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[en] Campylobacter jejuni is a leading cause of foodborne illnesses worldwide. Although considered fragile, this microaerophilic bacterium is able to survive in various challenging environments, which subsequently constitutes multiple sources of transmission for human infection. To test the assumption of acquiring specific features for adaption and survivals we established a workflow of phenotypic tests related to the survival and the persistence of recurrent and sporadic strains. A representative collection of 83 strains isolated over 13 years from human, mammal, poultry, and environmental sources in Luxembourg, representing different spreading patterns (endemic, epidemic, and sporadic), was screened for survival to oxidative stresses, for acclimating to aerobic conditions (AC), and for persistence on abiotic surfaces. Using the cgMLST Oxford typing scheme for WGS data, the collection was classified into genomic lineages corresponding to host-generalist strains (lineages A and D, CC ST-21), host-specific strains (lineages B, CC ST-257 and lineage C, CC ST-464) and sporadic strains. We established that when a strain survives concentrations beyond 0.25 mM superoxide stress, it is six times more likely to survive hyperoxide stress and that a highly adherent strain is 14 times more likely to develop a biofilm. Surprisingly, more than half of the strains could acclimate to AC but this capacity does not explain the difference between recurrent genomic lineages and sporadic strains and the survival to oxidative stresses, while recurrent strains have a significantly higher adhesion/biofilm formation capacity than sporadic ones. From this work, the genomic lineages with more stable genomes could be characterized by a specific combination of phenotypes, called metaphenotypes. From the functional genomic analyses, the presence of a potentially functional T6SS in the strains of lineage D might explain the propensity of these strains to be strong biofilm producers. Our findings support the hypothesis that phenotypical abilities contribute to the spatio-temporal adaptation and survival of stable genomic lineages. It suggests a selection of better-adapted and persistent strains in challenging stress environments, which could explain the prevalence of these lineages in human infections.
Disciplines :
Microbiology
Author, co-author :
NENNIG, Morgane ; University of Luxembourg > Faculty of Science, Technology and Medecine (FSTM) ; Laboratoire National de Santé > Microbiology department > Epidemiology and Microbial Genomics > Dr. ; INRAE, Nantes, France > UMR-1280 PhAN > Dr.
Clément, Arnaud; BioFilm Control, Biopôle Clermont-Limagne, Saint-Beauzire, France
Longueval, Emmanuelle; Laboratoire National de Santé > Microbiology department > Epidemiology and Microbial Genomics
Bernardi, Thierry; BioFilm Control, Biopôle Clermont-Limagne, Saint-Beauzire, France > Dr.
RAGIMBEAU, Catherine ; Laboratoire National de Santé > Microbiology department > Epidemiology and Microbial Genomics > Dr.
Tresse, Odile; INRAE, Nantes, France > UMR-1280 PhAN > Dr.
External co-authors :
yes
Language :
English
Title :
Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg
Annous B. A. Fratamico P. M. Smith J. L. (2009). Quorum sensing in biofilms: Why bacteria behave the way they do. J. Food Sci. 74 R24–R37. 10.1111/j.1750-3841.2008.01022.x 19200115
Atack J. M. Kelly D. J. (2009). Oxidative stress in Campylobacter jejuni: Responses, resistance and regulation. Future Microbiol. 4 677–690. 10.2217/fmb.09.44 19659424
Atack J. M. Harvey P. Jones M. A. Kelly D. J. (2008). The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J. Bacteriol. 190 5279–5290. 10.1128/JB.00100-08 18515414
Azeredo J. Azevedo N. F. Briandet R. Cerca N. Coenye T. Costa A. R. et al. (2017). Critical review on biofilm methods. Crit. Rev. Microbiol. 43 313–351. 10.1080/1040841X.2016.1208146 27868469
