Publication history:  Accepted - 3 June 2021;  Published online - 8 June 2021

Corcionivoschi, Nicolae

Gundogdu, Ozan

Microorganisms

Campylobacter is the most common bacterial cause of human gastroenteritis in the world, with the species Campylobacter jejuni being responsible for over 80% of Campylobacter infections [...]

LSHTM Research Online

microorganismsEditorialFoodborne Pathogen CampylobacterNicolae Corcionivoschi 1 and Ozan Gundogdu 2,*Citation: Corcionivoschi, N.;Gundogdu, O. Foodborne PathogenCampylobacter. Microorganisms 2021,9, 1241. https://doi.org/10.3390/microorganisms9061241Received: 24 May 2021Accepted: 3 June 2021Published: 8 June 2021Publisher’s Note: MDPI stays neutralwith regard to jurisdictional claims inpublished maps and institutional affil-iations.Copyright: © 2021 by the authors.Licensee MDPI, Basel, Switzerland.This article is an open access articledistributed under the terms andconditions of the Creative CommonsAttribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).1 Bacteriology Branch, Veterinary Sciences Division, Agri-Food and Biosciences Institute, Newforge Lane,Belfast BT9 5GB, UK; nicolae.corcionivoschi@afbini.gov.uk2 Department of Infection Biology, Faculty of Infectious & Tropical Diseases, London School of Hygiene &Tropical Medicine, Keppel Street, London WC1E 7HT, UK* Correspondence: Ozan.Gundogdu@lshtm.ac.ukCampylobacter is the most common bacterial cause of human gastroenteritis in theworld, with the species Campylobacter jejuni being responsible for over 80% of Campylobacterinfections [1]. C. jejuni is abundant within the avian gut and the consumption and han-dling of poultry is the main route of transmission to humans [2,3]. In humans, C. jejuniinfection ranges from asymptomatic carriage to bloody diarrhoea, fever and abdominalpains as well as serious post-infectious sequelae such as the neuromuscular paralysis ofGuillain–Barré syndrome [4]. In low-resource areas, Campylobacter infections are commonin young children (causing watery diarrhoea rather than the bloody diarrhoea that occursin high-resource countries) and are associated with many deaths, as well as stunted growthand life-long physical and cognitive deficiencies [5]. In addition, as highlighted by theWHO, C. jejuni is a multi-antibiotic-resistant pathogen and new therapeutics are urgentlyrequired [6].Historically, the lack of a convenient animal model, coupled with genetic diversity anddifficulties in culturing C. jejuni, has hampered pathogenesis research [7]. For this reason,it is important that the Campylobacter research community continues to investigate thisimportant human pathogen. This Special Issue was produced with the aim of promotingthe latest research on Campylobacter pathogenicity focusing on a range of topics fromvirulence determinants such as lipooligosaccharide (LOS) to functional characterisationof specific genes of interest. The Special Issue aims to look at novel infection models,immunological responses of Campylobacter infection and epidemiological studies with theoverarching aim of intervention and control strategies. Survival themes such as biofilms,antimicrobial resistance and omics-based topics such as the microbiome also form a keypart of the Special Issue. Overall, this Microorganisms Special Issue highlights some of themost up-to-date research relating to Campylobacter pathogenicity.Our aim to further understand the pathogenicity and physiology of Campylobacter hasbeen pursued by a number of research groups. Kovács et al. [8] investigate the virulencetraits of inpatient C. jejuni isolates and apply a transcriptomic approach to identify potentialgenes maintaining a role in intracellular survival. Characteristic groups of genes wereidentified as significantly upregulated, outlining a survival strategy of internalised C. jejuni,comprising genes related (1) to oxidative stress; (2) to a protective sheath formed by thecapsule, LOS, N-, and O-glycosylation systems; (3) to dynamic metabolic activity sup-ported by different translocases and the membrane-integrated component of the flagellarapparatus; and (4) to