Skip to main content

Advertisement

SpringerLink
Log in

Insights on the genomic diversity, virulence and resistance profile of a Campylobacter jejuni strain isolated from a hospitalized patient in Brazil

  • Clinical Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Campylobacteriosis is currently recognized as one of the major causes of foodborne bacterial diseases worldwide. In Brazil, there is insufficient data to estimate the impact of Campylobacter in public health. The aim of this present study was to characterize a C. jejuni CJ-HBSJRP strain isolated from a hospitalized patient in Brazil by its ability to invade human Caco-2 epithelial cells, to survive in U937 human macrophages, and to assess its phenotypic antimicrobial resistance profile. In addition, prophages, virulence and antimicrobial resistance genes were search using whole-genome sequencing data. The genetic relatedness was evaluated by MLST and cgMLST analysis by comparison with 29 other C. jejuni genomes isolated from several countries. The CJ-HBSJRP strain showed an invasion percentage of 50% in Caco-2 polarized cells, 37.5% of survivability in U937 cells and was phenotypically resistant to ampicillin, ciprofloxacin and nalidixic acid. A total of 94 virulence genes related to adherence, biofilm, chemotaxis, immune modulation, invasion process, metabolism, motility and toxin were detected. The resistance genes blaOXA-605 (blaOXA-61), cmeB and mutations in the QRDR region of gyrA were also found and none prophages were detected. The MLST analysis showed 23 different STs among the strains studied. Regarding cgMLST analysis, the CJ-HBSJRP strain was genetically distinct and did not group closely to any other isolate. The results obtained reinforce the pathogenic potential of the CJHBSJRP strain and highlighted the need for more careful attention to Campylobacter spp. infections in Brazil since this pathogen has been the most commonly reported zoonosis in several countries worldwide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

CJ-HBSJRP was assigned the BioSample accession SAMN16129301 at the website: https://www.ncbi.nlm.nih.gov/biosample/?term=SAMN16129301.

References

  1. ABPA e Associação Brasileira de Proteína Animal (2022) Annual Report https://abpa-br.org/wp-content/uploads/2022/05/Relatorio-Anual-ABPA-2022-1.pdf. Accessed 9 Jan 2022

  2. Agarwala R, Barrett T, Beck J, Benson DA et al (2016) Database resources of the national center for biotechnology information. Nucl Acids Res 44:D7–D19

    Article  CAS  Google Scholar 

  3. Arndt D, Grant JR, Marcu A et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44(W1):W16-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Alcock BP, Raphenya AR, Lau TTY et al (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48:D517–D525

    CAS  PubMed  Google Scholar 

  5. Babakhani FK, Bradley GA, Joens LA (1993) Newborn piglet model for campylobacteriosis. Infect Immun 61:3466–3475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Backert S, Hofreuter D (2013) Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen Campylobacter jejuni. J Microbiol Methods 95(1):8–23

    Article  CAS  PubMed  Google Scholar 

  7. Birk T, Wik MT, Lametsch R, Knochel S (2012) Acid stress response and protein induction in Campylobacter jejuni isolates with different acid tolerance. BMC Microbiol 12:13

    Article  Google Scholar 

  8. Biswas D, Hannon SJ, Townsend HGG, Potter A, Allan BJ (2011) Genes coding for virulence determinants of Campylobacter jejuni in human clinical and cattle isolates from Alberta, Canada, and their potential role in colonization of poultry. Int Microbiol 14:25–32

    CAS  PubMed  Google Scholar 

  9. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ (1988) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157:472–479

    Article  CAS  PubMed  Google Scholar 

  10. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naitali M, Briandet R (2015) Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45:167–178

    Article  CAS  PubMed  Google Scholar 

  11. Campioni F, Falcão JP (2014) Genotypic diversity and virulence markers of Yersinia enterocolitica biotype 1A strains isolated from clinical and non-clinical origins. APMIS 122:215–222

    Article  CAS  PubMed  Google Scholar 

  12. Cantero G, Correa-Fiz F, Ronco T, Strube M, Cerdà-Cuéllar M, Pedersen K (2018) Characterization of Campylobacter jejuni and Campylobacter coli Broiler Isolates by Whole-Genome Sequencing. Foodborne Pathog Dis 15:145–152

    Article  CAS  PubMed  Google Scholar 

  13. Center for Disease Control and Prevention (CDC) (2019) Antibiotic resistance threats in the united states. Atlanta, GA: U.S. Department of Health and Human Services

  14. Center for Disease Control and Prevention (CDC) (2021) Foodborne diseases active surveillance network (FoodNet): FoodNet Surveillance Report for 2021. U.S. Department of Health and Human Services, Atlanta, GA.

