Salmonella enterica virulence databases and bioinformatic analysis tools development.
Salmonella
Database
Virulence genes
WGS analyses tools
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 Oct 2024
24 Oct 2024
Historique:
received:
25
06
2024
accepted:
24
09
2024
medline:
25
10
2024
pubmed:
25
10
2024
entrez:
25
10
2024
Statut:
epublish
Résumé
Salmonella enterica, a prominent foodborne pathogen, contributes significantly to global foodborne illnesses annually. This species exhibits significant genetic diversity, potentially impacting its infectivity, disease severity, and antimicrobial resistance. Whole genome sequencing (WGS) offers comprehensive genetic insights that can be utilized for virulence assessment. However, existing bioinformatic tools for studying Salmonella virulence have notable limitations. To address this gap, a Salmonella Virulence Database with a non-redundant, comprehensive list of putative virulence factors was constructed. Two bioinformatic analysis tools, Virulence Factor Profile Assessment and Virulence Factor Profile Comparison tools, were developed. The former provides data on similarity to the reference genes, e-value, and bite score, while the latter assesses the presence/absence of virulence genes in Salmonella isolates and facilitates comparison of virulence profiles across multiple sequences. To validate the database and associated bioinformatic tools, WGS data from 43,853 Salmonella isolates spanning 14 serovars was extracted from GenBank, and WGS data previously generated in our lab was used. Overall, the Salmonella Virulence database and our bioinformatic tools effectively facilitated virulence assessment, enhancing our understanding of virulence profiles among Salmonella isolates and serovars. The public availability of these resources will empower researchers to assess Salmonella virulence comprehensively, which could inform strategies for pathogen control and risk evaluations associated with human illnesses.
Identifiants
pubmed: 39448688
doi: 10.1038/s41598-024-74124-x
pii: 10.1038/s41598-024-74124-x
doi:
Substances chimiques
Virulence Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25228Subventions
Organisme : U.S. Food and Drug Administration
ID : E0765901
Organisme : U.S. Food and Drug Administration
ID : E0765901
Organisme : U.S. Food and Drug Administration
ID : E0765901
Organisme : U.S. Food and Drug Administration
ID : E0765901
Informations de copyright
© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
CDC. in Antibiotic Resistance Threats in the United States, 2019. (2019).
(IFSAC), T.I.F.S.A.C. Foodborne illness source attribution estimates for 2017 for Salmonella, Escherichia coli O157, Listeria monocytogenes, and Campylobacter using multi-year outbreak surveillance data, United States (2019).
CDC. National Salmonella Surveillance Annual Report, 2018. (2016).
Sayers, S. et al. Victors: A web-based knowledge base of virulence factors in human and animal pathogens. Nucleic Acids Res. 47(D1), D693–D700 (2019).
doi: 10.1093/nar/gky999
pubmed: 30365026
Andino, A. & Hanning, I. Salmonella enterica: Survival, colonization, and virulence differences among serovars.Sci. World J.2015, 520179 (2015).
Foley, S. L. & Lynne, A. M. Food animal-associated Salmonella challenges: Pathogenicity and antimicrobial resistance. J. Anim. Sci. 86(14 Suppl), E173–E187 (2008).
doi: 10.2527/jas.2007-0447
pubmed: 17878285
Fierer, J. Invasive non-typhoidal Salmonella (iNTS) infections. Clin. Infect. Dis. 75 (4), 732–738 (2022).
doi: 10.1093/cid/ciac035
pubmed: 35041743
Suez, J. et al. Virulence gene profiling and pathogenicity characterization of non-typhoidal Salmonella accounted for invasive disease in humans. PLoS One. 8 (3), e58449 (2013).
doi: 10.1371/journal.pone.0058449
pubmed: 23505508
pmcid: 3591323
Johnson, T. J. & Nolan, L. K. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol. Mol. Biol. Rev. 73 (4), 750–774 (2009).
doi: 10.1128/MMBR.00015-09
pubmed: 19946140
pmcid: 2786578
Gokulan, K. et al. Impact of plasmids, including those encodingVirB4/D4 type IV secretion systems, on Salmonella enterica Serovar Heidelberg virulence in macrophages and epithelial cells. PLoS One. 8 (10), e77866 (2013).
