Adhesion, Biofilm Formation, and Genomic Features of Campylobacter jejuni Bf, an Atypical Strain Able to Grow under Aerobic Conditions
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
27446042
PubMed Central
PMC4927563
DOI
10.3389/fmicb.2016.01002
Knihovny.cz E-resources
- Keywords
- biofilm, confocal microscopy, food borne pathogen, genome sequence, oxidative stress,
- Publication type
- Journal Article MeSH
Campylobacter jejuni is the leading cause of bacterial enteritis in Europe. Human campylobacteriosis cases are frequently associated to the consumption of contaminated poultry meat. To survive under environmental conditions encountered along the food chain, i.e., from poultry digestive tract its natural reservoir to the consumer's plate, this pathogen has developed adaptation mechanisms. Among those, biofilm lifestyle has been suggested as a strategy to survive in the food environment and under atmospheric conditions. Recently, the clinical isolate C. jejuni Bf has been shown to survive and grow under aerobic conditions, a property that may help this strain to better survive along the food chain. The aim of this study was to evaluate the adhesion capacity of C. jejuni Bf and its ability to develop a biofilm. C. jejuni Bf can adhere to abiotic surfaces and to human epithelial cells, and can develop biofilm under both microaerobiosis and aerobiosis. These two conditions have no influence on this strain, unlike results obtained with the reference strain C. jejuni 81-176, which harbors only planktonic cells under aerobic conditions. Compared to 81-176, the biofilm of C. jejuni Bf is more homogenous and cell motility at the bottom of biofilm was not modified whatever the atmosphere used. C. jejuni Bf whole genome sequence did not reveal any gene unique to this strain, suggesting that its unusual property does not result from acquisition of new genetic material. Nevertheless some genetic particularities seem to be shared only between Bf and few others strains. Among the main features of C. jejuni Bf genome we noticed (i) a complete type VI secretion system important in pathogenicity and environmental adaptation; (ii) a mutation in the oorD gene involved in oxygen metabolism; and (iii) the presence of an uncommon insertion of a 72 amino acid coding sequence upstream from dnaK, which is involved in stress resistance. Therefore, the atypical behavior of this strain under aerobic atmosphere may result from the combination of insertions and mutations. In addition, the comparison of mRNA transcript levels of several genes targeted through genome analysis suggests the modification of regulatory processes in this strain.
See more in PubMed
Amblee V., Jeffery C. J. (2015). Physical features of intracellular proteins that moonlight on the cell surface. PLoS ONE 10:e0130575 10.1371/journal.pone.0130575 PubMed DOI PMC
Asakura H., Yamasaki M., Yamamoto S., Igimi S. (2007). Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol. Lett. 275 278–285. 10.1111/j.1574-6968.2007.00893.x PubMed DOI
Ashgar S. S., Oldfield N. J., Wooldridge K. G., Jones M. A., Irving G. J., Turner D. P., et al. (2007). CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut. J. Bacteriol. 189 1856–1865. 10.1128/JB.01427-06 PubMed DOI PMC
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 PubMed DOI PMC
Bachtiar B. M., Coloe P. J., Fry B. N. (2007). Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions. FEMS Immunol. Med. Microbiol. 49 149–154. 10.1111/j.1574-695X.2006.00182.x PubMed DOI
Baillon M.-L. A., van Vliet A. H., 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. PubMed PMC
Batz M., Hoffmann S., Morris J. G., Jr. (2014). Disease-outcome trees, EQ-5D scores, and estimated annual losses of quality-adjusted life years (QALYs) for 14 foodborne pathogens in the United States. Foodborne Pathog. Dis. 11 395–402. 10.1089/fpd.2013.1658 PubMed DOI
Bleumink-Pluym N. M., van Alphen L. B., Bouwman L. I., Wosten M. M., van Putten J. P. (2013). Identification of a functional type VI secretion system in Campylobacter jejuni conferring capsule polysaccharide sensitive cytotoxicity. PLoS Pathog. 9:e1003393 10.1371/journal.ppat.1003393 PubMed DOI PMC
Bronnec V., Haddad N., Cruveiller S., Hernould M., Tresse O., Zagorec M. (2016). Draft genome sequence of Campylobacter jejuni Bf, an atypical strain able to grow under aerobiosis Genome Announc. 4:e00120-16 10.1128/genomeA.00120-16 PubMed DOI PMC
Buswell C. M., Herlihy Y. M., Lawrence L. M., McGuiggan J. T., Marsh P. D., Keevil C. W., et al. (1998). Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl. Environ. Microbiol. 64 733–741. PubMed PMC
Butcher J., Flint A., Stahl M., Stintzi A. (2010). “Campylobacter Fur and PerR regulons,” in Iron uptake and homeostasis in microorganisms eds Cornelis P., Andrews S. C. (Haverhill: Caister Academic Press; ) 168–202.
