Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions

. 2015 ; 6 () : 709. [epub] 20150713

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid26217332

During the last years, Campylobacter has emerged as the leading cause of bacterial foodborne infections in developed countries. Described as an obligate microaerophile, Campylobacter has puzzled scientists by surviving a wide range of environmental oxidative stresses on foods farm to retail, and thereafter intestinal transit and oxidative damage from macrophages to cause human infection. In this study, confocal laser scanning microscopy (CLSM) was used to explore the biofilm development of two well-described Campylobacter jejuni strains (NCTC 11168 and 81-176) prior to or during cultivation under oxygen-enriched conditions. Quantitative and qualitative appraisal indicated that C. jejuni formed finger-like biofilm structures with an open ultrastructure for 81-176 and a multilayer-like structure for NCTC 11168 under microaerobic conditions (MAC). The presence of motile cells within the biofilm confirmed the maturation of the C. jejuni 81-176 biofilm. Acclimation of cells to oxygen-enriched conditions led to significant enhancement of biofilm formation during the early stages of the process. Exposure to these conditions during biofilm cultivation induced an even greater biofilm development for both strains, indicating that oxygen demand for biofilm formation is higher than for planktonic growth counterparts. Overexpression of cosR in the poorer biofilm-forming strain, NCTC 11168, enhanced biofilm development dramatically by promoting an open ultrastructure similar to that observed for 81-176. Consequently, the regulator CosR is likely to be a key protein in the maturation of C. jejuni biofilm, although it is not linked to oxygen stimulation. These unexpected data advocate challenging studies by reconsidering the paradigm of fastidious requirements for C. jejuni growth when various subpopulations (from quiescent to motile cells) coexist in biofilms. These findings constitute a clear example of a survival strategy used by this emerging human pathogen.

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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

Batz M. B., Hoffmann S., Morris J. G. (2012). Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J. Food Prot. 75, 1278–1291. 10.4315/0362-028X.JFP-11-418 PubMed DOI

Brown H. L., Reuter M., Hanman K., Betts R. P., van Vliet A. H. M. (2015). Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni. PLoS ONE 10:e0121680. 10.1371/journal.pone.0121680 PubMed DOI PMC

Butzler J. P. (2004). Campylobacter, from obscurity to celebrity. Clin. Microbiol. Infect. 10, 868–876. 10.1111/j.1469-0691.2004.00983.x PubMed DOI

Cameron A., Frirdich E., Huynh S., Parker C. T., Gaynor E. C. (2012). Hyperosmotic stress response of Campylobacter jejuni. J. Bacteriol. 194, 6116–6130. 10.1128/JB.01409-12 PubMed DOI PMC

Candon H. L., Allan B. J., Fraley C. D., Gaynor E. C. (2007). Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J. Bacteriol. 189, 8099–8108. 10.1128/JB.01037-07 PubMed DOI PMC

Chantarapanont W., Berrang M., Frank J. F. (2003). Direct microscopic observation and viability determination of Campylobacter jejuni on chicken skin. J. Food Prot. 66, 2222–2230. PubMed

Chaudhuri R. R., Loman N. J., Snyder L. A., Bailey C. M., Stekel D. J., Pallen M. J. (2008). xBASE2: a comprehensive resource for comparative bacterial genomics. Nucleic Acids Res. 36, D543–D546. 10.1093/nar/gkm928 PubMed DOI PMC

Corcoran A. T., Moran A. P. (2007). Influence of growth conditions on diverse polysaccharide production by Campylobacter jejuni. FEMS Immunol. Med. Microbiol. 49, 124–132. 10.1111/j.1574-695X.2006.00178.x PubMed DOI

Djordjevic D., Wiedmann M., McLandsborough L. A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microbiol. 68, 2950–2958. 10.1128/AEM.68.6.2950-2958.2002 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

EFSA. (2010). European food safety authority, European centre for disease prevention and control: analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008. EFSA J. 8, 1503–1603. 10.2903/j.efsa.2010.1503 DOI

EFSA. (2012). European food safety authority, european centre for disease prevention and control: the European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J. 10, 2597–3039. 10.2903/j.efsa.2012.2597 DOI

EFSA. (2013). European food safety authority, European centre for disease prevention and control: the European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J. 11, 3129–3379. 10.2903/j.efsa.2013.3129 DOI

Epps S. V. R., Harvey R. B., Hume M. E., Phillips T. D., Anderson R. C., Nisbet D. J. (2013). Foodborne Campylobacter: infections, metabolism, pathogenesis and reservoirs. Int. J. Environ. Res. Public Health 10, 6292–6304. 10.3390/ijerph10126292 PubMed DOI PMC

