of Yolk Sac Constitution for Embryo Survival , 2020, Veterinary pathology.

[9]  Zhe Ma,et al.  PagC is involved in salmonella pullorum OMVs production and affects biofilm production. , 2020, Veterinary microbiology.

[10]  Liang Zhang,et al.  The Characterization of Two-Component System PmrA/PmrB in Cronobacter sakazakii , 2020, Frontiers in Microbiology.

[11]  J. E. Olsen,et al.  Dynamics and Outcome of Macrophage Interaction Between Salmonella Gallinarum, Salmonella Typhimurium, and Salmonella Dublin and Macrophages From Chicken and Cattle , 2020, Frontiers in Cellular and Infection Microbiology.

[12]  Qigai He,et al.  Antibiotic Resistance Profiles of Salmonella Recovered From Finishing Pigs and Slaughter Facilities in Henan, China , 2019, Front. Microbiol..

[13]  Rafał Kolenda,et al.  Everything You Always Wanted to Know About Salmonella Type 1 Fimbriae, but Were Afraid to Ask , 2019, Front. Microbiol..

[14]  X. Jiao,et al.  Loss and Gain in the Evolution of the Salmonella enterica Serovar Gallinarum Biovar Pullorum Genome , 2019, mSphere.

[15]  Yitian Zhou,et al.  CitAB Two-Component System-Regulated Citrate Utilization Contributes to Vibrio cholerae Competitiveness with the Gut Microbiota , 2018, Infection and Immunity.

[16]  F. Jacob-Dubuisson,et al.  Structural insights into the signalling mechanisms of two-component systems , 2018, Nature Reviews Microbiology.

[17]  A. Jayaraman,et al.  The microbiota metabolite indole inhibits Salmonella virulence: Involvement of the PhoPQ two-component system , 2018, PloS one.

[18]  S. Wei,et al.  Construction of Salmonella Pullorum ghost by co-expression of lysis gene E and the antimicrobial peptide SMAP29 and evaluation of its immune efficacy in specific-pathogen-free chicks , 2018 .

[19]  S. Khanal,et al.  Isolation and Genomic Identification of Salmonella Pullorum in the Poultry Farms of Nepal , 2017 .

[20]  Didier Y. R. Stainier,et al.  Genetic compensation: A phenomenon in search of mechanisms , 2017, PLoS genetics.

[21]  Z. Pan,et al.  O-polysaccharide is important for Salmonella Pullorum survival in egg albumen, and virulence and colonization in chicken embryos , 2017, Avian pathology : journal of the W.V.P.A.

[22]  X. Jiao,et al.  Influence of Salmonella enterica serovar Pullorum pathogenicity island 2 on type III secretion system effector gene expression in chicken macrophage HD11 cells , 2017, Avian pathology : journal of the W.V.P.A.

[23]  Nancy R. Zhang,et al.  Allelic variation contributes to bacterial host specificity , 2015, Nature Communications.

[24]  M. A. De la Cruz,et al.  The two-component system CpxR/A represses the expression of Salmonella virulence genes by affecting the stability of the transcriptional regulator HilD , 2015, Front. Microbiol..

[25]  Sheng Yang,et al.  Multigene Editing in the Escherichia coli Genome via the CRISPR-Cas9 System , 2015, Applied and Environmental Microbiology.

[26]  Guang-jian Li,et al.  The Role of the QseC Quorum-Sensing Sensor Kinase in Epinephrine-Enhanced Motility and Biofilm Formation by Escherichia coli , 2014, Cell Biochemistry and Biophysics.

[27]  E. H. Chowdhury,et al.  Mode of vertical transmission of Salmonella enterica sub. enterica serovar Pullorum in chickens , 2014 .

[28]  D. Schifferli,et al.  Allelic variation in Salmonella: an underappreciated driver of adaptation and virulence , 2014, Front. Microbiol..

[29]  Steven C. Ricke,et al.  Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars , 2013, Microbiology and Molecular Reviews.

[30]  R. Edwards,et al.  Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution , 2012, PloS one.

