Multispecies biofilm formation by the contaminating microbiota in raw milk

References

• Al-Adawi AS, Gaylarde CC, Sunner J, Beech IB. 2016. Transfer of bacteria between stainless steel and chicken meat: a CLSM and DGGE study of biofilms. AIMS Microbiol. 2:340–358. doi:10.3934/microbiol.2016.3.340
   Web of Science ®Google Scholar
• Alvarez-Ordóñez A, Coughlan LM, Briandet R, Cotter PD. 2019. Biofilms in food processing environments: challenges and opportunities. Annu Rev Food Sci Technol. 10:173–195. doi:10.1146/annurev-food-032818-121805
   PubMed Web of Science ®Google Scholar
• Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C. 2014. Jvenn: an interactive Venn diagram viewer. BMC Bioinformatics. 15:293. doi:10.1186/1471-2105-15-293
   PubMed Web of Science ®Google Scholar
• Bharathi P, Bhowmick P, Shekar M, Karunasagar I. 2011. Biofilm formation by pure and mixed culture of Lactobacillus isolates on polystyrene surface in varying nutrient conditions. Biotechnol Bioinforma Bioeng. 1:93–98.
   Google Scholar
• Brasil. 2018. Normative Ruling n° 76 and n° 77, of November 26, 2018. Technical regulation on the collection of refrigerated raw milk and its bulk transport. Official Gazette of the Federative Republic of Brazil, Brasilia, DF, Ministry of Agriculture, Livestock and Supply. p. 9–13.
   Google Scholar
• Brooks JD, Flint SH. 2008. Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol. 43:2163–2176. doi:10.1111/j.1365-2621.2008.01839.x
   Web of Science ®Google Scholar
• Buckling A, Brockhurst MA. 2008. Kin selection and the evolution of virulence. Heredity (Edinb). 100:484–488. doi:10.1038/sj.hdy.6801093
   PubMed Web of Science ®Google Scholar
• Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ. 2014. Interactions in multispecies biofilms: do they actually matter?. Trends Microbiol. 22:84–91. doi:10.1016/j.tim.2013.12.004
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 108:4516–4522. doi:10.1073/pnas.1000080107
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. Isme J. 6:1621–1624. doi:10.1038/ismej.2012.8
   PubMed Web of Science ®Google Scholar
• Cappitelli F, Polo A, Villa F. 2014. Biofilm formation in food processing environments is still poorly understood and controlled. Food Eng Rev. 6:29–42. doi:10.1007/s12393-014-9077-8
   Web of Science ®Google Scholar
• Cherif-Antar A, Moussa–Boudjemâa B, Didouh N, Medjahdi K, Mayo B, Flórez AB. 2016. Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant. Dairy Sci & Technol. 96:27–38. doi:10.1007/s13594-015-0235-4
   Web of Science ®Google Scholar
• Cleto S, Matos S, Kluskens L, Vieira MJ. 2012. Characterization of contaminants from a sanitized milk processing plant. PLoS One. 7:e40189 doi:10.1371/journal.pone.0040189
   PubMed Web of Science ®Google Scholar
• Cole JK, Hutchison JR, Renslow RS, Kim YM, Chrisler WB, Engelmann HE, Dohnalkova AC, Hu D, Metz TO, Fredrickson JK, et al. 2014. Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions. Front Microbiol. 5:109.
   PubMed Web of Science ®Google Scholar
• Coyte KZ, Tabuteau H, Gaffney EA, Foster KR, Durham WM. 2017. Microbial competition in porous environments can select against rapid biofilm growth. Proc Natl Acad Sci Usa. 114:e161–e170. doi:10.1073/pnas.1525228113
   PubMed Web of Science ®Google Scholar
• Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 27:2194–2200. doi:10.1093/bioinformatics/btr381
   PubMed Web of Science ®Google Scholar
• Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 36:990–1004. doi:10.1111/j.1574-6976.2012.00325.x
   PubMed Web of Science ®Google Scholar
• Fabres-Klein MH, Santos MJC, Klein RC, Souza GN, Ribon A. 2015. An association between milk and slime increases biofilm production by bovine Staphylococcus aureus. BMC Vet Res. 11:3. doi:10.1186/s12917-015-0319-7
   PubMed Web of Science ®Google Scholar
• Faille C, Bénézech T, Midelet-Bourdin G, Lequette Y, Clarisse M, Ronse G, Ronse A, Slomianny C. 2014. Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments. Food Microbiol. 40:64–74. doi:10.1016/j.fm.2013.12.004
   PubMed Web of Science ®Google Scholar
• Filipello V, Di Ciccio PA, Colagiorgi A, Tilola M, Romanò A, Vitale N, Losio MN, Luini M, Zanardi E, Ghidini S, et al. 2019. Molecular characterisation and biofilm production in Staphylococcus aureus isolates from the dairy production chain in Northern Italy. Int Dairy J. 91:110–118. doi:10.1016/j.idairyj.2018.10.002
   Web of Science ®Google Scholar
• Filoche SK, Zhu M, Wu CD. 2004. In situ biofilm formation by multi-species oral bacteria under flowing and anaerobic conditions. J Dent Res. 83:802–806. doi:10.1177/154405910408301013
   PubMed Web of Science ®Google Scholar
• Flint S, Palmer J, Bloemen K, Brooks J, Crawford R. 2001. The growth of Bacillus stearothermophilus on stainless steel. J Appl Microbiol. 90:151–157. doi:10.1046/j.1365-2672.2001.01215.x
   PubMed Web of Science ®Google Scholar
• Foster KR, Bell T. 2012. Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol. 22:1845–1850. doi:10.1016/j.cub.2012.08.005
   PubMed Web of Science ®Google Scholar
• Hammer Ø, Harper DAT, Ryan PD. 2001. PAST - Palaeontological STatistics, ver. 1.89. Palae. 4:1–9.
