Distribution of extracellular DNA in Listeria monocytogenes biofilm

https://doi.org/10.17221/9/2019-CJFSCitation:Šuláková M., Pazlarová J., Meyer R.L., Demnerová K. (2019): Distribution of extracellular DNA in Listeria monocytogenes biofilm. Czech J. Food Sci., 37: 409-416.
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Extracellular DNA (eDNA) is an abundant matrix component that protects biofilm from environmental stress, facilitate horizontal gene transfer, and serve as a source of nutrients. eDNA is also found in Listeria monocytogenes biofilm, but it is unknown to which extent its importance as a matrix component varies in terms of phylogenetic relatedness. This study aims to determine if these variations exist. Biofilm forming capacity of ten L. monocytogenes strains of different phylogenetic lineages and serotypes was examined using crystal violet assay at 37°C and 22°C. eDNA content was evaluated fluorometrically at 37°C and at 22°C, then the 3D structure of biofilm was studied by confocal laser scanning microscopy (CLSM). Biofilm forming capacity differed significantly between the culturing conditions and was higher at 37°C than at ambient temperature. eDNA signal distribution was found to be influenced by strain and lineage. CLSM images revealed information about spatial distribution in the biofilm. The information about the eDNA spatial organisation in the biofilm contributes to the understanding of the role of eDNA in a biofilm formation.

Boháčová M., Pazlarová J. (2018): Extracellular DNA as
a Target Molecule for Biofilm Disruption. Chemické Listy, 112: 215–221.
Boháčová M., Zdeňková K., Tomáštíková Z., Fuchsová V., Demnerová K., Karpíšková R., Pazlarová J. (2018): Monitoring of resistance genes in Listeria monocytogenes isolates and their presence in the extracellular DNA of biofilms: a case study from the Czech Republic. Folia Microbiologica, 63: 653–664.  https://doi.org/10.1007/s12223-018-0603-6
Boháčová M., Pazlarová J., Fuchsová V., Švehláková T., Demnerová K. (2019): Quantitative evaluation of biofilm extracellular DNA by fluorescence-based techniques. Folia Microbiologica, 64: 567–577.  https://doi.org/10.1007/s12223-019-00681-8
Borucki M.K., Peppin J.D., White D., Call D.R., Loge F. (2003): Variation in biofilm formation among strains of Listeria monocytogenes variation in biofilm formation among strains of Listeria monocytogenes. Applied and Environmental Microbiology, 69: 7336–7342. https://doi.org/10.1128/AEM.69.12.7336-7342.2003
Branda S.S., Vik A., Friedman L., Kolter R. (2005): Biofilms: the matrix revisited. Trends in Microbiology, 13: 20–26.  https://doi.org/10.1016/j.tim.2004.11.006
Carpentier B., Cerf O. (2011): Review-Persistence of Listeria monocytogenes in food industry equipment and premises. International Journal of Food Microbiology, 145: 1–8. https://doi.org/10.1016/j.ijfoodmicro.2011.01.005
Combrouse T., Sadovskaya I., Faille C., Kol O., Guérardel Y., Midelet-Bourdin G. (2013): Quantification of the extracellular matrix of the Listeria monocytogenes biofilms of different phylogenic lineages with optimization of culture conditions. Journal of Applied Microbiology, 114: 1120–1131. https://doi.org/10.1111/jam.12127
Costerton J.W. (1999): Discussion: Introduction to biofilm. International Journal of Antimicrobial Agents, 11: 217–221.  https://doi.org/10.1016/S0924-8579(99)00018-7
de Aldecoa A.L.I., Zafra O., Gonzalez-Pastor J.E. (2017): Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Frontiers in Microbiology, 8: 1–19.