Chmielewski R., Frank J. (2003). Biofilm formation and control in food processing facilities. Compr. Rev. Food Sci. Food Saf. 2 22–32. 10.1111/j.1541-4337.2003.tb00012.x PubMed DOI
Chynoweth R. W., Hudson J. A., Thom K. (1998). Aerobic growth and survival of Campylobacter jejuni in food and stream water. Lett. Appl. Microbiol. 27 341–344. 10.1046/j.1472-765X.1998.00453.x PubMed DOI
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. 7:1 10.1186/s13099-015-0067-z PubMed DOI PMC
Costerton J. (1995). Overview of microbial biofilms. J. Ind. Microbiol. 15 137–140. 10.1007/BF01569816 PubMed DOI
Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M. (1995). Microbial biofilms. Ann. Rev. Microbiol. 49 711–745. 10.1146/annurev.mi.49.100195.003431 PubMed DOI
Del Rocio Leon-Kempis M., Guccione E., Mulholland F., Williamson M. P., Kelly D. J. (2006). The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol. Microbiol. 60 1262–1275. 10.1111/j.1365-2958.2006.05168.x PubMed DOI
Donlan R. M. (2002). Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8 881–890. 10.3201/eid0809.020063 PubMed DOI PMC
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 PubMed DOI PMC
Eberle K. N., Kiess A. S. (2012). Phenotypic and genotypic methods for typing Campylobacter jejuni and Campylobacter coli in poultry. Poult. Sci. 91 255–264. 10.3382/ps.2011-01414 PubMed DOI
EFSA and ECDC (2016). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 2015. 13:4329 10.2903/j.efsa.2015.4329 PubMed DOI PMC
Floch P., Pey V., Castroviejo M., Dupuy J. W., Bonneu M., de La Guardia A. H., et al. (2014). Role of Campylobacter jejuni gamma-glutamyl transpeptidase on epithelial cell apoptosis and lymphocyte proliferation. Gut Pathog. 6:1 10.1186/1757-4749-6-20 PubMed DOI PMC
Flanagan R. C., Neal-McKinney J. M., Dhillon A. S., Miller W. G., Konkel M. E. (2009). Examination of Campylobacter jejuni putative adhesins leads to the identification of a new protein, designated FlpA, required for chicken colonization. Infect. Immun. 77 2399–2407. 10.1128/IAI.01266-08 PubMed DOI PMC
Flint A., Sun Y.-Q., Butcher J., Stahl M., Huang H., Stintzi A. (2014). Phenotypic screening of a targeted mutant library reveals Campylobacter jejuni defenses against oxidative stress. Infect. Immun. 82 2266–2275. 10.1128/IAI.01528-13 PubMed DOI PMC
Fouts D. E., Mongodin E. F., Mandrell R. E., Miller W. G., Rasko D. A., Ravel J., et al. (2005). Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol. 3:e15 10.1371/journal.pbio.0030015 PubMed DOI PMC
Garénaux A., Guillou S., Ermel G., Wren B., Federighi M., Ritz M. (2008a). 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 PubMed DOI
Garénaux A., Jugiau F., Rama F., de Jonge R., Denis M., Federighi M., et al. (2008b). Survival of Campylobacter jejuni strains from different origins under oxidative stress conditions: effect of temperature. Curr. Microbiol. 56 293–297. 10.1007/s00284-007-9082-8 PubMed DOI
Gilbert P., Evans D. J., Brown M. R. (1993). Formation and dispersal of bacterial biofilms in vivo and in situ. J. Appl. Bacteriol. 74(Suppl.) 67S–78S. 10.1111/j.1365-2672.1993.tb04343.x PubMed DOI
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 PubMed DOI
Gundogdu O., Bentley S. D., Holden M. T., Parkhill J., Dorrell N., Wren B. W. (2007). Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8:162 10.1186/1471-2164-8-162 PubMed DOI PMC
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 PubMed DOI
Haddad N., Maillart G., Garénaux A., Jugiau F., Federighi M., Cappelier J. M. (2010). Adhesion ability of Campylobacter jejuni to Ht-29 cells increases with the augmentation of oxidant agent concentration. Curr. Microbiol. 61 500–505. 10.1007/s00284-010-9644-z PubMed DOI
Haddad N., Tresse O., Rivoal K., Chevret D., Nonglaton Q., Burns C. M., et al. (2012). Polynucleotide phosphorylase has an impact on cell biology of Campylobacter jejuni. Front. Cell. Infect. Microbiol. 2:30 10.3389/fcimb.2012.00030 PubMed DOI PMC
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 10.3201/eid2006.130635 PubMed DOI PMC