   Google Scholar
• Hantsis-Zacharov E, Halpern M. 2007. Culturable psychrotrophic bacterial communities in raw milk and their proteolytic and lipolytic traits. Appl Environ Microbiol. 73:7162–7168. doi:10.1128/AEM.00866-07
   PubMed Web of Science ®Google Scholar
• Jagmann N, Henke SF, Philipp B. 2015. Cells of Escherichia coli are protected against severe chemical stress by co-habiting cell aggregates formed by Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 99:8285–8294.
   Google Scholar
• Jahid IK, Han N, Zhang CY, Ha SD. 2015. Mixed culture biofilms of Salmonella Typhimurium and cultivable indigenous microorganisms on lettuce show enhanced resistance of their sessile cells to cold oxygen plasma. Food Microbiol. 46:383–394. doi:10.1016/j.fm.2014.08.003
   PubMed Web of Science ®Google Scholar
• Latorre AA, Van Kessel JS, Karns JS, Zurakowski MJ, Pradhan AK, Boor KJ, Jayarao BM, Houser BA, Daugherty CS, Schukken YH. 2010. Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. J Dairy Sci. 93:2792–2802. doi:10.3168/jds.2009-2717
   PubMed Web of Science ®Google Scholar
• Lehman SM, Donlan RM. 2015. Bacteriophage-mediated control of a two-species biofilm formed by microorganisms causing catheter-associated urinary tract infections in an in vitro urinary catheter model. Antimicrob Agents Chemother. 59:1127–1137. doi:10.1128/AAC.03786-14
   PubMed Web of Science ®Google Scholar
• Lopes SP, Ceri H, Azevedo NF, Pereira MO. 2012. Antibiotic resistance of mixed biofilms in cystic fibrosis: impact of emerging microorganisms on treatment of infection. Int J Antimicrob Agents. 40:260–263. doi:10.1016/j.ijantimicag.2012.04.020
   PubMed Web of Science ®Google Scholar
• Machado SG, Silva FL, Bazzolli DMS, Heyndrickx M, Costa PMA, Vanetti M. 2015. Pseudomonas spp. and Serratia liquefaciens as predominant spoilers in cold raw milk. J Food Sci. 80:M1842–M1849. doi:10.1111/1750-3841.12957
   PubMed Web of Science ®Google Scholar
• Machado SG, Baglinière F, Marchand S, Coillie EV, Vanetti MCD, Block J, Heyndrickx M. 2017. The biodiversity of the microbiota producing heat-resistant enzymes responsible for spoilage in processed bovine milk and dairy products. Front Microbiol. 8:302.
   PubMed Web of Science ®Google Scholar
• Majed R, Faille C, Kallassy M, Gohar M. 2016. Bacillus cereus Biofilms-Same, Only Different. Front Microbiol. 7:1054
   PubMed Web of Science ®Google Scholar
• Marchand S, Heylen K, Messens W, Coudijzer K, Vos P, Dewettinck K, Herman L, Block J, Heyndrickx M. 2009. Seasonal influence on heat-resistant proteolytic capacity of Pseudomonas lundensis and Pseudomonas fragi, predominant milk spoilers isolated from Belgian raw milk samples. Environ Microbiol. 11:467–482. doi:10.1111/j.1462-2920.2008.01785.x
   PubMed Web of Science ®Google Scholar
• Marcy JA, Pruett WP. 2001. Proteolytic microorganisms. In: Downs FP, Ito K, editors. Compendium of methods for the microbiological examination of foods. 4th ed. Washington, D.C.: APHA; p. 175–181.