Dell’Anno A., Danovaro R. (2005): Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science, 309: 2179. doi: 10.1126/science.1117475 https://doi.org/10.1126/science.1117475
Desvaux M., Hebraud M. (2006): The protein secretion systems in Listeria: inside out bacterial virulence. FEMS microbiology reviews, 30: 774–805. https://doi.org/10.1111/j.1574-6976.2006.00035.x
Djordjevic D., Wiedmann M., McLandsborough L.A. (2002): Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68: 2950–2958. https://doi.org/10.1128/AEM.68.6.2950-2958.2002
Doghri I., Rodriques S., Bazire, A., Dufour A., Kbar D., Sopena V., Sablé S., Laneluc I. (2015): Marine bacteria from the French Atlantic coast displaying high forming-biofilm abilities and different biofilm 3D architectures. BMC Microbiology, 15: 231–241.  https://doi.org/10.1186/s12866-015-0568-4
Donelli G., Bayston R., Costerton W.B., Shirtliff M.E. (2010): The first European congress on microbial biofilms: EUROBIOFILMS 2009, Rome, Italy, September 2–5, 2009. FEMS Immunology and Medical Microbiology, 59: 223–226. https://doi.org/10.1111/j.1574-695X.2010.00718.x
Farber J.M., Peterkin P.I. (1991): Listeria monocytogenes,
a food-borne pathogen. Microbiology Reviews. 55: 476–511.
Finkel S.E., Kolter R. (2001): DNA as a nutrient novel role for bacterial competence gene homologs. Journal of Bacteriology, 183: 6288–6293.  https://doi.org/10.1128/JB.183.21.6288-6293.2001
Flemming H.C. (2011): The perfect slime. Colloids and surfaces B: Biointerfaces, 86: 251–259. https://doi.org/10.1016/j.colsurfb.2011.04.025
Flemming H.C., Wingender J. (2010): The biofilm matrix. Nature Reviews Microbiology, 8: 623–633. https://doi.org/10.1038/nrmicro2415
Gelbicova T., Karpiskova R. (2012): Outdoor environment as a source of Listeria monocytogenes in food chain. Czech Journal of Food Sciences, 30: 83–88. https://doi.org/10.17221/7/2011-CJFS
Guilbaud M., Piveteau P., Desvaux M., Brisse S., Briandet R. (2015): Exploring the diversity of Listeria monocytogenes biofilm architecture by high-throughput confocal laser scanning microscopy and the predominance of the honeycomb-like morphotype. Applied and Environmental Microbiology, 81: 1804–1810. https://doi.org/10.1128/AEM.03173-14
Heydorn A., Nielsen A.T., Hentzer M., Sternberg C., Givskov M., Ersboll B.K., Molin S. (2000): Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology, 146: 2395–2407. https://doi.org/10.1099/00221287-146-10-2395
Chiang W.C., Nilsson M., Jensen P.O., Hoiby N., Nielsen T.E., Givskov M., Tolker-Nielsen T. (2013): Extracellular DNA shields against aminoglycosides in pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 57: 2352–2361. https://doi.org/10.1128/AAC.00001-13
Izano E.A., Amarante M.A., Kher W.B., Kaplan J.B. (2008): Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Applied and Environmental Microbioly, 74: 470–476. https://doi.org/10.1128/AEM.02073-07
Jakubovics N.S., Shields R.C., Rajarajan N., Burgess J.G. (2013): Life after death: the critical role of extracellular DNA in microbial biofilms. Letteres in Applied Microbiology, 57: 467–475.  https://doi.org/10.1111/lam.12134
Kadam S.R., den Besten H.M.W., van der Veen S., Zwietering M.H., Moezelaar R., Abee T. (2013): Diversity assessment of Listeria monocytogenes biofilm formation: Impact of growth condition, serotype and strain origin. International Journal of Food Microbiology, 165: 259–264. https://doi.org/10.1016/j.ijfoodmicro.2013.05.025
Kokare C.R., Chakraborty S., Khopade A.N., Mahadik K.R. (2009): Biofilm: Importance and applications. Indian Journal of Biotechnology, 8: 159–168.