Baillon M.-L. A. van Vliet A. H. M. Ketley J. M. Constantinidou C. Penn C. W. (1999). An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181 4798–4804. 10.1128/JB.181.16.4798-4804.1999 10438747
Bayliss C. D. Bidmos F. A. Anjum A. Manchev V. T. Richards R. L. Grossier J.-P. et al. (2012). Phase variable genes of Campylobacter jejuni exhibit high mutation rates and specific mutational patterns but mutability is not the major determinant of population structure during host colonization. Nucleic Acids Res. 40 5876–5889. 10.1093/nar/gks246 22434884
Beaulaurier J. Schadt E. E. Fang G. (2019). Deciphering bacterial epigenomes using modern sequencing technologies. Nat. Rev. Genet. 20 157–172. 10.1038/s41576-018-0081-3 30546107
Boysen L. Rosenquist H. Larsson J. T. Nielsen E. M. Sørensen G. Nordentoft S. et al. (2014). Source attribution of human campylobacteriosis in Denmark. Epidemiol. Infect. 142 1599–1608. 10.1017/S0950268813002719 24168860
Bronowski C. James C. E. Winstanley C. (2014). Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol. Lett. 356 8–19. 10.1111/1574-6968.12488 24888326
Brown H. L. Reuter M. Salt L. J. Cross K. L. Betts R. P. van Vliet A. H. M. (2014). Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl. Environ. Microbiol. 80 7053–7060. 10.1128/AEM.02614-14 25192991
Bukowski M. Hyz K. Janczak M. Hydzik M. Dubin G. Wladyka B. (2017). Identification of novel mazEF/pemIK family toxin-antitoxin loci and their distribution in the Staphylococcus genus. Sci. Rep. 7:13462. 10.1038/s41598-017-13857-4 29044211
Burgess C. M. Gianotti A. Gruzdev N. Holah J. Knøchel S. Lehner A. et al. (2016). The response of foodborne pathogens to osmotic and desiccation stresses in the food chain. Int. J. Food Microbiol. 221 37–53. 10.1016/j.ijfoodmicro.2015.12.014 26803272
Calland J. K. Pascoe B. Bayliss S. C. Mourkas E. Berthenet E. Thorpe H. A. et al. (2021). Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages. PLoS Genet. 17:e1009829. 10.1371/journal.pgen.1009829 34582435
Cha W. Mosci R. Wengert S. L. Singh P. Newton D. W. Salimnia H. et al. (2016). Antimicrobial susceptibility profiles of human Campylobacter jejuni isolates and association with phylogenetic lineages. Front. Microbiol. 7:589. 10.3389/fmicb.2016.00589 27199922
Chavant P. Gaillard-Martinie B. Talon R. Hébraud M. Bernardi T. (2007). A new device for rapid evaluation of biofilm formation potential by bacteria. J. Microbiol. Methods 68 605–612. 10.1016/j.mimet.2006.11.010 17218029
Chiu S.-W. Chen S.-Y. Wong H. (2008). Localization and expression of MreB in Vibrio parahaemolyticus under different stresses. Appl. Environ. Microbiol. 74 7016–7022. 10.1128/AEM.01020-08 18820055
Clark C. G. Berry C. Walker M. Petkau A. Barker D. O. R. Guan C. et al. (2016). Genomic insights from whole genome sequencing of four clonal outbreak Campylobacter jejuni assessed within the global C. jejuni population. BMC Genomics 17:990. 10.1186/s12864-016-3340-8 27912729
Cody A. J. Bray J. E. Jolley K. A. McCarthy N. D. Maiden M. C. J. (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. 10.1128/JCM.00080-17 28446571
Cody A. J. McCarthy N. M. Wimalarathna H. L. Colles F. M. Clark L. Bowler I. C. J. W. et al. (2012). A longitudinal 6-year study of the molecular epidemiology of clinical campylobacter isolates in oxfordshire, United Kingdom. J. Clin. Microbiol. 50 3193–3201. 10.1128/JCM.01086-12 22814466
Corcionivoschi N. Gundogdu O. Moran L. Kelly C. Scates P. Stef L. et al. (2015). Virulence characteristics of hcp+ Campylobacter jejuni and Campylobacter coli isolates from retail chicken. Gut Pathog. 7:20. 10.1186/s13099-015-0067-z 26207145
Coulthurst S. (2019). The Type VI secretion system: A versatile bacterial weapon. Microbiology 165 503–515. 10.1099/mic.0.000789 30893029