   Google Scholar
• Mittelman MW. 1998. Structure and functional characteristics of bacterial biofilms in fluid processing operations. J Dairy Science. 81:2760–2764. doi:10.3168/jds.S0022-0302(98)75833-3
   PubMed Web of Science ®Google Scholar
• Molva C, Sudagidan M, Okuklu B. 2009. Extracellular enzyme production and enterotoxigenic gene profiles of Bacillus cereus and Bacillus thuringiensis strains isolated from cheese in Turkey. Food Control. 20:829–834. doi:10.1016/j.foodcont.2008.10.016
   Web of Science ®Google Scholar
• Moons P, Michiels CW, Aertsen A. 2009. Bacterial interactions in biofilms. Crit Rev Microbiol. 35:157–168. doi:10.1080/10408410902809431
   PubMed Web of Science ®Google Scholar
• Nörnberg M, Mentges ML, Silveira ST, Tondo EĆ, Brandelli A. 2011. A psychrotrophic Burkholderia cepacia strain isolated from refrigerated raw milk showing proteolytic activity and adhesion to stainless steel. J Dairy Res. 78:257–262. doi:10.1017/S002202991100015X
   PubMed Web of Science ®Google Scholar
• Oliver SP, Boor KJ, Murphy SC, Murinda SE. 2009. Food safety hazards associated with consumption of raw milk. Foodborne Pathog Dis. 6:793–806. doi:10.1089/fpd.2009.0302
   PubMed Web of Science ®Google Scholar
• Oulahal-Lagsir N, Martial-Gros A, Bonneau M, Blum LJ. 2003. “Escherichia coli-milk” biofilm removal from stainless steel surfaces: synergism between ultrasonic waves and enzymes. Biofouling. 19:159–168.
   PubMed Web of Science ®Google Scholar
• Palmer RJ, Kazmerzak K, Hansen MC, Kolenbrander PE. 2001. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect Immun. 69:5794–5804. doi:10.1128/IAI.69.9.5794-5804.2001
   PubMed Web of Science ®Google Scholar
• Palmer JS, Flint SH, Schmid J, Brooks JD. 2010. The role of surface charge and hydrophobicity in the attachment of Anoxybacillus flavithermus isolated from milk powder. J Ind Microbiol Biotechnol. 37:1111–1119. doi:10.1007/s10295-010-0758-x
   PubMed Web of Science ®Google Scholar
• Parijs I, Steenackers HP. 2018. Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms. ISME J. 12:2061–2075. doi:10.1038/s41396-018-0146-5
   PubMed Web of Science ®Google Scholar
• Parkar SG, Flint SH, Palmer JS, Brooks JD. 2001. Factors influencing attachment of thermophilic bacilli to stainless steel. J Appl Microbiol. 90:901–908. doi:10.1046/j.1365-2672.2001.01323.x
   PubMed Web of Science ®Google Scholar
• Ponce ADR, Martins ML, Araujo EF, Mantovani HC, Vanetti M. 2012. AiiA quorum-sensing quenching controls proteolytic activity and biofilm formation by Enterobacter cloacae. Curr Microbiol. 65:758–763. doi:10.1007/s00284-012-0226-0
   PubMed Web of Science ®Google Scholar
• Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596.
   PubMed Web of Science ®Google Scholar
• Raats D, Offek M, Minz D, Halpern M. 2011. Molecular analysis of bacterial communities in raw cow milk and the impact of refrigeration on its structure and dynamics. Food Microbiol. 28:465–471. doi:10.1016/j.fm.2010.10.009
   PubMed Web of Science ®Google Scholar
• Rao D, Webb JS, Kjelleberg S. 2006. Microbial colonization and competition on the marine alga Ulva australis. Appl Environ Microbiol. 72:5547–5555. doi:10.1128/AEM.00449-06
   PubMed Web of Science ®Google Scholar
• Rendueles O, Ghigo JM. 2015. Mechanisms of competition in biofilm communities. Microbiol Spectr. 3:1–18.
