Biofilm Formation in Arcobacter butzleri and Arcobacter cryaerophilus: Phenotypic and Genotypic Characterization of Food and Environmental Isolates
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
41472038
PubMed Central
PMC12735934
DOI
10.3390/microorganisms13122835
PII: microorganisms13122835
Knihovny.cz E-zdroje
- Klíčová slova
- Arcobacter butzleri, Arcobacter cryaerophilus, biofilm formation, biofilm-associated genes, dynamic biofilm assay, foodborne pathogen, static biofilm assay,
- Publikační typ
- časopisecké články MeSH
Arcobacter butzleri and Arcobacter cryaerophilus are emerging foodborne and waterborne pathogens associated with enteritis and extraintestinal infections in humans. Their persistence in the environment and resistance to antimicrobial treatment are closely related to their ability to form biofilms, which provide protection against adverse conditions and support survival on food contact surfaces. This study evaluated both the genotypic and phenotypic aspects of biofilm formation among A. butzleri and A. cryaerophilus isolates from food and environmental sources. Six biofilm-associated genes (flaA, flaB, fliS, luxS, pta, and spoT) were detected by multiplex PCR, and biofilm production was assessed using the Christensen microtiter plate assay and Congo Red Agar (CRA) test. All A. cryaerophilus isolates carried the same gene set as A. butzleri, suggesting conserved genetic determinants of motility and Quorum sensing. However, phenotypic assays revealed interspecific variability: while most A. butzleri isolates formed strong biofilms, 70% of A. cryaerophilus strains showed moderate to strong formation despite all being CRA-negative. No direct correlation between gene presence and biofilm intensity was observed, indicating complex regulation of biofilm development. This study provides a comparative overview of biofilm formation in A. butzleri and A. cryaerophilus and highlights their adaptive potential and persistence in food-related environments.
Zobrazit více v PubMed
Ramees T.P., Dhama K., Karthik K., Rathore R.S., Kumar A., Saminathan M., Tiwari R., Malik Y.S., Singh R.K. Arcobacter: An emerging food-borne zoonotic pathogen, its public health concerns and advances in diagnosis and control—A comprehensive review. Vet. Q. 2017;37:136–161. doi: 10.1080/01652176.2017.1323355. PubMed DOI
Collado L., Figueras M.J. Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin. Microbiol. Rev. 2011;24:174–192. doi: 10.1128/CMR.00034-10. PubMed DOI PMC
Levican A., Collado L., Figueras M.J. Arcobacter cloacae sp. nov. and Arcobacter suis sp. nov., two new species isolated from food and sewage. Syst. Appl. Microbiol. 2013;36:22–27. doi: 10.1016/j.syapm.2012.11.003. PubMed DOI
Ferreira S., Queiroz J.A., Oleastro M., Domingues F.C. Insights in the pathogenesis and resistance of Arcobacter: A review. Crit. Rev. Microbiol. 2016;42:364–383. doi: 10.3109/1040841X.2014.954523. PubMed DOI
Chiarini E., Buzzanca D., Chiesa F., Botta C., Rantsiou K., Houf K., Alessandria V. Exploring multi-antibiotic resistance in Arcobacter butzleri isolates from a poultry processing plant in northern Italy: An in-depth inquiry. Food Control. 2024;163:110500. doi: 10.1016/j.foodcont.2024.110500. DOI
Couto F., Martins I., Vale F., Domingues F., Oleastro M., Ferreira S. Insights into macrolide resistance in Arcobacter butzleri: Potential resistance mechanisms and impact on bacterial fitness and virulence. J. Antimicrob. Chemother. 2024;79:2708–2717. doi: 10.1093/jac/dkae287. PubMed DOI
Donlan R.M., Costerton J.W. Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms. Clin. Microbiol. Rev. 2002;15:167–193. doi: 10.1128/CMR.15.2.167-193.2002. PubMed DOI PMC
Fanelli F., Di Pinto A., Mottola A., Mule G., Chieffi D., Baruzzi F., Tantillo G., Fusco V. Genomic Characterization of Arcobacter butzleri Isolated from Shellfish: Novel Insight into Antibiotic Resistance and Virulence Determinants. Front. Microbiol. 2019;10:670. doi: 10.3389/fmicb.2019.00670. PubMed DOI PMC
Assanta M.A., Roy D., Lemay M.-J., Montpetit D. Attachment of Arcobacter butzleri, Arcobacter cryaerophilus, and Arcobacter skirrowii to abiotic surfaces and survival in water at 4 °C. J. Food Prot. 2002;65:1240–1247. doi: 10.4315/0362-028X-65.8.1240. PubMed DOI