Dai L. Sahin O. Tang Y. Zhang Q. (2017). A mutator phenotype promoting the emergence of spontaneous oxidative stress-resistant mutants in Campylobacter jejuni. Appl. Environ. Microbiol. 83:e01685–17. 10.1128/AEM.01685-17 29030436
Day W. A. Sajecki J. L. Pitts T. M. Joens L. A. (2000). Role of Catalase in Campylobacter jejuni Intracellular Survival. Infect. Immun. 68 6337–6345. 10.1128/iai.68.11.6337-6345.2000 11035743
Dingle K. E. Colles F. M. Wareing D. R. A. Ure R. Fox A. J. Bolton F. E. et al. (2001). Multilocus sequence typing system for Campylobacter jejuni. J. Clin. Microbiol. 39 14–23. 10.1128/JCM.39.1.14-23.2001 11136741
Donlan R. M. Costerton J. W. (2002). Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15 167–193. 10.1128/CMR.15.2.167-193.2002 11932229
Duijster J. W. Franz E. Neefjes J. J. C. Mughini-Gras L. (2019). Occupational risk of salmonellosis and campylobacteriosis: A nationwide population-based registry study. Occup. Environ. Med. 76 617–624. 10.1136/oemed-2019-105868 31413185
Elhadidy M. Ali M. M. El-Shibiny A. Miller W. G. Elkhatib W. F. Botteldoorn N. et al. (2020). Antimicrobial resistance patterns and molecular resistance markers of Campylobacter jejuni isolates from human diarrheal cases. PLoS One 15:e0227833. 10.1371/journal.pone.0227833 31951631
European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC] (2006). The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2005 | European Food Safety Authority. EFSA J. 94:288. 10.2903/j.efsa.2006.94r
European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC] (2015). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 13:4329. 10.2903/j.efsa.2015.4329
European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC] (2019a). The European Union One Health 2018 zoonoses report. EFSA J. 17:e05926. 10.2903/j.efsa.2019.5926 32626211
European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC] (2019b). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J. 17:e05598. 10.2903/j.efsa.2019.5598 32626224
European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC] (2021). The european union one health 2019 zoonoses report. EFSA J. 19:e06406. 10.2903/j.efsa.2021.6406 33680134
Faria S. I. Teixeira-Santos R. Morais J. Vasconcelos V. Mergulhão F. J. (2021). The association between initial adhesion and cyanobacterial biofilm development. FEMS Microbiol. Ecol. 97:fiab052. 10.1093/femsec/fiab052 33784393
Fisher M. T. Stadtman E. R. (1992). Oxidative modification of Escherichia coli glutamine synthetase. Decreases in the thermodynamic stability of protein structure and specific changes in the active site conformation. J. Biol. Chem. 267 1872–1880. 1346137
Fridman C. M. Keppel K. Gerlic M. Bosis E. Salomon D. (2020). A comparative genomics methodology reveals a widespread family of membrane-disrupting T6SS effectors. Nat. Commun. 11:1085. 10.1038/s41467-020-14951-4 32109231
Fux C. A. Costerton J. W. Stewart P. S. Stoodley P. (2005). Survival strategies of infectious biofilms. Trends Microbiol. 13 34–40. 10.1016/j.tim.2004.11.010 15639630
Gallique M. Decoin V. Barbey C. Rosay T. Feuilloley M. G. J. Orange N. et al. (2017). Contribution of the Pseudomonas fluorescens MFE01 Type VI Secretion System to Biofilm Formation. PLoS One 12:e0170770. 10.1371/journal.pone.0170770 28114423
Garénaux A. Guillou S. Ermel G. Wren B. Federighi M. Ritz M. (2008). Role of the Cj1371 periplasmic protein and the Cj0355c two-component regulator in the Campylobacter jejuni NCTC 11168 response to oxidative stress caused by paraquat. Res. Microbiol. 159 718–726. 10.1016/j.resmic.2008.08.001 18775777
Garénaux A. Lucchetti-Miganeh C. Barloy-Hubler F. Ermel G. Federighi M. Tresse O. et al. (2007). “Better understand the campylobacter conundrum: Parallel between campylobacter jejuni genome, sequence study and physiology,” in New Developments in Food Microbiology Research, ed. Berger M. C. (New York, NY: Nova Publishers), 1–90.