   Web of Science ®Google Scholar
• Rickard AH, McBain AJ, Ledder RG, Handley PS, Gilbert P. 2003. Coaggregation between freshwater bacteria within biofilm and planktonic communities. FEMS Microbiol Lett. 220:133–140. doi:10.1016/S0378-1097(03)00094-6
   PubMed Web of Science ®Google Scholar
• Røder HL, Sørensen SJ, Burmølle M. 2016. Studying bacterial multispecies biofilms: where to start? Trends Microbiol. 24:503–513. doi:10.1016/j.tim.2016.02.019
   PubMed Web of Science ®Google Scholar
• Ryu JH, Beuchat LR. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl Environ Microbiol. 71:247–254. doi:10.1128/AEM.71.1.247-254.2005
   PubMed Web of Science ®Google Scholar
• Salta M, Wharton JA, Dennington SP, Stoodley P, Stokes KR. 2013. Anti-biofilm performance of three natural products against initial bacterial attachment. Int J Mol Sci. 14:21757–21780. doi:10.3390/ijms141121757
   PubMed Web of Science ®Google Scholar
• Samaržija D, Zamberlin Š, Pogačić T. 2012. Psychrotrophic bacteria and milk and dairy products quality. Mljekarstvo. 62:77–95.
   Web of Science ®Google Scholar
• Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 75:7537–7541. doi:10.1128/AEM.01541-09
   PubMed Web of Science ®Google Scholar
• Sharma M, Anand SK. 2002. Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol. 19:627–636. doi:10.1006/fmic.2002.0472
   Web of Science ®Google Scholar
• Simões M, Simões LC, Vieira MJ. 2009. Species association increases biofilm resistance to chemical and mechanical treatments. Water Res. 43:229–237.
   Google Scholar
• Sørhaug T, Stepaniak L. 1997. Psychrotrophs and their enzymes in milk and dairy products: Quality aspects. Trends Food Sci Technol. 8:35–41. doi:10.1016/S0924-2244(97)01006-6
   Web of Science ®Google Scholar
• Teh KH, Lindsay D, Palmer J, Andrewes P, Bremer P, Flint S. 2014. Proteolysis in ultra-heat-treated skim milk after exposure to multispecies biofilms under conditions modelling a milk tanker. Int J Dairy Technol. 67:176–181. doi:10.1111/1471-0307.12114
   Web of Science ®Google Scholar
• Thiele JH, Chartrain M, Zeikus JG. 1988. Control of interspecies electron flow during anaerobic digestion: role of floc formation in syntrophic methanogenesis. Appl Environ Microbiol. 54:10–19.
   PubMed Web of Science ®Google Scholar
• Viana ES, Campos MEM, Ponce AR, Mantovani HC, Vanetti MCD. 2009. Biofilm formation and acyl homoserine lactone production in Hafnia alvei isolated from raw milk. Biol Res. 42:427–436.
   PubMed Web of Science ®Google Scholar
• Vithanage NR, Bhongir J, Jadhav SR, Ranadheera CS, Palombo EA, Yeager TR, Datta N. 2017. Species-level discrimination of psychrotrophic pathogenic and spoilage gram-negative raw milk isolates using a combined MALDI-TOF MS proteomics-bioinformatics-based approach. J Proteome Res. 16:2188–2203. doi:10.1021/acs.jproteome.6b01046
   PubMed Web of Science ®Google Scholar
• Vlková H, Babák V, Seydlová R, Pavlík I, Schlegelova J. 2008. Biofilms and hygiene on dairy farms and in the dairy industry: sanitation chemical products and their effectiveness on biofilms - a review. Czech J Food Sci. 26:309–323. doi:10.17221/1128-CJFS
   Web of Science ®Google Scholar
• Wang R, Neoh KG, Shi Z, Kang ET, Tambyah PA, Chiong E. 2012. Inhibition of Escherichia coli and Proteus mirabilis adhesion and biofilm formation on medical grade silicone surface. Biotechnol Bioeng. 109:336–345. doi:10.1002/bit.23342
   PubMed Web of Science ®Google Scholar
• Wu MY, Sendamangalam V, Xue Z, Seo Y. 2012. The influence of biofilm structure and total interaction energy on Escherichia coli retention by Pseudomonas aeruginosa biofilm. Biofouling. 28:1119–1128. doi:10.1080/08927014.2012.732070
   PubMed Web of Science ®Google Scholar
• Xu D, Jia R, Li Y, Gu T. 2017. Advances in the treatment of problematic industrial biofilms. World J Microbiol Biotechnol. 33:97. doi:10.1007/s11274-016-2203-4
   PubMed Web of Science ®Google Scholar
• Yuan L, Burmølle M, Sadiq FA, Wang N, He G. 2018. Interspecies variation in biofilm-forming capacity of psychrotrophic bacterial isolates from Chinese raw milk. Food Control. 91:47–57. doi:10.1016/j.foodcont.2018.03.026
   Web of Science ®Google Scholar
• Yuan L, Hansen MF, Røder HL, Wang N, Burmølle M, He G. 2019. Mixed-species biofilms in the food industry: current knowledge and novel control strategies. Crit Rev Food Sci Nutr. 1–17. DOI: doi:10.1080/10408398.2019.1632790
   PubMed Web of Science ®Google Scholar