hitherto unknown genes. Talukdar et al. [9] investigate C. jejuni CadFand FlpA virulence proteins in binding to host cell fibronectin. The authors demonstratethat the C. jejuni CadF and FlpA adhesins facilitate the binding of C. jejuni to the hostcells, permit delivery of effector proteins into the cytosol of a host target cell and aid in therewiring of host cell signalling pathways to alter host cell behaviour. Guirado et al. [10]discuss the differential distribution of the wlaN and cgtB genes, which are associated withGuillain–Barré Syndrome in C. jejuni isolates from humans, broiler chickens and wildbirds. The authors detect two variants of a G-rich region within the cgtB gene, suggestingMicroorganisms 2021, 9, 1241. https://doi.org/10.3390/microorganisms9061241 https://www.mdpi.com/journal/microorganismsMicroorganisms 2021, 9, 1241 2 of 4that, similarly to wlaN, the G-tract in the cgtB gene mediates the phase variation control ofcgtB expression. Guk et al. [11] investigate hyper-aerotolerant C. coli from duck sourcesand their increased potential of virulence, antimicrobial resistance and genetic relatedness.Recently, aerotolerant (AT) C. jejuni with the ability to survive under aerobic stress hasbeen reported. The authors investigate the prevalence of hyper-aerotolerant (HAT) C. colifrom duck sources with these strains most likely being transmitted to humans through thefood chain given their aerotolerance.A number of research articles investigate infection models and/or immunological as-pects of C. jejuni infection. Kløve et al. [12] show that the immunopathological sequelae in C.jejuni-infected mice were due to Toll-like receptor 4 (TLR4)-dependent immune responsesinduced by bacterial LOS. Here, the authors further investigate and identify TLR4 involvedin mediating C. coli LOS-induced immune responses in intestinal and extra-intestinal com-partments during murine campylobacteriosis. Heimesaat et al. [13] investigate the use ofthe polyphenolic compound resveratrol to alleviate acute C. jejuni-induced enterocolitis in apreclinical intervention study. Functional analyses revealed that resveratrol treatment couldeffectively rescue colonic epithelial barrier function in C. jejuni-infected mice. The authorsdescribe that peroral resveratrol treatment does exert potent disease-alleviating effectsduring acute experimental campylobacteriosis. Heimesaat et al. [14] also investigate theimmune-modulatory properties of the octapeptide NAP in C. jejuni-infected mice sufferingfrom acute enterocolitis. The authors discuss how they used an acute C. jejuni induced ente-rocolitis model, and they surveyed the anti-pathogenic and immune-modulatory effects ofthe octapeptide NAP, which is well-known for its neuroprotective and anti-inflammatoryproperties. NAP treatment resulted in less distinct innate and adaptive pro-inflammatoryimmune responses that were not restricted to the intestinal tract but could also be observedin extra-intestinal and even systemic compartments. NAP treatment further resulted inless frequent translocation of viable pathogens from the intestinal tract to extra-intestinalareas including systemic tissue sites.In conjunction with basic laboratory research, applied research is important for us toinvestigate Campylobacter in the real world. Rapp et al. [15] study the importance of the farmenvironment and wildlife for transmission of C. jejuni, specifically in a pasture-based dairyherd. The results indicate that management of grazed pasture and supplementary feed con-taminated by bird droppings could be targeted to effectively reduce transmission of C. jejunito dairy herds, the farm environment and, ultimately, to humans. Šimunović et al. [16]compare C. jejuni from slaughterhouse and surface-water isolates, indicating the betteradaptation of the former to the chicken host environment. The authors highlight adapta-tion of C. jejuni slaughterhouse isolates to the chicken host, as well as increased biofilmcell resistance due to increased efflux pump activity. Di Donato et al. [17] investigate theprevalence, population diversity and antimicrobial