Nagler M., Insam H., Pietramellara G., Ascher-Jenull J. (2018): Extracellular DNA in natural environments: features, relevance and applications. Applied Microbiology and Biotechnology, 102: 6343–6356. https://doi.org/10.1007/s00253-018-9120-4
Okshevsky M., Meyer R.L. (2013): The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Critical Reviews in Microbiology, 41: 341–352. https://doi.org/10.3109/1040841X.2013.841639
Okshevsky M., Meyer R.L. (2014): Evaluation of fluorescent stains for visualizing extracellular DNA in biofilms. Journal of Microbiological Methods, 105: 102–104.  https://doi.org/10.1016/j.mimet.2014.07.010
Okshevsky M., Meyer R.L. (2015): The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Critical Review in Microbiology, 41: 341–352. https://doi.org/10.3109/1040841X.2013.841639
Okshevsky M., Regina V.R., Meyer R.L. (2015): Extracellular DNA as a target for biofilm control. Current Opinion in Biotechnology, 33: 73–80.  https://doi.org/10.1016/j.copbio.2014.12.002
Orsi R.H., den Bakker H.C., Wiedmann M. (2011): Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. International Journal of Medical Microbiology, 301: 79–96. https://doi.org/10.1016/j.ijmm.2010.05.002
Padovani G.C., Fucio S.B., Ambrosano G.M., Correr-Sobrinho L., Puppin-Rontani R.M. (2015): In situ bacterial accumulation on dental restorative materials. CLSM/COMSTAT analysis. American Journal of Dentistry, 28: 3–8.
Pan Y., Breidt F., Gorski L. (2010): Synergistic effects of sodium chloride, glucose, and temperature on biofilm formation by Listeria monocytogenes serotype 1/2a and 4b strains. Applied and Environmental Microbiology, 76: 1433–1441. https://doi.org/10.1128/AEM.02185-09
Pan Y., Jr F.B., Kathariou S., Breidt F. (2006): Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Applied and Environmental Microbiology, 72: 7711–7717. https://doi.org/10.1128/AEM.01065-06
Powell L.C., Pritchard M.F., Ferguson E.L., Powell K.A., Patel S.U., Rye P.D., Sakellakou S.M., Buurma N.J., Brilliant Ch.D., Copping J.M., Menzies G.E., Lewis P.D., Hill K.E., Thomas D.W. (2018): Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides. NPJ Biofilms Microbiomes, 4: 13. doi:10.1038/s41522-018-0056-3 https://doi.org/10.1038/s41522-018-0056-3
Sutherland I.W. (2001): The biofilm matrix an immobilized but dynamic microbial environment. Trends in Microbiology, 9: 222–227. https://doi.org/10.1016/S0966-842X(01)02012-1
Tang L., Schramm A., Neu T.R., Revsbech N.P., Meyer R.L. (2013): Extracellular DNA in adhesion and biofilm formation of four environmental isolates: a quantitative study. FEMS Microbiology Ecology, 86: 394–403. https://doi.org/10.1111/1574-6941.12168
Vázquez-boland J.A., Kuhn M., Berche P., Chakraborty T., Domi G., González-zorn B., Wehland J. (2001): Listeria pathogenesis and molecular virulence determinants. Clinical Microbiology Reviewes, 14: 584–640. https://doi.org/10.1128/CMR.14.3.584-640.2001
Xavier J.B., Foster K.R. (2007): Cooperation and conflict in microbial biofilms. Proceedings of the National Academy of Sciences of USA, 104: 876–881. https://doi.org/10.1073/pnas.0607651104
Xiao J., Koo H. (2010): Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms. Journal of Applied Microbiology, 108: 2103–2113.
Zetzmann M., Okshevsky M., Endres J., Sedlag A., Caccia N., Auchter M., Waidmann M.S., Desvaux M., Meyer R.L., Riedel U. (2015): DNase-Sensitive and -Resistant Modes of Biofilm Formation by Listeria monocytogenes. Frontiers in Microbiology, 6: 1–11. https://doi.org/10.3389/fmicb.2015.01428
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