Abstract
Biofilms can constitute permanent threats to food safety and public health. Bacteria and viruses lodged in biofilm can escape cleaning and sanitizing agents. The aim of this study was to compare Pseudomonas aeruginosa developing and mature biofilms produced on agri-food surfaces in terms of interaction with murine norovirus. Whether they were mature or still developing the biofilms apparently accumulated murine norovirus in large numbers after 24 h of contact with medium which viral titer was 2.6 × 104 pfu ml−1 (≈ 8 log10 genome copies ml−1). This appeared unrelated to surfaces’ nature and bacterial viable count but related to polysaccharide and protein contents. Virus releases may also occur mainly in connection with P. aeruginosa biofilm dispersal systems. These findings suggest that the effectiveness of surface cleaning agents and procedures for reducing the risks of biofilms-related viral contaminations need to be re-evaluated in relation with biofilm components. However, more repetitions and further in-depth specific studies are needed for confirmation of these findings and more clarifications on virus-biofilm interaction phenomenon.
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Abbreviations
- VLPs:
-
Virus-like particles
- FCV:
-
Feline calicivirus
References
Ainsworth, C. (1994). Isolation of R N A from floral tissue of Rumex acetosa (Sorrel). Plant Molecular Biology Reporter, 12(3), 198–199.
Allesen-Holm, M., Barken, K. B., Yang, L., Klausen, M., Webb, J. S., Kjelleberg, S., Molin, S., Givskov, M., & Tolker-Nielsen, T. (2006). A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Molecular Microbiology, 59(4), 1114–1128. https://doi.org/10.1111/j.1365-2958.2005.05008.x
Anwar, H., Dasgupta, M. K., & Costerton, J. W. (1990). Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrobial Agents and Chemotherapy, 34(11), 2043–2046. https://doi.org/10.1128/AAC.34.11.2043
ASTM. (2013). ASTM E2562-12 standard test method for quantification of Pseudomonas aeruginosas biofilm grown with high shaer and continuous flow using CDC biofilm reactor (pp. 1–2). West Conshohocken: ASTM international.
Byrd, M. S., Sadovskaya, I., Vinogradov, E., Lu, H., April, B., Richardson, S. H., Ma, L., Ralston, B., Parsek, M. R., Erin, M., Lam, J. S., & Wozniak, D. J. (2009). Genetic and biochemical analyses of the pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Molecular Microbiology, 73(4), 622–638. https://doi.org/10.1111/j.1365-2958.2009.06795.x
Carpentier, B., & Cerf, O. (1993). Biofilms and their consequences, with particular reference to hygiene in the food industry. Journal of Applied Bacteriology, 75, 499–511. https://doi.org/10.1111/j.1365-2672.1993.tb01587.x
Chew, S. C., Kundukad, B., Seviour, T., Van der Maarel, J. R., Yang, L., Rice, S. A., Doyle, P., & Kjelleberg, S. (2014). Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides. Mbio, 5(4), e01536-e11514. https://doi.org/10.1128/mBio.01536-14
Das, T., Ibugo, A. I., Klare, W., & Manefield, M. (2016). Role of pyocyanin and extracellular DNA in facilitating Pseudomonas aeruginosa biofilm formation. Microbial biofilm-importance and applications (p. 26). London: Intech Open.
Davey, M. E., Caiazza, N. C., & O’Toole, G. A. (2003). Rhamnolipid surfactant production affects bio lm architecture in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 185(3), 1027–1036. https://doi.org/10.1128/JB.185.3.1027
Donlan, R. M., Piede, J. A., Heyes, C. D., Sanii, L., Murga, R., Edmonds, P., El-Sayed, I., & El-Sayed, M. A. (2004). Model system for growing and quantifying. Applied and Environmental Microbiology, 70(8), 4980–4988. https://doi.org/10.1128/AEM.70.8.4980
Feng, K., Divers, E., Ma, Y., & Li, J. (2011). Inactivation of human norovirus surrogate, human norovirus virus-like particles, and vesicular stomatitis virus by gamma irradiation. Applied and Environmental Microbiology, 77(10), 3507–3517.
Girard, M., Ngazoa, S., Mattison, K., & Jean, J. (2010). Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. Journal of Food Protection, 73(2), 400–404.