Ghatak S. Armstrong C. M. Reed S. He Y. (2020). Comparative Methylome Analysis of Campylobacter jejuni Strain YH002 Reveals a Putative Novel Motif and Diverse Epigenetic Regulations of Virulence Genes. Front. Microbiol. 11:610395. 10.3389/fmicb.2020.610395 33424813
González M. Hänninen M.-L. (2012). Effect of temperature and antimicrobial resistance on survival of Campylobacter jejuni in well water: Application of the Weibull model. J. Appl. Microbiol. 113 284–293. 10.1111/j.1365-2672.2012.05342.x 22612521
Good L. Miller W. G. Niedermeyer J. Osborne J. Siletzky R. M. Carver D. et al. (2019). Strain-specific differences in survival of campylobacter spp. In naturally contaminated turkey feces and water. Appl. Environ. Microbiol. 85:e01579–19. 10.1128/AEM.01579-19 31519663
Gorman R. Adley C. C. (2004). An evaluation of five preservation techniques and conventional freezing temperatures of –20°C and –85°C for long-term preservation of Campylobacter jejuni. Lett. Appl. Microbiol. 38 306–310. 10.1111/j.1472-765X.2004.01490.x 15214730
Grant K. A. Park S. F. (1995). Molecular characterization of katA from Campylobacter jejuni and generation of a catalase-deficient mutant of Campylobacter coli by interspecific allelic exchange. Microbiology 141 1369–1376. 10.1099/13500872-141-6-1369 7670638
Guccione E. J. Kendall J. J. Hitchcock A. Garg N. White M. A. Mulholland F. et al. (2017). Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability. Environ. Microbiol. 19 4326–4348. 10.1111/1462-2920.13930 28892295
Gunther N. W. Chen C.-Y. (2009). The biofilm forming potential of bacterial species in the genus Campylobacter. Food Microbiol. 26 44–51. 10.1016/j.fm.2008.07.012 19028304
Handley R. A. Mulholland F. Reuter M. Ramachandran V. K. Musk H. Clissold L. et al. (2015). PerR controls oxidative stress defence and aerotolerance but not motility-associated phenotypes of Campylobacter jejuni. Microbiology 161 1524–1536. 10.1099/mic.0.000109 25968890
Hanning I. Jarquin R. Slavik M. (2008). Campylobacter jejuni as a secondary colonizer of poultry biofilms. J. Appl. Microbiol. 105 1199–1208. 10.1111/j.1365-2672.2008.03853.x 18557961
Harrison J. W. Dung T. T. N. Siddiqui F. Korbrisate S. Bukhari H. Tra M. P. V. et al. (2014). Identification of possible virulence marker from campylobacter jejuni isolates. Emerg. Infect. Dis. 20 1026–1029. 10.3201/eid2006.130635 24856088
Hwang S. Kim M. Ryu S. Jeon B. (2011). Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. PLoS One 6:e22300. 10.1371/journal.pone.0022300 21811584
Hwang S. Zhang Q. Ryu S. Jeon B. (2012). Transcriptional regulation of the CmeABC multidrug efflux pump and the KatA catalase by CosR in Campylobacter jejuni. J. Bacteriol. 194 6883–6891. 10.1128/JB.01636-12 23065977
Ica T. Caner V. Istanbullu O. Nguyen H. D. Ahmed B. Call D. R. et al. (2012). Characterization of mono- and mixed-culture Campylobacter jejuni biofilms. Appl. Environ. Microbiol. 78 1033–1038. 10.1128/AEM.07364-11 22179238
Imlay J. A. (2008). Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77 755–776. 10.1146/annurev.biochem.77.061606.161055 18173371
Jana B. Fridman C. M. Bosis E. Salomon D. (2019). A modular effector with a DNase domain and a marker for T6SS substrates. Nat. Commun. 10:3595. 10.1038/s41467-019-11546-6 31399579
Jiang F. Wang X. Wang B. Chen L. Zhao Z. Waterfield N. R. et al. (2016). The pseudomonas aeruginosa type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell Rep. 16 1502–1509. 10.1016/j.celrep.2016.07.012 27477276
Jolley K. A. Bray J. E. Maiden M. C. J. (2018). Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 3:124. 10.12688/wellcomeopenres.14826.1 30345391
Joshua G. W. P. (2006). Biofilm formation in Campylobacter jejuni. Microbiology 152 387–396. 10.1099/mic.0.28358-0 16436427