[31]  P. Kaiser,et al.  Immune dynamics following infection of avian macrophages and epithelial cells with typhoidal and non-typhoidal Salmonella enterica serovars; bacterial invasion and persistence, nitric oxide and oxygen production, differential host gene expression, NF-κB signalling and cell cytotoxicity. , 2012, Veterinary immunology and immunopathology.

[32]  D. Call,et al.  Salmonella Enteritidis strains from poultry exhibit differential responses to acid stress, oxidative stress, and survival in the egg albumen. , 2012, Foodborne pathogens and disease.

[33]  P. Barrow,et al.  Pullorum disease and fowl typhoid—new thoughts on old diseases: a review , 2011, Avian pathology : journal of the W.V.P.A.

[34]  J. Jian,et al.  Expression, purification and antibody preparation of flagellin FlaA from Vibrio alginolyticus strain HY9901 , 2010, Letters in applied microbiology.

[35]  S. Gottesman,et al.  A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two‐component system , 2009, Molecular microbiology.

[36]  M. Lemos,et al.  Molecular differentiation between Salmonella enterica subsp enterica serovar Pullorum and Salmonella enterica subsp enterica serovar Gallinarum , 2009, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[37]  Naotake Ogasawara,et al.  Anaerobic Regulation of Citrate Fermentation by CitAB in Escherichia coli , 2008, Bioscience, biotechnology, and biochemistry.

[38]  Y. Chuang,et al.  Identification of the genetic determinants of Salmonella enterica serotype Typhimurium that may regulate the expression of the type 1 fimbriae in response to solid agar and static broth culture conditions , 2008, BMC Microbiology.

[39]  Akinori Kato,et al.  The PhoQ/PhoP regulatory network of Salmonella enterica. , 2008, Advances in experimental medicine and biology.

[40]  F. C. Soncini,et al.  Induction of RpoS Degradation by the Two-Component System Regulator RstA in Salmonella enterica , 2007, Journal of bacteriology.

[41]  E. Groisman,et al.  The PmrA/PmrB and RcsC/YojN/RcsB systems control expression of the Salmonella O‐antigen chain length determinant , 2006, Molecular microbiology.

[42]  B. De Moor,et al.  In silico identification and experimental validation of PmrAB targets in Salmonella typhimurium by regulatory motif detection , 2004, Genome Biology.

[43]  Stanley N Cohen,et al.  DpiA Binding to the Replication Origin of Escherichia coli Plasmids and Chromosomes Destabilizes Plasmid Inheritance and Induces the Bacterial SOS Response , 2003, Journal of bacteriology.

[44]  G. Unden,et al.  Function of DcuS from Escherichia coli as a Fumarate-stimulated Histidine Protein Kinase in Vitro * , 2002, The Journal of Biological Chemistry.

[45]  M. Bott,et al.  The sensor kinase CitA (DpiB) of Escherichia coli functions as a high-affinity citrate receptor , 2002, Archives of Microbiology.

[46]  A. Smith,et al.  Salmonella enterica Serovar Pullorum Persists in Splenic Macrophages and in the Reproductive Tract during Persistent, Disease-Free Carriage in Chickens , 2001, Infection and Immunity.

[47]  Ann M Stock,et al.  Histidine kinases and response regulator proteins in two-component signaling systems. , 2001, Trends in biochemical sciences.

[48]  H. Shivaprasad Fowl typhoid and pullorum disease. , 2000, Revue scientifique et technique.

[49]  F. Fang,et al.  Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. , 2000, Science.

[50]  B. Hargis,et al.  Tracing the Origins of Salmonella Outbreaks , 2000, Science.

[51]  M. Bott,et al.  The periplasmic domain of the histidine autokinase CitA functions as a highly specific citrate receptor , 1999, Molecular microbiology.

[52]  M. Popoff,et al.  The RcsB–RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity , 1998, Molecular microbiology.

[53]  S. Miller,et al.  PmrA–PmrB‐regulated genes necessary for 4‐aminoarabinose lipid A modification and polymyxin resistance , 1998, Molecular microbiology.

[54]  K. Roland,et al.  Spontaneous pmrA mutants of Salmonella typhimurium LT2 define a new two-component regulatory system with a possible role in virulence , 1993, Journal of bacteriology.

[55]  S. Miller,et al.  Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages , 1990, Journal of bacteriology.

[56]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.