Hunter, R. C., & Beveridge, T. J. (2005). Application of a pH-sensitive fluoroprobe (C-SNARF-4) for pH microenvironment analysis in Pseudomonas aeruginosa biofilms. Applied and Environmental Microbiology, 71(5), 2501–2510. https://doi.org/10.1128/AEM.71.5.2501
Jennings, L. K., Storek, K. M., Ledvina, H. E., Coulon, C., Marmont, L. S., Sadovskaya, I., Secor, P. R., Tseng, B. S., Scian, M., Filloux, A., Wozniak, D. J., Howell, P. L., & Parsek, M. R. (2015). Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proceedings of the National Academy of Sciences, 112(36), 11353–11358. https://doi.org/10.1073/pnas.1503058112
Khalifa, A. B. H., Moissenet, D., Thien, H. V., & Khedher, M. (2011). Les facteurs de virulence de pseudomonas aeruginosa: Mecanismes et modes de regulations. Annales De Biologie Clinique (paris), 69(4), 393–403. https://doi.org/10.1684/abc.2011.0589
Kilcoyne, M., Gerlach, J. Q., Farrell, M. P., Bhavanandan, V. P., & Joshi, L. (2011). Periodic acid-Schiff’s reagent assay for carbohydrates in a microtiter plate format. Analytical Biochemistry, 416(1), 18–26. https://doi.org/10.1016/j.ab.2011.05.006
Kumar, C. G., & Anand, S. (1998). Significance of microbial biofilms in food industry: A review. International Journal of Food Microbiology, 42(1), 9–27. https://doi.org/10.1016/S0168-1605(98)00060-9
Lorowitz, W., Saxton, E., Sondossi, M., & Nakaoka, K. (2005). Integrating statistic with a microbiology laboratory activity. Microbiology Education, 6, 14–19. https://doi.org/10.1128/me.6.1.14-19.2005
Luppens, S. B. I., Reij, M. W., Van, D. R. W. L., Rombouts, F. M., Abee, T., & Van Der, H. R. W. L. (2002). Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Applied and Environment Microbiology, 68(9), 4194–4200. https://doi.org/10.1128/AEM.68.9.4194
Ma, L., Conover, M., Lu, H., Parsek, M. R., Bayles, K., & Wozniak, D. J. (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathogens, 5(3), 1–11. https://doi.org/10.1371/journal.ppat.1000354
Mann, E. E., & Wozniak, D. J. (2015). Pseudomonas biofilm matrix composition and niche biology Ethan. FEMS Microbiology Reviews, 36(4), 893–916. https://doi.org/10.1111/j.1574-6976.2011.00322.x.Pseudomonas
Mittal, R., Aggarwal, S., Sharma, S., Chhibber, S., & Harjai, K. (2009). Urinary tract infections caused by Pseudomonas aeruginosa: A minireview. Journal of Infection and Public Health, 2(3), 101–111. https://doi.org/10.1016/j.jiph.2009.08.003
Oss Van, O. C. J. (2003). Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. Journal of Molecular Biology, 16(2002), 177–190.
Schrader, C., Schielke, A., Ellerbroek, L., & Johne, R. (2012). PCR inhibitors—occurrence, properties and removal. Journal of Applied Microbiology, 113, 1014–1026. https://doi.org/10.1111/j.1365-2672.2012.05384.x
Skraber, S., Helmi, K., Willame, R., Ferréol, M., Gantzer, C., Hoffmann, L., & Cauchie, H. M. (2007). Occurrence and persistence of bacterial and viral faecal indicators in wastewater biofilms. Water Science and Technology, 55(8–9), 377–385. https://doi.org/10.2166/wst.2007.280
Skraber, S., Ogorzaly, L., Helmi, K., Maul, A., Hoffmann, L., Cauchie, H. M., & Gantzer, C. (2009). Occurrence and persistence of enteroviruses, noroviruses and F-specific RNA phages in natural wastewater biofilms. Water Research, 43(19), 4780–4789. https://doi.org/10.1016/j.watres.2009.05.020
Stewart, P., & Costerton, J. W. (2001). Antibiotic resistance of bacteria in biofilms. Lancet, 358, 135–138.
Taube, S., Perry, J. W., Yetming, K., Patel, S. P., Auble, H., Shu, L., Nawar, H. F., Lee, C. H., Connell, T. D., Shayman, J. A., & Wobus, C. E. (2009). Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. Journal of Virology, 83(9) 4092–4101. https://doi.org/10.1128/JVI.02245-08
Taube, S., Perry, J. W., McGreevy, E., Yetming, K., Perkins, C., Henderson, K., & Wobus, C. E. (2012) Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. Journal of Virology, 86(10), 5584–5593. https://doi.org/10.1128/JVI.06854-11
Wingender, J., & Flemming, H. C. (2011). Biofilms in drinking water and their role as reservoir for pathogens. International Journal of Hygiene and Environmental Health, 214(6), 417–423. https://doi.org/10.1016/j.ijheh.2011.05.009
Zhu, Y., Kawai, H., Hashiba, S., Amarasiri, M., Kitajima, M., Okabe, S., & Sano, D. (2020). The effect of GD10a ganglioside-expressing bacterial strains on murine norovirus infectivity. Molecules, 25(18), 4084. https://doi.org/10.3390/molecules25184084
Acknowledgements
The authors thank Mrs. Coralie Goetz and Mr. Eric Jubinville at Université Laval for reviewing the manuscript.
Funding
This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC Grant #262956). There is no cross funding.
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Samandoulgou, I., Vimont, A., Fernandez, B. et al. Murine Norovirus Interaction with Pseudomonas aeruginosa Biofilm in a Dynamic Bioreactor. Food Environ Virol 13, 485–492 (2021). https://doi.org/10.1007/s12560-021-09490-0
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DOI: https://doi.org/10.1007/s12560-021-09490-0