Kaakoush N. O. Miller W. G. De Reuse H. Mendz G. L. (2007). Oxygen requirement and tolerance of Campylobacter jejuni. Res. Microbiol. 158 644–650. 10.1016/j.resmic.2007.07.009 17890061
Kanehisa M. Sato Y. Kawashima M. Furumichi M. Tanabe M. (2016). KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44 D457–D462. 10.1093/nar/gkv1070 26476454
Kanwal S. Noreen Z. Aalam V. Akhtar J. Masood F. Javed S. et al. (2019). Variation in antibiotic susceptibility and presence of type VI secretion system (T6SS) in Campylobacter jejuni isolates from various sources. Comp. Immunol. Microbiol. Infect. Dis. 66:101345. 10.1016/j.cimid.2019.101345 31476607
Karki A. B. Marasini D. Oakey C. K. Mar K. Fakhr M. K. (2018). Campylobacter coli from retail liver and meat products is more aerotolerant than Campylobacter jejuni. Front. Microbiol. 9:2951. 10.3389/fmicb.2018.02951 30631306
Kim J. Lee J.-Y. Lee H. Choi J. Y. Kim D. H. Wi Y. M. et al. (2017). Microbiological features and clinical impact of the type VI secretion system (T6SS) in Acinetobacter baumannii isolates causing bacteremia. Virulence 8 1378–1389. 10.1080/21505594.2017.1323164 28448786
Kim J. Park H. Kim J. Kim J. H. Jung J. I. Cho S. et al. (2019). Comparative analysis of aerotolerance, antibiotic resistance, and virulence gene prevalence in campylobacter jejuni isolates from retail raw chicken and duck meat in South Korea. Microorganisms 7:433. 10.3390/microorganisms7100433 31658662
Kim J.-S. Li J. Barnes I. H. A. Baltzegar D. A. Pajaniappan M. Cullen T. W. et al. (2008). Role of the Campylobacter jejuni Cj1461 DNA Methyltransferase in Regulating Virulence Characteristics. J. Bacteriol. 190 6524–6529. 10.1128/JB.00765-08 18689478
Kittl S. Heckel G. Korczak B. M. Kuhnert P. (2013). Source attribution of human campylobacter isolates by MLST and Fla-typing and association of genotypes with quinolone resistance. PLoS One 8:e81796. 10.1371/journal.pone.0081796 24244747
Koskella B. Brockhurst M. A. (2014). Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38 916–931. 10.1111/1574-6976.12072 24617569
Kovač J. Cadež N. Lušicky M. Nielsen E. M. Ocepek M. Raspor P. et al. (2014). The evidence for clonal spreading of quinolone resistance with a particular clonal complex of Campylobacter jejuni. Epidemiol. Infect. 142 2595–2603. 10.1017/S0950268813003245 24534165
Lee H. Lee S. Kim S. Ha J. Lee J. Choi Y. et al. (2019). The risk of aerotolerant Campylobacter jejuni strains in poultry meat distribution and storage. Microbial. Pathog. 134:103537. 10.1016/j.micpath.2019.05.020 31145980
Lertpiriyapong K. Gamazon E. R. Feng Y. Park D. S. Pang J. Botka G. et al. (2012). Campylobacter jejuni type VI secretion system: Roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. PLoS One 7:e42842. 10.1371/journal.pone.0042842 22952616
Liaw J. Hong G. Davies C. Elmi A. Sima F. Stratakos A. et al. (2019). The Campylobacter jejuni type VI secretion system enhances the oxidative stress response and host colonization. Front. Microbiol. 10:2864. 10.3389/fmicb.2019.02864 31921044
Luo N. Pereira S. Sahin O. Lin J. Huang S. Michel L. et al. (2005). Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. U.S.A. 102 541–546. 10.1073/pnas.0408966102 15634738
MacDonald E. White R. Mexia R. Bruun T. Kapperud G. Lange H. et al. (2015). Risk factors for sporadic domestically acquired campylobacter infections in norway 2010–2011: A national prospective case-control study. PLoS One 10:e0139636. 10.1371/journal.pone.0139636 26431341
Macé S. Haddad N. Zagorec M. Tresse O. (2015). Influence of measurement and control of microaerobic gaseous atmospheres in methods for Campylobacter growth studies. Food Microbiol. 52 169–176. 10.1016/j.fm.2015.07.014 26338132
Machado M. P. Halkilahti J. Jaakkonen A. Silva D. N. Mendes I. Nalbantoglu Y. et al. (2017). INNUca GitHub. Available Online at: https://github.com/B-UMMI/INNUca (accessed January 24, 2022).
