1887

Journal of Medical Microbiology logo

Volume 72, Issue 7

The rare serovar Isangi: genomic characterization of the antimicrobial resistance, virulence potential and epidemiology of Brazilian strains in comparison to global isolates No Access

Abstract

serovar Isangi (. Isangi) is a rare non-typhoidal serovar, related to invasive nosocomial infections in various countries and to increasing antimicrobial resistance rates.

Despite existing reports on . Isangi, there is a lack of information of specific traits regarding this serovar, which could be improved through genomic analyses.

Our goals were to characterize the antimicrobial resistance, virulence potential and genomic relatedness of 11 . Isangi strains from Brazil in comparison to 185 genomes of global isolates using whole-genome sequencing (WGS) data.

Phenotypic resistance was determined by disc-diffusion. The search for resistance genes, plasmids, prophages, pathogenicity islands (SPIs) and virulence genes, plus multi-locus sequence typing (MLST) and core-genome MLST (cgMLST) were performed using WGS.

Brazilian . Isangi strains showed phenotypic resistance to nalidixic acid, ciprofloxacin and streptomycin, and harboured antimicrobial resistance [, , ] and heavy metal tolerance () genes. Col(pHAD28) and IncFII(S) plasmids, virulence genes related to adherence, macrophage induction, magnesium uptake, regulation and type III secretion systems, 12 SPIs and eight prophages were detected. The 185 additional global genomes analysed harboured resistance genes against 11 classes of antimicrobial compounds, 22 types of plasmids, 32 prophages, 14 SPIs, and additional virulence genes related to serum resistance, stress adaptation and toxins. Sequence type (ST)216 was assigned to genomes from Brazil and other countries, while ST335 was the most frequent ST, especially among South African genomes. cgMLST showed that Brazilian genomes were more closely related to genomes from European and African countries, the USA and Taiwan, while the majority of South African genomes were more closely related among each other.

The presence of . Isangi strains from Brazil and different countries showing a close genomic correlation, antimicrobial resistance profiles to drugs used in human therapy and a large number of virulence determinants reinforced the need for stronger initiatives to monitor rare non-typhoidal serovars such as . Isangi in order to prevent its dissemination among human and non-human sources.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , cgMLST , MLST and Salmonella Isangi
Funding
This study was supported by the:
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Award Finance Code 001)
    • Principle Award Recipient: FelipePinheiro Vilela
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 304803/2021-9)
    • Principle Award Recipient: JulianaPfrimer Falcao
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 304399/2018-3)
    • Principle Award Recipient: JulianaPfrimer Falcao
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 141017/2021-0)
    • Principle Award Recipient: FelipePinheiro Vilela
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (Award 2019/19338-8)
    • Principle Award Recipient: JulianaPfrimer Falcao
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001736
2023-07-18
2024-05-13
Loading full text...

Full text loading...