Fields J. A., Thompson S. A. (2008). Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J. Bacteriol. 190, 3411–3416. 10.1128/JB.01928-07 PubMed DOI PMC

Frirdich E., Vermeulen J., Biboy J., Soares F., Taveirne M. E., Johnson J. G., et al. . (2014). Peptidoglycan ld-Carboxypeptidase Pgp2 influences Campylobacter jejuni helical cell shape and pathogenic properties and provides the substrate for the dl-Carboxypeptidase Pgp1. J. Biol. Chem. 289, 8007–8018. 10.1074/jbc.M113.491829 PubMed DOI PMC

Garenaux 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 PubMed DOI

Golz G., Rosner B., Hofreuter D., Josenhans C., Kreienbrock L., Lowenstein A., et al. . (2014). Relevance of Campylobacter to public health-the need for a one health approach. Int. J. Med. Microbiol. 304, 817–823. 10.1016/j.ijmm.2014.08.015 PubMed DOI

Gundogdu O., Mills D. C., Elmi A., Martin M. J., Wren B. W., Dorrell N. (2011). The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J. Bacteriol. 193, 4238–4249. 10.1128/JB.05189-11 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

Guyard-Nicodeme M., Tresse O., Houard E., Jugiau F., Courtillon C., El Manaa K., et al. . (2013). Characterization of Campylobacter spp. transferred from naturally contaminated chicken legs to cooked chicken slices via a cutting board. Int. J. Food Microbiol. 164, 7–14. 10.1016/j.ijfoodmicro.2013.03.009 PubMed DOI

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 PubMed DOI

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., Zhang Q. J., 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

Ica T., Caner V., Istanbullu O., Hung Duc N., Ahmed B., Call D. R., et al. . (2011). Characterization of mono- and mixed-culture Campylobacter jejuni biofilms. Appl. Environ. Microbiol. 78, 1033–1038. 10.1128/AEM.07364-11 PubMed DOI PMC

Jang K. I., Kim M. G., Ha S. D., Kim K. S., Lee K. H., Chung D. H., et al. . (2007). Morphology and adhesion of Campylobacter jejuni to chicken skin under varying conditions. J. Microbiol. Biotechnol. 17, 202–206. PubMed

Jones K. (2001). The Campylobacter conundrum. Trends Microbiol. 9, 365–366. 10.1016/S0966-842X(01)02106-0 PubMed DOI

Joshua G. W. P., Guthrie-Irons C., Karlyshev A. V., Wren B. W. (2006). Biofilm formation in Campylobacter jejuni. Microbiology 152, 387–396. 10.1099/mic.0.28358-0 PubMed DOI

Kaakoush N. O., Mitchell H. M., Man S. M. (2014). Role of emerging Campylobacter species in inflammatory bowel diseases. Inflamm. Bowel Dis. 20, 2189–2197. 10.1097/MIB.0000000000000074 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

Kelly D. J. (2008). Complexity and versatility in the physiology and metabolism of Campylobacter jejuni, in Campylobacter, 3rd Edn., eds Nachamkin I., Szymanski C. M., Blaser M. J. (Washington, DC: American Society for Microbiology Press; ), 41–62. 10.1128/9781555815554.ch3 DOI

Kudirkiene E., Cohn M. T., Stabler R. A., Strong P. C. R., Serniene L., Wren B. W., et al. . (2012). Phenotypic and genotypic characterizations of Campylobacter jejuni isolated from the broiler meat production process. Curr. Microbiol. 65, 398–406. 10.1007/s00284-012-0170-z PubMed DOI

Lawes J. R., Vidal A., Clifton-Hadley F. A., Sayers R., Rodgers J., Snow L., et al. . (2012). Investigation of prevalence and risk factors for Campylobacter in broiler flocks at slaughter: results from a UK survey. Epidemiol. Infect. 140, 1725–1737. 10.1017/S0950268812000982 PubMed DOI

Lee Y. D., Choi J. P., Mok C. K., Ji G. E., Kim H. Y., Noh B. S., et al. (2004). Expression of flagellin proteins of Campylobacter jejuni within microaerobic and aerobic exposures. J. Microbiol. Biotechnol. 14, 1227–1231.