Melo R. T. Grazziotin A. L. Júnior E. C. V. Prado R. R. Mendonça E. P. Monteiro G. P. et al. (2019). Evolution of Campylobacter jejuni of poultry origin in Brazil. Food Microbiol. 82 489–496. 10.1016/j.fm.2019.03.009 31027810
Montgomery M. P. Robertson S. Koski L. Salehi E. Stevenson L. M. Silver R. et al. (2018). Multidrug-resistant Campylobacter jejuni outbreak linked to puppy exposure - United States, 2016-2018. MMWR Morb. Mortal. Wkly. Rep. 67 1032–1035. 10.15585/mmwr.mm6737a3 30235182
Mou K. T. Muppirala U. K. Severin A. J. Clark T. A. Boitano M. Plummer P. J. (2015). A comparative analysis of methylome profiles of Campylobacter jejuni sheep abortion isolate and gastroenteric strains using PacBio data. Front. Microbiol. 5:782. 10.3389/fmicb.2014.00782 25642218
Mouftah S. F. Cobo-Díaz J. F. Álvarez-Ordóñez A. Mousa A. Calland J. K. Pascoe B. et al. (2021). Stress resistance associated with multi-host transmission and enhanced biofilm formation at 42 °C among hyper-aerotolerant generalist Campylobacter jejuni. Food Microbiol. 95:103706. 10.1016/j.fm.2020.103706 33397624
Mughini-Gras L. Smid J. H. Wagenaar J. A. de Boer A. G. Havelaar A. H. Friesema I. H. M. et al. (2012). Risk factors for campylobacteriosis of chicken, ruminant, and environmental origin: A combined case-control and source attribution analysis. PLoS One 7:e42599. 10.1371/journal.pone.0042599 22880049
Mughini-Gras L. Smid J. H. Wagenaar J. A. Koene M. G. J. Havelaar A. H. Friesema I. H. M. et al. (2013). Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets. Epidemiol. Infect. 141 2526–2535. 10.1017/S0950268813000356 23445833
Nennig M. Llarena A.-K. Herold M. Mossong J. Penny C. Losch S. et al. (2021). Investigating Major Recurring Campylobacter jejuni Lineages in Luxembourg Using Four Core or Whole Genome Sequencing Typing Schemes. Front. Cell. Infect. Microbiol. 10:608020. 10.3389/fcimb.2020.608020 33489938
Nguyen V. T. Fegan N. Turner M. S. Dykes G. A. (2012). Role of Attachment to Surfaces on the Prevalence and Survival of Campylobacter through Food Systems. J. Food Prot. 75 195–206. 10.4315/0362-028X.JFP-11-012 22221378
O’Kane P. M. Connerton I. F. (2017). Characterisation of aerotolerant forms of a robust chicken colonizing Campylobacter coli. Front Microbiol. 8:513. 10.3389/fmicb.2017.00513 28396658
Oh E. Jeon B. (2014). Role of alkyl hydroperoxide reductase (AhpC) in the biofilm formation of Campylobacter jejuni. PLoS One 9:e87312. 10.1371/journal.pone.0087312 24498070
Oh E. Chui L. Bae J. Li V. Ma A. Mutschall S. K. et al. (2018). Frequent implication of multistress-tolerant Campylobacter jejuni in human infections. Emerg. Infect. Dis. 24 1037–1044. 10.3201/eid2406.171587 29774830
Oh E. Kim J.-C. Jeon B. (2016). Stimulation of biofilm formation by oxidative stress in Campylobacter jejuni under aerobic conditions. Virulence 7 846–851. 10.1080/21505594.2016.1197471 27268722
Oh E. McMullen L. M. Chui L. Jeon B. (2017). Differential survival of hyper-aerotolerant Campylobacter jejuni under different gas conditions. Front. Microbiol. 8:954. 10.3389/fmicb.2017.00954 28611753
Oh E. McMullen L. Jeon B. (2015b). Impact of oxidative stress defense on bacterial survival and morphological change in Campylobacter jejuni under aerobic conditions. Front. Microbiol. 6:295. 10.3389/fmicb.2015.00295 25914692
Oh E. McMullen L. Jeon B. (2015a). High prevalence of hyper-aerotolerant Campylobacter jejuni in retail poultry with potential implication in human infection. Front. Microbiol. 6:1263. 10.3389/fmicb.2015.01263 26617597
Page R. Peti W. (2016). Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat. Chem. Biol. 12 208–214. 10.1038/nchembio.2044 26991085
Park M. Hwang S. Ryu S. Jeon B. (2021). CosR regulation of perr transcription for the control of oxidative stress defense in campylobacter jejuni. Microorganisms 9:1281. 10.3390/microorganisms9061281 34208393
Parkhill J. Wren B. W. Mungall K. Ketley J. M. Churcher C. Basham D. et al. (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403 665–668. 10.1038/35001088 10688204