doi: 10.1371/journal.pone.0077866
pubmed: 24098597
pmcid: 3789690
Brown, E. et al. Use of whole-genome sequencinG for food safety and public health in the United States. Foodborne Pathog Dis. 16(7), 441–450 (2019).
doi: 10.1089/fpd.2019.2662
pubmed: 31194586
pmcid: 6653787
Mao, C. et al. Curation, integration and visualization of bacterial virulence factors in PATRIC. Bioinformatics. 31 (2), 252–258 (2015).
doi: 10.1093/bioinformatics/btu631
pubmed: 25273106
Wattam, A. R. et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res. 45(D1), D535–D542 (2017).
doi: 10.1093/nar/gkw1017
pubmed: 27899627
Chen, L. et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 33 (Database issue), D325–D328 (2005).
doi: 10.1093/nar/gki008
pubmed: 15608208
Han, J. et al. Infection biology of Salmonella enterica. EcoSal Plus, eesp–0001. (2024).
McKinney, W. Pandas: A foundational python library for data analysis and statistics. Python High. Perform. Sci. Comput. 14(9), 1–9 (2011).
Azimi, T. et al. Molecular mechanisms of Salmonella effector proteins: A comprehensive review. Infect. Drug Resist.13, 11–26 (2020).
doi: 10.2147/IDR.S230604
pubmed: 32021316
pmcid: 6954085
Dos Santos, A. M. P., Ferrari, R. G. & Conte-Junior, C. A. Virulence factors in Salmonella Typhimurium: The sagacity of a bacterium. Curr. Microbiol. 76(6), 762–773 (2019).
doi: 10.1007/s00284-018-1510-4
pubmed: 29785632
Silva, C., Puente, J. L. & Calva, E. Salmonella Virulence plasmid: Pathogenesis and ecology. Pathog. Dis. (2017).
Sharma, A. K. et al. Bacterial virulence factors: Secreted for survival. Indian J. Microbiol. 57(1), 1–10 (2017).
doi: 10.1007/s12088-016-0625-1
pubmed: 28148975
Algarni, S. et al. Development of an antimicrobial resistance plasmid transfer gene database for enteric bacteria. Front. Bioinform. 3, 1279359 (2023).
doi: 10.3389/fbinf.2023.1279359
pubmed: 38033626
pmcid: 10682676
Tate, H. et al. Genomic diversity, antimicrobial resistance, and virulence gene profiles of Salmonella Serovar Kentucky isolated from humans, food, and animal Ceca content sources in the United States. Foodborne Pathog Dis. 19(8), 509–521 (2022).
doi: 10.1089/fpd.2022.0005
pubmed: 35960531
Aljahdali, N. H. et al. Genotypic and phenotypic characterization of incompatibility group FIB positive Salmonella enterica Serovar Typhimurium isolates from Food animal sources. Genes (Basel), 11(11), (2020).
Switt, A. I. et al. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i. Foodborne Pathog Dis. 6 (4), 407–415 (2009).
doi: 10.1089/fpd.2008.0213
pubmed: 19292687
pmcid: 3186709
Hopkins, K. L. et al. Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: A new pandemic strain?. Euro. Surveill 15(22), 19580 (2010).
doi: 10.2807/ese.15.22.19580-en
pubmed: 20546690
Marcus, S. L. et al. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect. 2 (2), 145–156 (2000).
doi: 10.1016/S1286-4579(00)00273-2
pubmed: 10742687
Teklemariam, A. D. et al. Human salmonellosis: A continuous global threat in the farm-to-Fork Food Safety Continuum. Foods, 12(9). (2023).