Šilha D., Sirotková S., Švarcová K., Hofmeisterová L., Koryčanová K., Šilhová L. Biofilm formation ability of Arcobacter-like and Campylobacter strains under different conditions and on food processing materials. Microorganisms. 2021;9:2017. doi: 10.3390/microorganisms9102017. PubMed DOI PMC
Martins R., Mateus C., Domingues F., Bücker R., Oleastro M., Ferreira S. Effect of atmospheric conditions on pathogenic phenotypes of Arcobacter butzleri. Microorganisms. 2022;10:2409. doi: 10.3390/microorganisms10122409. PubMed DOI PMC
Mateus C., Maia C.J., Domingues F., Bücker R., Oleastro M., Ferreira S. Evaluation of bile salts on the survival and modulation of virulence of Aliarcobacter butzleri. Antibiotics. 2023;12:1387. doi: 10.3390/antibiotics12091387. PubMed DOI PMC
Salazar-Sánchez A., Baztarrika I., Alonso R., Fernández-Astorga A., Martínez-Ballesteros I., Martinez-Malaxetxebarria I. Arcobacter butzleri Biofilms: Insights into the Genes Beneath Their Formation. Microorganisms. 2022;10:1280. doi: 10.3390/microorganisms10071280. PubMed DOI PMC
Guerry P. Campylobacter flagella: Not just for motility. Trends Microbiol. 2007;15:456–461. doi: 10.1016/j.tim.2007.09.006. PubMed DOI
Martínez-Malaxetxebarria I., Girbau C., Salazar-Sánchez A., Baztarrika I., Martínez-Ballesteros I., Laorden L., Alonso R., Fernández-Astorga A. Genetic characterization and biofilm formation of potentially pathogenic foodborne Arcobacter isolates. Int. J. Food Microbiol. 2022;373:109712. doi: 10.1016/j.ijfoodmicro.2022.109712. PubMed DOI
Reeser R.J., Medler R.T., Billington S.J., Jost B.H., Joens L.A. Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl. Environ. Microbiol. 2007;73:1908–1913. doi: 10.1128/AEM.00740-06. PubMed DOI PMC
Potrykus K., Cashel M. (p)ppGpp: Still magical? Annu. Rev. Microbiol. 2008;62:35–51. doi: 10.1146/annurev.micro.62.081307.162903. PubMed DOI
Šilha D., Šilhová-Hrušková L., Vytřasová J. Modified isolation method of Arcobacter spp. from different environmental and food samples. Folia Microbiol. 2015;60:515–521. doi: 10.1007/s12223-015-0395-x. PubMed DOI
Douidah L., De Zutter L., Vandamme P., Houf K. Identification of five human and mammal associated Arcobacter species by a novel multiplex-PCR assay. J. Microbiol. Methods. 2010;80:281–286. doi: 10.1016/j.mimet.2010.01.009. PubMed DOI
Figueras M.J., Levican A., Collado L. Updated 16S rRNA-RFLP method for the identification of all currently characterised Arcobacter spp. BMC Microbiol. 2012;12:292. doi: 10.1186/1471-2180-12-292. PubMed DOI PMC
Marshall S.M., Melito P.L., Woodward D.L., Johnson W.M., Rodgers F.G., Mulvey M.R. Rapid identification of Campylobacter, Arcobacter, and Helicobacter isolates by PCR-restriction fragment length polymorphism analysis of the 16S rRNA gene. J. Clin. Microbiol. 1999;37:4158–4160. doi: 10.1128/JCM.37.12.4158-4160.1999. PubMed DOI PMC
Freeman D.J., Falkiner F.R., Keane C.T. New method for detecting slime production by coagulase negative staphylococci. J. Clin. Pathol. 1989;42:872–874. doi: 10.1136/jcp.42.8.872. PubMed DOI PMC
Kaiser T.D.L., Pereira E.M., dos Santos K.R.N., Maciel E.L.N., Schuenck R.P., Nunes A.P.F. Modification of the Congo red agar method to detect biofilm production by Staphylococcus epidermidis. Diagn. Microbiol. Infect. Dis. 2013;75:235–239. doi: 10.1016/j.diagmicrobio.2012.11.014. PubMed DOI
Christensen G.D., Simpson W.A., Younger J.J., Baddour L.M., Barrett F.F., Melton D.M., Beachey E.H. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: A quantitative model for the adherence of staphylococci to medical devices. J. Clin. Microbiol. 1985;22:996–1006. doi: 10.1128/jcm.22.6.996-1006.1985. PubMed DOI PMC
Stepanović S., Vuković D., Dakić I., Savić B., Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods. 2000;40:175–179. doi: 10.1016/S0167-7012(00)00122-6. PubMed DOI
Hall-Stoodley L., Costerton J.W., Stoodley P. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004;2:95–108. doi: 10.1038/nrmicro821. PubMed DOI
Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: A common cause of persistent infections. Science. 1999;284:1318–1322. doi: 10.1126/science.284.5418.1318. PubMed DOI