Hepworth P. J., Ashelford K. E., Hinds J., Gould K. A., Witney A. A., Williams N. J., et al. (2011). Genomic variations define divergence of water/wildlife-associated Campylobacter jejuni niche specialists from common clonal complexes. Environ. Microbiol. 13 1549–1560. 10.1111/j.1462-2920.2011.02461.x PubMed DOI PMC
Hinton A., Jr. (2016). Growth of Campylobacter incubated aerobically in fumarate-pyruvate media or media supplemented with dairy, meat, or soy extracts and peptones. Food Microbiol. 58 23–28. 10.1016/j.fm.2016.03.010 PubMed DOI
Hofreuter D., Tsai J., Watson R. O., Novik V., Altman B., Benitez M., et al. (2006). Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74 4694–4707. 10.1128/IAI.00210-06 PubMed DOI PMC
Hughes N. J., Clayton C. L., Chalk P. A., Kelly D. J. (1998). Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate: flavodoxin and 2-Oxoglutarate: acceptor oxidoreductases which mediate electron transport to NADP. J. Bacteriol. 180 1119–1128. PubMed PMC
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 PubMed DOI PMC
Hwang S., Miller W. G., Ryu S., Jeon B. (2014). Divergent distribution of the sensor kinase CosS in non-thermotolerant Campylobacter species and its functional incompatibility with the response regulator CosR of Campylobacter jejuni. PLoS ONE 9:e89774 10.1371/journal.pone.0089774 PubMed DOI PMC
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 PubMed DOI PMC
Hyytiäinen H., Juntunen P., Akrenius N., Hänninen M.-L. (2012). Importance of RNA stabilization: evaluation of ansB, ggt, and rpoA transcripts in microaerophilic Campylobacter jejuni 81176. Arch. Microbiol. 194 803–808. 10.1007/s00203-012-0820-3 PubMed DOI
Ishikawa T., Mizunoe Y., Kawabata S.-I., Takade A., Harada M., Wai S. N., et al. (2003). The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J. Bacteriol. 185 1010–1017. 10.1128/JB.185.3.1010-1017.2003 PubMed DOI PMC
Jeon B., Muraoka W. T., Zhang Q. (2010). Advances in Campylobacter biology and implications for biotechnological applications. Microb. Biotechnol. 3 242–258. 10.1111/j.1751-7915.2009.00118.x PubMed DOI PMC
Jin S., Joe A., Lynett J., Hani E. K., Sherman P., Chan V. L. (2001). JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol. Microbiol. 39 1225–1236. 10.1111/j.1365-2958.2001.02294.x PubMed DOI
Joshua G. P., Guthrie-Irons C., Karlyshev A., Wren B. (2006). Biofilm formation in Campylobacter jejuni. Microbiology 152 387–396. 10.1099/mic.0.28358-0 PubMed DOI
Kalmokoff M., Lanthier P., Tremblay T. L., Foss M., Lau P. C., Sanders G., et al. (2006). Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J. Bacteriol. 188 4312–4320. 10.1128/JB.01975-05 PubMed DOI PMC
Kervella M., Pagès J.-M., Pei Z., Grollier G., Blaser M. J., Fauchere J. (1993). Isolation and characterization of two Campylobacter glycine-extracted proteins that bind to HeLa cell membranes. Infect. Immun. 61 3440–3448. PubMed PMC
Kim J. -C., Oh E., Hwang S., Ryu S., Jeon B. (2015). Non-selective regulation of peroxide and superoxide resistance genes by PerR in Campylobacter jejuni. Front. Microbiol. 6:126 10.3389/fmicb.2015.00126 PubMed DOI PMC
Konkel M. E., Garvis S. G., Tipton S. L., Anderson D. E., Jr., Cieplak W., Jr. (1997). Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol. Microbiol. 24 953–963. 10.1046/j.1365-2958.1997.4031771.x PubMed DOI
Konkel M. E., Larson C. L., Flanagan R. C. (2010). Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J. Bacteriol. 192 68–76. 10.1128/JB.00969-09 PubMed DOI PMC
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 PubMed DOI PMC
Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. Methods 25 402–408. 10.1006/meth.2001.1262 PubMed DOI
Monteville M. R., Yoon J. E., Konkel M. E. (2003). Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149 153–165. 10.1099/mic.0.25820-0 PubMed DOI
Moser I., Schroeder W., Salnikow J. (1997). Campylobacter jejuni major outer membrane protein and a 59-kDa protein are involved in binding to fibronectin and INT 407 cell membranes. FEMS Microbiol. Lett. 157 233–238. 10.1111/j.1574-6968.1997.tb12778.x PubMed DOI
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 PubMed DOI
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 PubMed DOI PMC