Lu X., Weakley A. T., Aston D. E., Rasco B. A., Wang S., Konkel M. E. (2012). Examination of nanoparticle inactivation of Campylobacter jejuni biofilms using infrared and Raman spectroscopies. J. Appl. Microbiol. 113, 952–963. 10.1111/j.1365-2672.2012.05373.x PubMed DOI PMC

McLennan M. K., Ringoir D. D., Frirdich E., Svensson S. L., Wells D. H., Jarrell H., et al. . (2008). Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white-reactive polysaccharide. J. Bacteriol. 190, 1097–1107. 10.1128/JB.00516-07 PubMed DOI PMC

Mooney A., Byrne C., Clyne M., Johnson-Henry K., Sherman P., Bourke B. (2003). Invasion of human epithelial cells by Campylobacter upsaliensis. Cell. Microbiol. 5, 835–847. 10.1046/j.1462-5822.2003.00325.x PubMed DOI

Moore J. E., Corcoran D., Dooley J. S. G., Fanning S., Lucey B., Matsuda M., et al. . (2005). Campylobacter. Vet. Res. 36, 351–382. 10.1051/vetres:2005012 PubMed DOI

Muller S., Pflock M., Schar J., Kennard S., Beier D. (2007). Regulation of expression of atypical orphan response regulators of Helicobacter pylori. Microbiol. Res. 162, 1–14. 10.1016/j.micres.2006.01.003 PubMed DOI

Nachamkin I., Allos B. M., Ho T. (1998). Campylobacter species and Guillain-Barre syndrome. Clin. Microbiol. Rev. 11, 555–567. PubMed PMC

Naito M., Frirdich E., Fields J. A., Pryjma M., Li J. J., Cameron A., et al. . (2010). Effects of Sequential Campylobacter jejuni 81-176 Lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J. Bacteriol. 192, 2182–2192. 10.1128/JB.01222-09 PubMed DOI PMC

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

Nguyen V. T., Turner M. S., Dykes G. A. (2011). Influence of cell surface hydrophobicity on attachment of Campylobacter to abiotic surfaces. Food Microbiol. 28, 942–950. 10.1016/j.fm.2011.01.004 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

Powell L. F., Lawes J. R., Clifton-Hadley F. A., Rodgers J., Harris K., Evans S. J., et al. . (2012). The prevalence of Campylobacter spp. in broiler flocks and on broiler carcases, and the risks associated with highly contaminated carcases. Epidemiol. Infect. 140, 2233–2246. 10.1017/S0950268812000040 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

Reid A. N., Pandey R., Palyada K., Naikare H., Stintzi A. (2008). Identification of Campylobacter jejuni genes involved in the response to acidic pH and stomach transit. Appl. Environ. Microbiol. 74, 1583–1597. 10.1128/AEM.01507-07 PubMed DOI PMC

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 PubMed DOI PMC

Salloway S., Mermel L. A., Seamans M., Aspinall G. O., Shin J. E. N., Kurjanczyk L. A., et al. . (1996). Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD(3). Infect. Immun. 64, 2945–2949. PubMed PMC

Sanders S. Q., Boothe D. H., Frank J. F., Arnold J. W. (2007). Culture and detection of Campylobacter jejuni within mixed microbial populations of biofilms on stainless steel. J. Food Prot. 70, 1379–1385. PubMed

Sanders S. Q., Frank J. F., Arnold J. W. (2008). Temperature and nutrient effects on Campylobacter jejuni attachment on multispecies biofilms on stainless steel. J. Food Prot. 71, 271–278. PubMed

Stahl M., Stintzi A. (2011). Identification of essential genes in C. jejuni genome highlights hyper-variable plasticity regions. Funct. Integr. Genomics 11, 241–257. 10.1007/s10142-011-0214-7 PubMed DOI

Sulaeman S., Hernould M., Schaumann A., Coquet L., Bolla J. M., De 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 PubMed DOI PMC

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 (R). J. Appl. Microbiol. 108, 1303–1312. 10.1111/j.1365-2672.2009.04534.x PubMed 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

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 PubMed DOI PMC

Teh K. H., Flint S., French N. (2010). Biofilm formation by Campylobacter jejuni in controlled mixed-microbial populations. Int. J. Food Microbiol. 143, 118–124. 10.1016/j.ijfoodmicro.2010.07.037 PubMed DOI

Van Vliet A. H. M., Ketley J. M., Park S. F., Penn C. W. (2002). The role of iron in Campylobacter gene regulation, metabolism and oxidative stress defense. FEMS Microbiol. Rev. 26, 173–186. 10.1111/j.1574-6976.2002.tb00609.x PubMed DOI

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