Pascoe B. Méric G. Murray S. Yahara K. Mageiros L. Bowen R. et al. (2015). Enhanced biofilm formation and multi-host transmission evolve from divergent genetic backgrounds in Campylobacter jejuni. Environ. Microbiol. 17 4779–4789. 10.1111/1462-2920.13051 26373338
Pesci E. C. Cottle D. L. Pickett C. L. (1994). Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect. Immun. 62 2687–2694. 10.1128/iai.62.7.2687-2694.1994 8005660
Price L. B. Lackey L. G. Vailes R. Silbergeld E. (2007). The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environ. Health Perspect. 115 1035–1039. 10.1289/ehp.10050 17637919
Ragimbeau C. Colin S. Devaux A. Decruyenaere F. Cauchie H.-M. Losch S. et al. (2014). Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A. BMC Microbiol. 14:205. 10.1186/s12866-014-0205-7 25163418
Ravel A. Pintar K. Nesbitt A. Pollari F. (2016). Non food-related risk factors of campylobacteriosis in Canada: A matched case-control study. BMC Public Health 16:1016. 10.1186/s12889-016-3679-4 27677338
Reuter M. Mallett A. Pearson B. M. van Vliet A. H. M. (2010). Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 76 2122–2128. 10.1128/AEM.01878-09 20139307
Robinson L. Liaw J. Omole Z. Xia D. van Vliet A. H. M. Corcionivoschi N. et al. (2021). Bioinformatic analysis of the campylobacter jejuni type VI secretion system and effector prediction. Front. Microbiol. 12:694824. 10.3389/fmicb.2021.694824 34276628
Rodrigues R. C. Haddad N. Chevret D. Cappelier J.-M. Tresse O. (2016). Comparison of proteomics profiles of Campylobacter jejuni strain Bf under microaerobic and aerobic conditions. Front. Microbiol. 7:1596. 10.3389/fmicb.2016.01596 27790195
Rodrigues R. C. Pocheron A.-L. Hernould M. Haddad N. Tresse O. Cappelier J.-M. (2015). Description of Campylobacter jejuni Bf, an atypical aero-tolerant strain. Gut Pathog. 7:30. 10.1186/s13099-015-0077-x 26594244
Sana T. G. Flaugnatti N. Lugo K. A. Lam L. H. Jacobson A. Baylot V. et al. (2016). Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc. Natl. Acad. Sci. U.S.A. 113 E5044–E5051. 10.1073/pnas.1608858113 27503894
Sánchez-Romero M. A. Casadesús J. (2020). The bacterial epigenome. Nat. Rev. Microbiol. 18 7–20. 10.1038/s41579-019-0286-2 31728064
Shagieva E. Demnerova K. Michova H. (2021). Waterborne isolates of campylobacter jejuni are able to develop aerotolerance, survive exposure to low temperature, and interact with acanthamoeba polyphaga. Front. Microbiol. 12:730858. 10.3389/fmicb.2021.730858 34777280
Sheppard S. K. Cheng L. Méric G. de Haan C. P. A. Llarena A.-K. Marttinen P. et al. (2014). Cryptic ecology among host generalist Campylobacter jejuni in domestic animals. Mol. Ecol. 23 2442–2451. 10.1111/mec.12742 24689900
Silva M. Machado M. P. Silva D. N. Rossi M. Moran-Gilad J. Santos S. et al. (2018). chewBBACA: A complete suite for gene-by-gene schema creation and strain identification. Microb. Genom. 4:e000166. 10.1099/mgen.0.000166 29543149
Snider J. Thibault G. Houry W. A. (2008). The AAA+ superfamily of functionally diverse proteins. Genome Biol. 9:216. 10.1186/gb-2008-9-4-216 18466635
Stahl M. Butcher J. Stintzi A. (2012). Nutrient acquisition and metabolism by Campylobacter jejuni. Front. Cell Infect. Microbiol. 2:5. 10.3389/fcimb.2012.00005 22919597
Sulaeman S. Bihan G. L. Rossero A. Federighi M. Dé E. Tresse O. (2010). Comparison between the biofilm initiation of Campylobacter jejuni and Campylobacter coli strains to an inert surface using BioFilm Ring Test®. J. Appl. Microbiol. 108 1303–1312. 10.1111/j.1365-2672.2009.04534.x 19796124
Sulaeman S. Hernould M. Schaumann A. Coquet L. Bolla J.-M. Dé E. et al. (2012). Enhanced adhesion of Campylobacter jejuni to abiotic surfaces is mediated by membrane proteins in oxygen-enriched conditions. PLoS One 7:e46402. 10.1371/journal.pone.0046402 23029510
Svensson S. L. Pryjma M. Gaynor E. C. (2014). Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of campylobacter jejuni. PLoS One 9:e106063. 10.1371/journal.pone.0106063 25166748