resistance of C. coli isolated in Italianswine at slaughterhouses. The authors identify a strong correlation between phenotypicand genotypic resistance to fluoroquinolone and tetracycline. Liang et al. [18] investigatethe development of a lyophilisation process for Campylobacter bacteriophage storage andtransport. In this study, the authors describe the development of a lyophilisation ap-proach to maintain phage titers, ensure efficacy and reduce transport costs of Campylobacterbacteriophages.As with all modern science, the use of in silico bioinformatics approaches to studyrelevant research questions goes hand in hand with laboratory science. Bandoy andWeimer [19] use machine learning combined with Campylobacter population genomics toreveal virulence gene allelic variants that cause disease. The authors validated a novelframework to define infection mechanism using a combination of a GWAS, machinelearning and bacterial population genomics that ranked allelic variants to identify disease.The Special Issue also provides three reviews. Pumtang-on et al. [20] perform asystematic review of C. jejuni vaccine candidates for chickens, highlighting the need forincreased consistency in the way C. jejuni vaccine studies in poultry are designed andreported in order to be able to undertake a robust comparison of C. jejuni vaccine candidates.Microorganisms 2021, 9, 1241 3 of 4Mousavi et al. [21] discuss a novel clinical C. jejuni infection model based on sensitisationof mice to LOS. The review highlights the major role of LOS-driven innate immunity inpathogenesis of campylobacteriosis, including post-infectious autoimmune diseases, andpromote the preclinical evaluation of novel pharmaceutical strategies for prophylaxis andtreatment. Tram et al. [22] discuss C. jejuni and biofilms. This review examines factors thatcan trigger biofilm formation and is a timely reminder of the importance of biofilms inrelation to C. jejuni survival.This Special Issue highlights the latest developments within Campylobacter research,particularly those relating to pathogenicity.Conflicts of Interest: The authors declare no conflict of interest.References1. Gundogdu, O.; Wren, B.W. Microbe Profile: Campylobacter jejuni—Survival instincts. Microbiology 2020, 166, 230–232. [CrossRef]2. Ijaz, U.Z.; Sivaloganathan, L.; McKenna, A.; Richmond, A.; Kelly, C.; Linton, M.; Stratakos, A.C.; Lavery, U.; Elmi, A.;Wren, B.W.; et al. Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competi-tive to Environmental Drivers and a Window of Opportunity for Campylobacter. Front. Microbiol. 2018, 9, 2452. [CrossRef][PubMed]3. McKenna, A.; Ijaz, U.Z.; Kelly, C.; Linton, M.; Sloan, W.T.; Green, B.D.; Lavery, U.; Dorrell, N.; Wren, B.W.; Richmond, A.; et al.Impact of industrial production system parameters on chicken microbiomes: Mechanisms to improve performance and reduceCampylobacter. Microbiome 2020, 8, 1–13. [CrossRef] [PubMed]4. Young, K.T.; Davis, L.M.; DiRita, V.J. Campylobacter jejuni: Molecular biology and pathogenesis. Nat. Rev. Genet. 2007, 5, 665–679.[CrossRef] [PubMed]5. Amour, C.; Gratz, J.; Mduma, E.R.; Svensen, E.; Rogawski, E.T.; McGrath, M.; Seidman, J.C.; McCormick, B.J.J.; Shrestha, P.S.;Samie, A.; et al. Epidemiology and Impact ofCampylobacterInfection in Children in 8 Low-Resource Settings: Results From theMAL-ED Study. Clin. Infect. Dis. 2016, 63, 1171–1179. [CrossRef]6. WHO. Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, And Development of New Antibiotics; WHO:Geneva, Switzerland, 27 February 2017.7. Gundogdu, O.; Da Silva, D.T.; Mohammad, B.; Elmi, A.; Wren, B.W.; van Vliet, A.; Dorrell, N. The Campylobacter jejuni OxidativeStress Regulator RrpB Is Associated with a Genomic Hypervariable Region and Altered Oxidative Stress Resistance. Front.Microbiol. 