  15. Chen L et al (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:325–328

    Article  Google Scholar 

  16. Clausen PTLC, Aarestrup FM, Lund O (2018) Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics 19(1):307

    Article  PubMed  PubMed Central  Google Scholar 

  17. Clinical and Laboratory Standards Institute (CLSI) (2016) Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. 3rd ed. CLSI guideline M45. CLSI, Wayne, PA

  18. Clinical and Laboratory Standards Institute (CLSI) (2022) Performance standards for antimicrobial susceptibility testing. 32st ed. CLSI supplement M100. Clinical and Laboratory Standards Institute

  19. Coker AO, Isokpehi RD, Thomas BN, Amisu KO, Obi CL (2002) Human campylobacteriosis in developing countries. Emerg Infect Dis 8:237–243

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cody AJ, Bray JE, Jolley KA, Mccarthy ND, Maiden MCJ (2017) Core genome Multilocus sequence typing scheme for stable, comparative analyses of Campylobacter jejuni and C. coli human disease isolates. J Clin Microbiol 55:2086–2097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Connerton IF, Connerton PL (2017) Chapter 8 - Campylobacter Foodborne Disease. In: Dodd CER, Aldsworth T, Stein RA, Cliver DO, Riemann HP (eds) Foodborne Diseases, 3rd edn. Academic Press, pp 209–221

    Chapter  Google Scholar 

  22. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJ, Urwin R, Maiden MC (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39(1):14–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Emanowicz M, Meade J, Burgess C, Bolton D, Egan J, Lynch H et al (2022) Antimicrobial resistance and genomic diversity of Campylobacter jejuni isolates from broiler caeca and neck skin samples collected at key stages during processing. Food Control 135:108664

    Article  CAS  Google Scholar 

  24. Epps SV, Harvey RB, Hume ME, Phillips TD, Anderson RC, Nisbet DJ (2013) Foodborne Campylobacter: Infections, metabolism, pathogenesis and reservoirs. Int J Environ Res Public Health 10:6292–6304

    Article  PubMed  PubMed Central  Google Scholar 

  25. Everest PH, Goossens H, Butzler JP, Lloyd D, Knutton S, Ketley JM, Williams PH (1992) Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol 37:319–332

    Article  CAS  PubMed  Google Scholar 

  26. Ewers EC, Anisowicz SK, Ferguson TM et al (2018) Antibiotic resistance, molecular characterizations, and clinical manifestations of Campylobacteriosis at a military medical center in Hawaii from 2012–2016: a retrospective analysis. Sci Rep 8:11736

    Article  PubMed  PubMed Central  Google Scholar 

  27. European Food Safety Authority and European Centre for Disease Prevention and Control (2022) The european union one health 2021 Zoonoses Report. EFSA J 20(12):7666

    Google Scholar 

  28. Frazão MR, Cao G, Medeiros MIC, Duque SS, Allard MW, Falcão JP (2021) Antimicrobial Resistance Profiles and Phylogenetic Analysis of Campylobacter jejuni Strains Isolated in Brazil by Whole Genome Sequencing. Microb Drug Resist 27:(5)660–669

  29. Gomes CN, Frazão MR, Passaglia J, Duque SS, Medeiros MIC, Falcão JP (2019) Molecular epidemiology and resistance profile of Campylobacter jejuni and C. coli strains isolated from different sources in Brazil. Microb Drug Resist 00:1–10

    Google Scholar 

  30. Gomes CN, Barker DOR, Duque SS, Che EV, Jayamanna V, Taboada EN, Falcão JP (2021a) Campylobacter coli isolated in Brazil typed by core genome Multilocus Sequence Typing shows high genomic diversity in a global context. Infect Genet Evol 95:105018

    Article  CAS  PubMed  Google Scholar 

  31. Gomes CN, Campioni F, Vilela FP, Duque SS, Falcão JP (2021b) Campylobacter coli strains from Brazil can invade phagocytic and epithelial cells and induce IL-8 secretion. Braz J Microbiol 52:859–867

  32. Gomes CN, Campioni F, Barker DOR, Che EV, Duque SS, Taboada EN, Falcão JP (2023) Antimicrobial resistance genotypes and phenotypes of Campylobacter coli isolated from different sources over a 16-year period in Brazil. J Glob Antimicrob Resist 33:109–113