References

  1. World Health Organization (WHO) Salmonella (non-typhoidal); 2018 https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal) accessed 13 June 2023
  2. U.S. Center for Disease Control and Prevention (CDC) Salmonella - information for healthcare professionals and laboratories; 2022 https://www.cdc.gov/salmonella/general/technical.html accessed 13 June 2023
  3. McDermott PF, Zhao S, Tate H. Antimicrobial resistance in nontyphoidal Salmonella. Microbiol Spectr 2018; 6: [View Article] [PubMed]
     [Google Scholar]
  4. World Health Organization (WHO) Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics; 2017 https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf
  5. U.S. Center for Disease Control and Prevention (CDC) Antibiotic resistance threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019 10.15620/cdc:82532
  6. Xiong W, Sun Y, Zeng Z. Antimicrobial use and antimicrobial resistance in food animals. Environ Sci Pollut Res Int 2018; 25:18377–18384 [View Article] [PubMed]
     [Google Scholar]
  7. Brown EW, Bell R, Zhang G, Timme R, Zheng J et al. Salmonella genomics in public health and food safety. EcoSal Plus 2021; 9:eESP00082020 [View Article] [PubMed]
     [Google Scholar]
  8. U.S. Center for Disease Control and Prevention (CDC) National enteric disease surveillance: Salmonella annual report, 2016; 2018 https://www.cdc.gov/nationalsurveillance/pdfs/2016-Salmonella-report-508.pdf
  9. European Food Safety Authority (EFSA), European Center for Disease Prevention and Control (ECDC) The european union one health 2019 zoonoses report. EFSA J 2021; 19:e06406 [View Article]
     [Google Scholar]
  10. Monte DFM, Nethery MA, Barrangou R, Landgraf M, Fedorka-Cray PJ. Whole-genome sequencing analysis and CRISPR genotyping of rare antibiotic-resistant Salmonella enterica serovars isolated from food and related sources. Food Microbiol 2021; 93:103601 [View Article] [PubMed]
     [Google Scholar]
  11. Jurukov B, Simeonov C. Apropos of a case of salmonellosis caused by Salmonella mission var. isangi. Folia Med 1967; 9:157–160 [PubMed]
     [Google Scholar]
  12. Kruger T, Szabo D, Keddy KH, Deeley K, Marsh JW et al. Infections with nontyphoidal Salmonella species producing TEM-63 or a novel TEM enzyme, TEM-131, in South Africa. Antimicrob Agents Chemother 2004; 48:4263–4270 [View Article] [PubMed]
     [Google Scholar]
  13. Govinden U, Mocktar C, Moodley P, Sturm AW, Essack SY. CTX-M-37 in Salmonella enterica serotype Isangi from Durban, South Africa. Int J Antimicrob Agents 2006; 28:288–291 [View Article] [PubMed]
     [Google Scholar]
  14. Wadula J, von Gottberg A, Kilner D, de Jong G, Cohen C et al. Nosocomial outbreak of extended-spectrum beta-lactamase-producing Salmonella isangi in pediatric wards. Pediatr Infect Dis J 2006; 25:843–844 [View Article] [PubMed]
     [Google Scholar]
  15. Usha G, Chunderika M, Prashini M, Willem SA, Yusuf ES. Characterization of extended-spectrum beta-lactamases in Salmonella spp. at a tertiary hospital in Durban, South Africa. Diagn Microbiol Infect Dis 2008; 62:86–91 [View Article] [PubMed]
     [Google Scholar]
  16. Bisi-Johnson MA, Obi CL, Vasaikar SD, Baba KA, Hattori T. Molecular basis of virulence in clinical isolates of Escherichia coli and Salmonella species from a tertiary hospital in the Eastern Cape, South Africa. Gut Pathog 2011; 3:9 [View Article] [PubMed]
     [Google Scholar]
  17. Paglietti B, Falchi G, Mason P, Chitsatso O, Nair S et al. Diversity among human non-typhoidal salmonellae isolates from Zimbabwe. Trans R Soc Trop Med Hyg 2013; 107:487–492 [View Article] [PubMed]
     [Google Scholar]
  18. Suleyman G, Perri M, Vager D, Samuel L, Zervos MJ et al. Characterization of Salmonella Isangi possessing a CTX-M15 ESBL associated with an outbreak in a US Hospital. Diagn Microbiol Infect Dis 2016; 85:386–390 [View Article] [PubMed]
     [Google Scholar]
  19. Li X-P, Gao R-H, Hou P-B, Ren Y-Y, Zhang H-N et al. Characterization of the Salmonella enterica serotype Isangi isolated from patients for the first time in China. Foodborne Pathog Dis 2017; 14:427–431 [View Article] [PubMed]
     [Google Scholar]
  20. Kulkarni RD, Ajantha GS, Shubhada C, Jain P. Isolation of Salmonella enterica serotype Isangi from a suspected case of enteric encephalopathy. Indian J Med Microbiol 2009; 27:65–66 [PubMed]
     [Google Scholar]
  21. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. beta-lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 2005; 56:115–121 [View Article] [PubMed]
     [Google Scholar]
  22. Pulido-Landínez M, Sánchez-Ingunza R, Guard J, Pinheiro do Nascimento V. Assignment of serotype to Salmonella enterica isolates obtained from poultry and their environment in southern Brazil. Lett Appl Microbiol 2013; 57:288–294 [View Article] [PubMed]
     [Google Scholar]
  23. Jibril AH, Okeke IN, Dalsgaard A, Kudirkiene E, Akinlabi OC et al. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria. PLoS One 2020; 15:e0238190 [View Article] [PubMed]
     [Google Scholar]
  24. Brazilian Association of Animal Protein (ABPA) Annual report 2021; 2021 http://abpa-br.org/relatorios/ accessed 27 August 2021
  25. Vilela FP, Pribul BR, Rodrigues DDP, Balkey M, Allard M et al. Draft genome sequences of 80 Salmonella enterica serovar infantis strains isolated from food, environmental, human, and veterinary sources in Brazil. Microbiol Resour Announc 2021; 10:e0031321 [View Article] [PubMed]
     [Google Scholar]
  26. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing. In CLSI Supplement M100, 30th. edn Wayne, PA: Clinical and Laboratory Standards Institute; 2020
     [Google Scholar]
  27. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  28. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