2016, 7, 2117. [CrossRef]8. Kovács, J.K.; Cox, A.; Schweitzer, B.; Maróti, G.; Kovács, T.; Fenyvesi, H.; Emődy, L.; Schneider, G. Virulence Traits of InpatientCampylobacter jejuni Isolates, and a Transcriptomic Approach to Identify Potential Genes Maintaining Intracellular Survival.Microorganisms 2020, 8, 531. [CrossRef] [PubMed]9. Talukdar, P.K.; Negretti, N.M.; Turner, K.L.; Konkel, M.E. Molecular Dissection of the Campylobacter jejuni CadF and FlpAVirulence Proteins in Binding to Host Cell Fibronectin. Microorganisms 2020, 8, 389. [CrossRef]10. Guirado, P.; Paytubi, S.; Miró, E.; Iglesias-Torrens, Y.; Navarro, F.; Cerdà-Cuéllar, M.; Attolini, C.S.-O.; Balsalobre, C.; Madrid, C.Differential Distribution of the wlaN and cgtB Genes, Associated with Guillain-Barré Syndrome, in Campylobacter jejuni Isolatesfrom Humans, Broiler Chickens, and Wild Birds. Microorganisms 2020, 8, 325. [CrossRef]11. Guk, J.-H.; Kim, J.; Song, H.; Kim, J.; An, J.-U.; Kim, J.; Ryu, S.; Jeon, B.; Cho, S. Hyper-Aerotolerant Campylobacter coli from DuckSources and Its Potential Threat to Public Health: Virulence, Antimicrobial Resistance, and Genetic Relatedness. Microorganisms2019, 7, 579. [CrossRef]12. Kløve, S.; Genger, C.; Weschka, D.; Mousavi, S.; Bereswill, S.; Heimesaat, M.M. Toll-Like Receptor-4 Is Involved in MediatingIntestinal and Extra-Intestinal Inflammation in Campylobacter coli-Infected Secondary Abiotic IL-10-/- Mice. Microorganisms 2020,8, 1882. [CrossRef]13. Heimesaat, M.M.; Mousavi, S.; Escher, U.; De Sá, F.D.L.; Peh, E.; Schulzke, J.-D.; Kittler, S.; Bücker, R.; Bereswill, S. ResveratrolAlleviates Acute Campylobacter jejuni Induced Enterocolitis in a Preclinical Murine Intervention Study. Microorganisms 2020, 8,1858. [CrossRef]14. Heimesaat, M.M.; Mousavi, S.; Kløve, S.; Genger, C.; Weschka, D.; Giladi, E.; Bereswill, S.; Gozes, I. Immune-modulatoryProperties of the Octapeptide NAP in Campylobacter jejuni Infected Mice Suffering from Acute Enterocolitis. Microorganisms2020, 8, 802. [CrossRef]15. Rapp, D.; Ross, C.; Hea, S.-Y.; Brightwell, G. Importance of the Farm Environment and Wildlife for Transmission of Campylobacterjejuni in A Pasture-Based Dairy Herd. Microorganisms 2020, 8, 1877. [CrossRef]16. Šimunović, K.; Zajkoska, S.; Bezek, K.; Klančnik, A.; Maganja, D.B.; Možina, S.S. Comparison of Campylobacter jejuni Slaugh-terhouse and Surface-Water Isolates Indicates Better Adaptation of Slaughterhouse Isolates to the Chicken Host Environment.Microorganisms 2020, 8, 1693. [CrossRef]Microorganisms 2021, 9, 1241 4 of 417. Di Donato, G.; Marotta, F.; Nuvoloni, R.; Zilli, K.; Neri, D.; Di Sabatino, D.; Calistri, P.; Di Giannatale, E. Prevalence, PopulationDiversity and Antimicrobial Resistance of Campylobacter coli Isolated in Italian Swine at Slaughterhouse. Microorganisms 2020, 8,222. [CrossRef] [PubMed]18. Liang, L.; Carrigy, N.B.; Kariuki, S.; Muturi, P.; Onsare, R.; Nagel, T.; Vehring, R.; Connerton, P.L.; Connerton, I.F. Developmentof a Lyophilization Process for Campylobacter Bacteriophage Storage and Transport. Microorganisms 2020, 8, 282. [CrossRef][PubMed]19. Bandoy, D.D.R.; Weimer, B.C. Biological Machine Learning Combined with Campylobacter Population Genomics RevealsVirulence Gene Allelic Variants Cause Disease. Microorganisms 2020, 8, 549. [CrossRef] [PubMed]20. Pumtang-On, P.; Mahony, T.; Hill, R.; Vanniasinkam, T. A Systematic Review of Campylobacter jejuni Vaccine Candidates forChickens. Microorganisms 2021, 9, 397. [CrossRef] [PubMed]21. Mousavi, S.; Bereswill, S.; Heimesaat, M.M. Novel Clinical Campylobacter jejuni Infection Models Based on Sensitization ofMice to Lipooligosaccharide, A Major Bacterial Factor Triggering Innate Immune Responses in Human Campylobacteriosis.Microorganisms 2020, 8, 482. [CrossRef] [PubMed]22. Tram, G.; Day, C.J.; Korolik, V. Bridging the Gap: A Role for Campylobacter jejuni Biofilms. Microorganisms 2020, 8, 452. [CrossRef][PubMed]

Foodborne Pathogen Campylobacter.

Campylobacter is the most common bacterial cause of human gastroenteritis in the world, with the species Campylobacter jejuni being responsible for over 80% of Campylobacter infections [...

Nicolae Corcionivoschi

Ozan Gundogdu

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Foodborne Pathogen Campylobacter

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Foodborne Pathogen Campylobacter

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