Høiby N., Ciofu O., Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 2010;5:1663–1674. doi: 10.2217/fmb.10.125. PubMed DOI
Flemming H.-C., Wingender J. The biofilm matrix. Nat. Rev. Microbiol. 2010;8:623–633. doi: 10.1038/nrmicro2415. PubMed DOI
Ferreira S., Fraqueza M.J., Queiroz J.A., Domingues F.C., Oleastro M. Genetic diversity, antibiotic resistance and biofilm-forming ability of Arcobacter butzleri isolated from poultry and environment from a Portuguese slaughterhouse. Int. J. Food Microbiol. 2013;162:82–88. doi: 10.1016/j.ijfoodmicro.2013.01.003. PubMed DOI
Kalmokoff M., Lanthier P., Tremblay T.-L., Foss M., Lau P.C., Sanders G., Austin J., Kelly J., Szymanski C.M. Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J. Bacteriol. 2006;188:4312–4320. doi: 10.1128/JB.01975-05. PubMed DOI PMC
Harshey R.M. Bacterial motility on a surface: Many ways to a common goal. Annu. Rev. Microbiol. 2003;57:249–273. doi: 10.1146/annurev.micro.57.030502.091014. PubMed DOI
Pratt L.A., Kolter R. Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 1998;30:285–293. doi: 10.1046/j.1365-2958.1998.01061.x. PubMed DOI
Ho H.T., Lipman L.J.A., Wösten M.M.S.M., van Asten A.J., Gaastra W. Arcobacter spp. possess two very short flagellins of which FlaA is essential for motility. FEMS Immunol. Med. Microbiol. 2008;53:85–95. doi: 10.1111/j.1574-695X.2008.00405.x. PubMed DOI
Medina G., Neves P., Flores-Martin S., Manosalva C., Andaur M., Otth C., Lincopan N., Fernández H. Transcriptional analysis of flagellar and putative virulence genes of Arcobacter butzleri as an endocytobiont of Acanthamoeba castellanii. Arch. Microbiol. 2019;201:1075–1083. doi: 10.1007/s00203-019-01678-0. PubMed DOI
Lee J.-S., Bae Y.-M., Han A., Lee S.-Y. Development of Congo red broth method for the detection of biofilm-forming or slime-producing Staphylococcus sp. LWT. 2016;73:707–714. doi: 10.1016/j.lwt.2016.03.023. DOI
Moreno X., Ventura M., Panizo M.M., Garcés M.F. Evaluación de la formación de biopelículas en aislamientos bacterianos y fúngicos por el método semicuantitativo de microtitulación con cristal violeta y el cualitativo de agar con rojo Congo. Biomédica. 2023;43:77–88. doi: 10.7705/biomedica.6732. PubMed DOI PMC
Girbau C., Martinez-Malaxetxebarria I., Muruaga G., Carmona S., Alonso R., Fernández-Astorga A. Study of biofilm formation ability of foodborne Arcobacter butzleri under different conditions. J. Food Prot. 2017;80:758–762. doi: 10.4315/0362-028X.JFP-16-505. PubMed DOI
Disli H.B., Hizlisoy H., Gungor C., Barel M., Dishan A., Gundog D.A., Al S., Onmaz N.E., Yildirim Y., Gonulalan Z. Investigation and characterization of Aliarcobacter spp. isolated from cattle slaughterhouse in Türkiye. Int. Microbiol. 2024;27:1321–1332. doi: 10.1007/s10123-023-00478-3. PubMed DOI
Stepanović S., Cirković I., Mijac V., Švabić-Vlahović M. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol. 2003;20:339–343. doi: 10.1016/S0740-0020(02)00123-5. DOI
Wolska K.I., Grudniak A.M., Rudnicka Z., Markowska K. Genetic control of bacterial biofilms. J. Appl. Genet. 2016;57:225–238. doi: 10.1007/s13353-015-0309-2. PubMed DOI PMC
Pacios O., Blasco L., Bleriot I., Fernandez-Garcia L., Ambroa A., López M., Bou G., Cantón R., Garcia-Contreras R., Wood T.K., et al. (p)ppGpp and its role in bacterial persistence: New challenges. Antimicrob. Agents Chemother. 2020;64:e01283-20. doi: 10.1128/AAC.01283-20. PubMed DOI PMC
Achinas S., Charalampogiannis N., Euverink G.J.W. A brief recap of microbial adhesion and biofilms. Appl. Sci. 2019;9:2801. doi: 10.3390/app9142801. DOI
Schütze A., Benndorf D., Püttker S., Kohrs F., Bettenbrock K. The impact of ackA, pta, and ackA-pta mutations on growth, gene expression and protein acetylation in Escherichia coli K-12. Front. Microbiol. 2020;11:233. doi: 10.3389/fmicb.2020.00233. PubMed DOI PMC
Ju X., Li J., Zhu M., Lu Z., Lv F., Zhu X., Bie X. Effect of the luxS gene on biofilm formation and antibiotic resistance by Salmonella serovar Dublin. Food Res. Int. 2018;107:385–393. doi: 10.1016/j.foodres.2018.02.039. PubMed DOI
Han X., Bai H., Liu L., Dong H., Liu R., Song J., Ding C., Qi K., Liu H., Yu S. The luxS gene functions in the pathogenesis of avian pathogenic Escherichia coli. Microb. Pathog. 2013;55:21–27. doi: 10.1016/j.micpath.2012.09.008. PubMed DOI