Teh A. H. T. Lee S. M. Dykes G. A. (2019). Association of some Campylobacter jejuni with Pseudomonas aeruginosa biofilms increases attachment under conditions mimicking those in the environment. PLoS One 14:e0215275. 10.1371/journal.pone.0215275 30970009
The UniProt Consortium (2021). UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Res. 49 D480–D489. 10.1093/nar/gkaa1100 33237286
Tresse O. Shannon K. Pinon A. Malle P. Vialette M. Midelet-Bourdin G. (2007). Variable adhesion of Listeria monocytogenes isolates from food-processing facilities and clinical cases to inert surfaces. J. Food Prot. 70 1569–1578. 10.4315/0362-028x-70.7.1569 17685327
Turonova H. Briandet R. Rodrigues R. Hernould M. Hayek N. Stintzi A. et al. (2015). Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: Comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions. Front. Microbiol. 6:709. 10.3389/fmicb.2015.00709 26217332
Turonova H. Neu T. R. Ulbrich P. Pazlarova J. Tresse O. (2016). The biofilm matrix of Campylobacter jejuni determined by fluorescence lectin-binding analysis. Biofouling 32 597–608. 10.1080/08927014.2016.1169402 27097059
Vallenet D. Calteau A. Cruveiller S. Gachet M. Lajus A. Josso A. et al. (2017). MicroScope in 2017: An expanding and evolving integrated resource for community expertise of microbial genomes. Nucleic Acids Res. 45 D517–D528. 10.1093/nar/gkw1101 27899624
Vallenet D. Calteau A. Dubois M. Amours P. Bazin A. Beuvin M. et al. (2020). MicroScope: An integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res. 48 D579–D589. 10.1093/nar/gkz926 31647104
Vegge C. S. Jansen van Rensburg M. J. Rasmussen J. J. Maiden M. C. J. Johnsen L. G. Danielsen M. et al. (2016). Glucose metabolism via the entner-doudoroff pathway in campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates. Front. Microbiol. 7:1877. 10.3389/fmicb.2016.01877 27920773
Vegosen L. Breysse P. N. Agnew J. Gray G. C. Nachamkin I. Sheikh K. et al. (2015). Occupational exposure to swine, poultry, and cattle and antibody biomarkers of campylobacter jejuni exposure and autoimmune peripheral neuropathy. PLoS One 10:e0143587. 10.1371/journal.pone.0143587 26636679
Wimalarathna H. M. Richardson J. F. Lawson A. J. Elson R. Meldrum R. Little C. L. et al. (2013). Widespread acquisition of antimicrobial resistance among Campylobacter isolates from UK retail poultry and evidence for clonal expansion of resistant lineages. BMC Microbiol. 13:160. 10.1186/1471-2180-13-160 23855904
Wood T. E. Aksoy E. Hachani A. (2020). From welfare to warfare: The arbitration of host-microbiota interplay by the type VI secretion system. Front. Cell. Infect. Microbiol. 10:587948. 10.3389/fcimb.2020.587948 33194832
World Health Organization [WHO] (2013). The Global View Of Campylobacteriosis. Geneva: World Health Organization.
Yahara K. Méric G. Taylor A. J. de Vries S. P. W. Murray S. Pascoe B. et al. (2017). Genome-wide association of functional traits linked with Campylobacter jejuni survival from farm to fork. Environ. Microbiol. 19 361–380. 10.1111/1462-2920.13628 27883255
Yamasaki M. Igimi S. Katayama Y. Yamamoto S. Amano F. (2004). Identification of an oxidative stress-sensitive protein from Campylobacter jejuni, homologous to rubredoxin oxidoreductase/rubrerythrin. FEMS Microbiol. Lett. 235 57–63. 10.1016/j.femsle.2004.04.012 15158262
Yan X. Gurtler J. B. Fratamico P. M. Hu J. Juneja V. K. (2012). Phylogenetic identification of bacterial MazF toxin protein motifs among probiotic strains and foodborne pathogens and potential implications of engineered probiotic intervention in food. Cell Biosci. 2:39. 10.1186/2045-3701-2-39 23186337
Yao H. Shen Z. Wang Y. Deng F. Liu D. Naren G. et al. (2016). Emergence of a potent multidrug efflux pump variant that enhances campylobacter resistance to multiple antibiotics. mBio 7:e01543–16. 10.1128/mBio.01543-16 27651364
Zoued A. Brunet Y. R. Durand E. Aschtgen M.-S. Logger L. Douzi B. et al. (2014). Architecture and assembly of the Type VI secretion system. Biochim. Biophys. Acta 1843 1664–1673. 10.1016/j.bbamcr.2014.03.018 24681160