    Article  CAS  PubMed  Google Scholar 

  33. Griggs DJ, Peake L, Johnson MM, Mott SGA, Piddock LJV (2009) β-Lactamase-Mediated β-Lactam Resistance in Campylobacter Species: Prevalence of Cj0299 (blaOXA-61) and Evidence for a Novel β-Lactamase. In: Jejuni C Antimicrob Agents Chemother 53(8):3357–3364

  34. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L et al (2014) ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58(1):212–220

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hickey TE, McVeigh AL, Scott DA, Michielutti RE, Bixby A, Carroll SA, Bourgeois AL, Guerry P (2000) Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect Immun 68:6535e6541

    Article  Google Scholar 

  36. Hu L, Kopecko DJ (2000) Interactions of Campylobacter with eukaryotic cells: gut luminal colonization and mucosal invasion mechanisms. In: Nachamkin I, Blaser MJ (eds) Campylobacter, 2nd edn. American Society of Microbiology, Washington, DC, pp 191–215

    Google Scholar 

  37. Jolley KA, Maiden MCJ (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kilmartin D, Morris D, O’Hare C, Corbett-Feeney G, Cormican M (2005) Clonal expansion may account for high levels of quinolone resistance in Salmonella enterica serovar enteritidis. Appl Environ Microbiol 71:2587–2591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lakin SM, Dean C, Noyes NR, Dettenwanger A, Ross AS, Doster E et al (2017) MEGARes: an antimicrobial resistance database for high throughput sequencing. Nucl Acids Res 45:D574–D580

    Article  CAS  PubMed  Google Scholar 

  40. Liu YY, Chiou CS, Chen CC (2016) PGAdb-builder: a web service tool for creating pan-genome allele database for molecular fine typing. Sci Rep 6:36213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Llarena A-K, Taboada E, Rossi M (2017) Whole-genome sequencing in epidemiology of Campylobacter jejuni. Infections J Clin Microbiol 55:1269–1275

    PubMed  Google Scholar 

  42. Luo N, Sahin O, Lin J, Michel LO, Zhang Q (2003) In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrob Agents Chemother 47(1):390–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Man SM (2011) The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 8:669e685

    Article  Google Scholar 

  44. Man SM, Kaakoush NO, Leach ST, Nahidi L, Lu HK, Norman J, Day AS, Zhang L, Mitchell HM (2010) Host attachment, invasion, and stimulation of proinflammatory cytokines by Campylobacter concisus and other non-Campylobacter jejuni Campylobacter species. J Infect Dis 202:1855–1865

    Article  CAS  PubMed  Google Scholar 

  45. McArthur AG, Waglechner N, Nizam FY et al (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Marotta F, Garofolo G, di Marcantonio L, Di Serafino G, Neri D, Romantini R et al (2019) Antimicrobial resistance genotypes and phenotypes of Campylobacter jejuni isolated in Italy from humans, birds from wild and urban habitats, and poultry. PLoS ONE 14(10):e0223804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Redondo N, Carroll A, Namara EMC (2019) Molecular characterization of Campylobacter causing human clinical infection using whole-genome sequencing: virulence, antimicrobial resistance and phylogeny in Ireland. PloS One 14:88–219

    Article  Google Scholar 

  48. Rozynek E, Dzierzanowska-Fangrat K, Jozwiak P, Popowski J, Korsak D, Dzierzanowska D (2005) Prevalence of potential virulence markers in Polish Campylobacter jejuni and Campylobacter coli isolates obtained from hospitalized children and from chicken carcasses. J Med Microbiol 54:615e619

    Article  Google Scholar 

  49. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinform Appl Note 30:2068–2069

    CAS  Google Scholar 

  50. Siddiqee MH, Henry R, Coleman RA, Deletic A, McCarthy DT (2019) Campylobacter in an Urban Estuary: Public Health Insights from Occurrence, HeLa Cytotoxicity, and Caco-2 Attachment Cum Invasion. Microbes Environ 27 34(4):436–445

    Article  Google Scholar 

  51. Signorini ML and Flores-Luna J (2010) Contamination of poultry products. Handbook of Poultry Science and Technology, New Jersey: John Wiley & Sons, Inc. 2:463–493

  52. Silva J, Leite D, Fernandes M, Mena C, Gibbs PA (2011) Campylobacter spp. as a foodborne pathogen: a review. Front Microbiol 2:1–12