Park S. F. (2002). The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int. J. Food. Microbiol. 74 177–188. 10.1016/S0168-1605(01)00678-X PubMed DOI
Parker C. T., Gilbert M., Yuki N., Endtz H. P., Mandrell R. E. (2008). Characterization of lipooligosaccharide-biosynthetic loci of Campylobacter jejuni reveals new lipooligosaccharide classes: evidence of mosaic organizations. J. Bacteriol. 190 5681–5689. 10.1128/JB.00254-08 PubMed DOI PMC
Parker C. T., Horn S. T., Gilbert M., Miller W. G., Woodward D. L., Mandrell R. E. (2005). Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. J. Clin. Microbiol. 43 2771–2781. 10.1128/JCM.43.6.2771-2781.2005 PubMed DOI PMC
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 PubMed DOI
Pearson B. M., Gaskin D. J., Segers R. P., Wells J. M., Nuijten P. J., van Vliet A. H. (2007). The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J. Bacteriol. 189 8402–8403. 10.1128/JB.01404-07 PubMed DOI PMC
Pei Z., Burucoa C., Grignon B., Baqar S., Huang X.-Z., Kopecko D. J., et al. (1998). Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun. 66 938–943. PubMed PMC
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. PubMed PMC
Rahman H., King R. M., Shewell L. K., Semchenko E. A., Hartley-Tassell L. E., Wilson J. C., et al. (2014). Characterisation of a multi-ligand binding chemoreceptor CcmL (Tlp3) of Campylobacter jejuni. PLoS Pathog. 10:e1003822 10.1371/journal.ppat.1003822 PubMed DOI PMC
Reeser R. J., Medler R. T., Billington S. J., Jost B. H., Joens L. A. (2007). Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl. Environ. Microbiol. 73 1908–1913. 10.1128/AEM.00740-06 PubMed DOI PMC
Reuter M., Mallett A., Pearson B. M., van Vliet A. H. (2010). Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 76 2122–2128. 10.1128/AEM.01878-09 PubMed DOI PMC
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. 7:1 10.1186/s13099-015-0077-x PubMed DOI PMC
Stewart P. S., Franklin M. J. (2008). Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6 199–210. 10.1038/nrmicro1838 PubMed DOI
Sulaeman S., Le Bihan G., Rossero A., Federighi M., De 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 PubMed DOI
Sung K., Khan S. (2015). “Biofilm development by Campylobacter jejuni,” in Biofilms in the Food Environment 2nd Edn eds Pometto A. L., Demirci A. 29–50. 10.1002/9781118864036.ch2 DOI
Svensson S. L., Davis L. M., MacKichan J. K., Allan B. J., Pajaniappan M., Thompson S. A., et al. (2009). The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol. Microbiol. 71 253–272. 10.1111/j.1365-2958.2008.06534.x PubMed DOI PMC
Takamiya M., Ozen A., Rasmussen M., Alter T., Gilbert T., Ussery D. W., et al. (2011). Genome Sequence of Campylobacter jejuni strain 327, a strain isolated from a turkey slaughterhouse. Stand. Genomic Sci. 4 113–122. 10.4056/sigs.1313504 PubMed DOI PMC
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 PubMed DOI PMC
Turonova H., Neu T., 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 PubMed DOI
Vallenet D., Belda E., Calteau A., Cruveiller S., Engelen S., Lajus A., et al. (2013). MicroScope - an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res. 41 D636–D647. 10.1093/nar/gks1194 PubMed DOI PMC
Vallenet D., Labarre L., Rouy Z., Barbe V., Bocs S., Cruveiller S., et al. (2006). MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 34 53–65. 10.1093/nar/gkj406 PubMed DOI PMC
WHO (2013). The Global View of Campylobacteriosis: Report of an Expert Consultation. Geneva: WHO Document Production Services; 57.
Zeng X., Mo Y., Xu F., Lin J. (2013a). Identification and characterization of a periplasmic trilactone esterase, Cee, revealed unique features of ferric enterobactin acquisition in Campylobacter. Mol. Microbiol. 87 594–608. 10.1111/mmi.12118 PubMed DOI PMC
Zeng X., Xu F., Lin J. (2013b). Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition in Campylobacter. FEMS Microbiol. Lett. 347 83–91. 10.1111/1574-6968.12221 PubMed DOI PMC
Ziprin R. L., Young C. R., Stanker L. H., Hume M. E., Konkel M. E. (1999). The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein. Avian Dis. 43 586–589. 10.2307/1592660 PubMed DOI