     [Google Scholar]
  29. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article] [PubMed]
     [Google Scholar]
  30. Roer L, Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Kaas RS et al. Is the evolution of Salmonella enterica subsp. enterica linked to restriction-modification systems?. mSystems 2016; 1:e00009-16 [View Article]
     [Google Scholar]
  31. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  32. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
     [Google Scholar]
  33. Alikhan N-F, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet 2018; 14:e1007261 [View Article] [PubMed]
     [Google Scholar]
  34. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Group AS et al. The enterobase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152 [View Article]
     [Google Scholar]
  35. Salipante SJ, Hall BG. Determining the limits of the evolutionary potential of an antibiotic resistance gene. Mol Biol Evol 2003; 20:653–659 [View Article] [PubMed]
     [Google Scholar]
  36. Song S, Hwang S, Lee S, Ha N-C, Lee K. Interaction mediated by the putative tip regions of MdsA and MdsC in the formation of a Salmonella-specific tripartite efflux pump. PLoS One 2014; 9:e100881 [View Article] [PubMed]
     [Google Scholar]
  37. Vilela FP, Gomes CN, Passaglia J, Rodrigues DP, Costa RG et al. Genotypic resistance to quinolone and tetracycline in Salmonella dublin strains isolated from humans and animals in Brazil. Microb Drug Resist 2019; 25:143–151 [View Article] [PubMed]
     [Google Scholar]
  38. Fiegen U, Klein G, de Jong A, Kehrenberg C. Detection of a novel qnrB19-carrying plasmid variant mediating decreased fluoroquinolone susceptibility in Salmonella enterica serovar hadar. Microb Drug Resist 2017; 23:280–284 [View Article] [PubMed]
     [Google Scholar]
  39. Vilela FP, Falcão JP, Campioni F. Analysis of resistance gene prevalence in whole-genome sequenced Enterobacteriales from Brazil. Microb Drug Resist 2020; 26:594–604 [View Article] [PubMed]
     [Google Scholar]
  40. Hobman JL, Crossman LC. Bacterial antimicrobial metal ion resistance. J Med Microbiol 2015; 64:471–497 [View Article] [PubMed]
     [Google Scholar]
  41. Argudín MA, Hoefer A, Butaye P. Heavy metal resistance in bacteria from animals. Res Vet Sci 2019; 122:132–147 [View Article] [PubMed]
     [Google Scholar]
  42. Liu W-Q, Feng Y, Wang Y, Zou Q-H, Chen F et al. Salmonella paratyphi C: genetic divergence from Salmonella choleraesuis and pathogenic convergence with Salmonella typhi. PLoS One 2009; 4:e4510 [View Article] [PubMed]
     [Google Scholar]
  43. Rehman T, Yin L, Latif MB, Chen J, Wang K et al. Adhesive mechanism of different Salmonella fimbrial adhesins. Microb Pathog 2019; 137:103748 [View Article] [PubMed]
     [Google Scholar]
  44. Hurley D, McCusker MP, Fanning S, Martins M. Salmonella-host interactions - modulation of the host innate immune system. Front Immunol 2014; 5:481 [View Article] [PubMed]
     [Google Scholar]
  45. Wang M, Qazi IH, Wang L, Zhou G, Han H. Salmonella virulence and immune escape. Microorganisms 2020; 8:407 [View Article]
     [Google Scholar]
  46. Kingsley RA, Humphries AD, Weening EH, De Zoete MR, Winter S et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun 2003; 71:629–640 [View Article] [PubMed]
     [Google Scholar]
  47. Seribelli AA, da Silva P, Frazão MR, Kich JD, Allard MW et al. Phylogenetic relationship and genomic characterization of Salmonella typhimurium strains isolated from swine in Brazil. Infect Genet Evol 2021; 93:104977 [View Article] [PubMed]
     [Google Scholar]
  48. Haghjoo E, Galán JE. Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci U S A 2004; 101:4614–4619 [View Article] [PubMed]
     [Google Scholar]
  49. Uzzau S, Bossi L, Figueroa-Bossi N. Differential accumulation of Salmonella [Cu, Zn] superoxide dismutases SodCI and SodCII in intracellular bacteria: correlation with their relative contribution to pathogenicity. Mol Microbiol 2002; 46:147–156 [View Article] [PubMed]
     [Google Scholar]
  50. Rosselin M, Virlogeux-Payant I, Roy C, Bottreau E, Sizaret P-Y et al. Rck of Salmonella enterica, subspecies enterica serovar enteritidis, mediates zipper-like internalization. Cell Res 2010; 20:647–664 [View Article] [PubMed]
     [Google Scholar]
  51. Boyd D, Peters GA, Cloeckaert A, Boumedine KS, Chaslus-Dancla E et al. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J Bacteriol 2001; 183:5725–5732 [View Article] [PubMed]
     [Google Scholar]
  52. Bach S, de Almeida A, Carniel E. The Yersinia high-pathogenicity island is present in different members of the family Enterobacteriaceae. FEMS Microbiol Lett 2000; 183:289–294 [View Article] [PubMed]
     [Google Scholar]
  53. Gao R, Naushad S, Moineau S, Levesque R, Goodridge R et al. Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica. BMC Genomics 2020; 21:374 [View Article] [PubMed]
     [Google Scholar]
  54. Seribelli AA, da Silva P, da Cruz MF, de Almeida F, Frazão MR et al. Insights about the epidemiology of Salmonella Typhimurium isolates from different sources in Brazil using comparative genomics. Gut Pathog 2021; 13:27 [View Article] [PubMed]
     [Google Scholar]
  55. Brüssow H, Canchaya C, Hardt W-D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 2004; 68:560–602 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001736
Loading
The rare Salmonella enterica serovar Isangi: genomic characterization of the antimicrobial resistance, virulence potential and epidemiology of Brazilian strains in comparison to global isolates
J. Med. Microbiol. 72, 001736 (2023); https://doi.org/10.1099/jmm.0.001736
/content/journal/jmm/10.1099/jmm.0.001736
/content/journal/jmm/10.1099/jmm.0.001736
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error