    Article  Google Scholar 

  53. Skarp CPA, Hänninen ML, Rautelin HIK (2016) Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 22(2):103–109

    Article  CAS  PubMed  Google Scholar 

  54. Sopwith W, Birtles A, Matthews M, Fox A, Gee S, Painter M, Regan M, Syed Q, Bolton E (2006) Campylobacter jejuni multilocus sequence types in humans, northwest England, 2003–2004. Emerg Infect Dis 12:1500–1507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Strahilevitz J, Jacoby GA, Hopper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22:664–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Su M, Satola SW, Read TD (2019) Genome-based prediction of bacterial antibiotic resistance. J Clin Microbiol 57:e01405-e1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Young KT, Davis LM, Dirita VJ (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5:665–679

    Article  CAS  PubMed  Google Scholar 

  58. Westerman TL, Bogomolnaya L, Andrews-Polymenis HL, Sheats MK, Elfenbein JR (2018) The Salmonella type-3 secretion system-1 and flagellar motility influence the neutrophil respiratory burst. PLoS ONE 13(9):e0203698

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wieczorek K, Wolkowicz T, Osek J (2018) Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front Microbiol 9:1508

    Article  PubMed  PubMed Central  Google Scholar 

  60. Würfel SFR, Jorge S, Oliveira NR, Kremer FS, Sanchez CD, Campos VF, Pinto LS, da Silva WP, Dellagostin OA (2020) Campylobacter jejuni isolated from poultry meat in Brazil: in silico analysis and genomic features of two strains with different phenotypes of antimicrobial susceptibility. Mol Biol Rep 47:671–681

    Article  Google Scholar 

  61. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O et al (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67(11):2640–2644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C, Francisco AP, Carrico JA, Achtman M (2018) GrapeTree: Visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 28:1395–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The study was supported by the Public Health Agency of Canada research under the supervision of Dr. Eduardo N. Taboada and by Sao Paulo Research Foundation—FAPESP (Proc. 2019/19338-8 and Proc. 2022/07013-0) under Dr. Juliana P. Falcao supervision. During the course of this work, Dr. Carolina N. Gomes was supported by FAPESP (Proc. 2015/23408-0 and Proc. 2018/26043-1). Falcão, J.P. received a productive fellowship from Council for Scientific and Technological Development (CNPq: Proc.304399/2018-3 and 304803/2021-9).

Author information

Authors and Affiliations

  1. Departamento de Análises Clínicas, Toxicológicas E Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto- Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil

    Carolina Nogueira Gomes, Miliane Rodrigues Frazão & Juliana Pfrimer Falcão

  2. Laboratório de Patogenicidade Microbiana E Imunidade Inata, Faculdade de Medicina de Ribeirão Preto- Universidade de São Paulo, São Paulo, Brazil

    Amanda Aparecida Seribelli

  3. National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, MB, Canada

    Dillon Oliver Reese Barker, Emily Victoria Che & Eduardo Napoleon Taboada

  4. Centro de Investigação de Microrganismos, Departamento de Doenças Dermatológicas, Infecciosas E Parasitárias- Faculdade de Medicina de São José Do Rio Preto, São José Do Rio Preto, São Paulo, Brazil

    Mara Corrêa Lelles Nogueira

Authors
  1. Carolina Nogueira Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miliane Rodrigues Frazão
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amanda Aparecida Seribelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dillon Oliver Reese Barker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emily Victoria Che
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mara Corrêa Lelles Nogueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eduardo Napoleon Taboada
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Juliana Pfrimer Falcão
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CNG: conceptualization, formal analysis, investigation, data curation, writing—original draft, preparation, and visualization. MRF: formal analysis, investigation. AAS: formal analysis, investigation. DORB: formal analysis, investigation, writing—review and editing. EVC: formal analysis, investigation, writing—review and editing. MCLN: resources, data curation. ENT: supervision, project administration, and funding. JPF: resources, writing—review and editing, supervision, project administration, and funding.

Corresponding author

Correspondence to Juliana Pfrimer Falcão.

Ethics declarations

Conflicts of interest

Author Juliana Pfrimer Falcao is an Associate Editor for Brazilian Journal of Microbiology and the peer-review process for this article was independently handled by another member of the journal editorial board.

Additional information

Responsible Editor: Roxane M Piazza

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomes, C.N., Frazão, M.R., Seribelli, A.A. et al. Insights on the genomic diversity, virulence and resistance profile of a Campylobacter jejuni strain isolated from a hospitalized patient in Brazil. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01314-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s42770-024-01314-0

Keywords

Search

Navigation