Cheng, R. A. & Wiedmann, M. Recent advances in our understanding of the diversity and roles of chaperone-usher Fimbriae in facilitating Salmonella host and tissue tropism. Front. Cell. Infect. Microbiol. 10, 628043 (2020).
doi: 10.3389/fcimb.2020.628043
pubmed: 33614531
Humphries, A. D. et al. Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol. Lett. 201 (2), 121–125 (2001).
doi: 10.1111/j.1574-6968.2001.tb10744.x
pubmed: 11470349
Forest, C. et al. Contribution of the stg fimbrial operon of Salmonella enterica Serovar Typhi during interaction with human cells. Infect. Immun. 75 (11), 5264–5271 (2007).
doi: 10.1128/IAI.00674-07
pubmed: 17709421
pmcid: 2168283
Zhang, X. L. et al. Salmonella enterica serovar typhi uses type IVB pili to enter human intestinal epithelial cells. Infect. Immun. 68 (6), 3067–3073 (2000).
doi: 10.1128/IAI.68.6.3067-3073.2000
pubmed: 10816445
pmcid: 97533
Wear, S. S. et al. Investigation of core machinery for biosynthesis of vi antigen capsular polysaccharides in Gram-negative bacteria. J. Biol. Chem. 298 (1), 101486 (2022).
doi: 10.1016/j.jbc.2021.101486
pubmed: 34896394
Rychlik, I., Gregorova, D. & Hradecka, H. Distribution and function of plasmids in Salmonella enterica. Vet. Microbiol. 112 (1), 1–10 (2006).
doi: 10.1016/j.vetmic.2005.10.030
pubmed: 16303262
Huehn, S. et al. Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathog Dis. 7 (5), 523–535 (2010).
doi: 10.1089/fpd.2009.0447
pubmed: 20039795
Lan, T. T. Q. et al. Distribution of virulence genes among Salmonella Serotypes isolated from pigs in Southern Vietnam. J. Food. Prot. 81 (9), 1459–1466 (2018).
doi: 10.4315/0362-028X.JFP-17-408
pubmed: 30084656
Baumler, A. J. et al. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect. Immun. 64 (1), 61–68 (1996).
doi: 10.1128/iai.64.1.61-68.1996
pubmed: 8557375
pmcid: 173728
Wang, F. et al. Flagellar Motility is Critical for Salmonella enterica Serovar Typhimurium Biofilm Development. (1664-302X (Print)).
Tawfick, M. M., Rosser, A. & Rajakumar, K. Heterologous expression of the Salmonella enterica Serovar Paratyphi A Stk fimbrial operon suggests a potential for repeat sequence-mediated low-frequency phase variation. Infect. Genet. Evol. 85, 104508 (2020).
doi: 10.1016/j.meegid.2020.104508
pubmed: 32835875
El Qaidi, S. et al. NleB/SseK effectors from Citrobacter rodentium, Escherichia coli, and Salmonella enterica display distinct differences in host substrate specificity. J. Biol. Chem. 292(27), 11423–11430 (2017).
doi: 10.1074/jbc.M117.790675
pubmed: 28522607
pmcid: 5500807
Jaslow, S. L. et al. Salmonella activation of STAT3 signaling by SarA effector promotes intracellular replication and production of IL-10. Cell. Rep. 23(12), 3525–3536 (2018).
doi: 10.1016/j.celrep.2018.05.072
pubmed: 29924996
pmcid: 6314477
Mulder, D. T., Cooper, C. A. & Coombes, B. K. Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica Serovar Typhimurium. Infect. Immun. 80 (6), 1996–2007 (2012).
doi: 10.1128/IAI.06205-11
pubmed: 22493086
pmcid: 3370595
Bao, H. et al. Genetic diversity and evolutionary features of type VI secretion systems in Salmonella. Future Microbiol. 14, 139–154 (2019).
doi: 10.2217/fmb-2018-0260
pubmed: 30672329
Chen, C., Yang, X. & Shen, X. Confirmed and potential roles of bacterial T6SSs in the intestinal ecosystem. Front. Microbiol. 10, 1484 (2019).
doi: 10.3389/fmicb.2019.01484
pubmed: 31316495
pmcid: 6611333
Blondel, C. J. et al. Identification and distribution of new candidate T6SS effectors encoded in Salmonella pathogenicity Island 6. Front. Microbiol. 14, 1252344 (2023).
doi: 10.3389/fmicb.2023.1252344
pubmed: 37664116
pmcid: 10469887
Thomson, N. R. et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18 (10), 1624–1637 (2008).
doi: 10.1101/gr.077404.108
pubmed: 18583645
pmcid: 2556274