In situ characterisation of biofilms formed by psychrotrophic meat spoilage pseudomonads

References

• Balaban N. 2008. Control of biofilm infections by signal manipulation. Berlin (Germany): Springer Berlin Heidelberg.
   Google Scholar
• Baudin M, Cinquin B, Sclavi B, Pareau D, Lopes F. 2017. Understanding the fundamental mechanisms of biofilms development and dispersal: BIAM (Biofilm intensity and architecture measurement), a new tool for studying biofilms as a function of their architecture and fluorescence intensity. J Microbiol Methods. 140:47–57. doi:10.1016/j.mimet.2017.06.021
   PubMed Web of Science ®Google Scholar
• Beroz F, Yan J, Meir Y, Sabass B, Stone HA, Bassler BL, Wingreen NS. 2018. Verticalization of bacterial biofilms. Nature Phys. 14:954–960. doi:10.1038/s41567-018-0170-4
   PubMed Web of Science ®Google Scholar
• Carey DN, Knut D, Ned SW, Bonnie LB. 2015. Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J. 9:1700–1709.
   PubMed Web of Science ®Google Scholar
• Casaburi A, Piombino P, Nychas G-J, Villani F, Ercolini D. 2015. Bacterial populations and the volatilome associated to meat spoilage. Food Microbiol. 45:83–102. doi:10.1016/j.fm.2014.02.002
   PubMed Web of Science ®Google Scholar
• Champomier-Vergès MC, Stintzi A, Meyer JM. 1996. Acquisition of iron by the non-siderophore-producing Pseudomonas fragi. Int J Microbiol. 142:1191–1199.
   Google Scholar
• Chen W, Hu H, Zhang C, Huang F, Zhang D, Zhang H. 2017. Adaptation response of Pseudomonas fragi on refrigerated solid matrix to a moderate electric field. BMC Microbiol. 17:32. doi:10.1186/s12866-017-0945-2
   PubMed Web of Science ®Google Scholar
• Corry JEL. 2006. Microbiological analysis of red meat, poultry and eggs: Spoilage organisms of red meat and poultry. Cambridge: Woodhead Publishing.
   Google Scholar
• Das T, Sharma PK, Busscher HJ, van der Mei HC, Krom BP. 2010. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol. 76:3405–3408. doi:10.1128/AEM.03119-09
   PubMed Web of Science ®Google Scholar
• Delaquis PJ, Gariépy C, Montpetit D. 1992. Confocal scanning laser microscopy of porcine muscle colonized by meat spoilage bacteria. Int J Food Microbiol. 9:147–153. doi:10.1016/0740-0020(92)80021-U
   Google Scholar
• Delaquis PJ, McCurdy AR. 1990. Colonization of beef muscle surfaces by Pseudomonas fluorescens and Pseudomonas fragi. J Food Sci. 4:898–902.
   Google Scholar
• Diane M, Scott AR, Nicolas B, Peter DS, Staffan K. 2011. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol. 10:39–50.
   PubMed Web of Science ®Google Scholar
• Drescher K, Dunkel J, Nadell CD, van Teeffelen S, Grnja I, Wingreen NS, Stone HA, Bassler BL. 2016. Architectural transitions in Vibrio cholerae biofilms at single-cell resolution. Proc Natl Acad Sci USA. 113:E2066–E2072. doi:10.1073/pnas.1601702113
   PubMed Web of Science ®Google Scholar
• Drescher K, Shen Y, Bassler BL, Stone HA. 2013. Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc Natl Acad Sci USA. 110:4345–4350. doi:10.1073/pnas.1300321110
   PubMed Web of Science ®Google Scholar
• Drosinos E, Board RG. 1995. Microbial and physiochemical attributes of minced lamb–sources of contamination with pseudomonads. Int J Food Microbiol. 12:189–197. doi:10.1016/S0740-0020(95)80097-2
   Google Scholar
• Duskova M, Kamenik J, Karpiskova R. 2013. Weissella viridescens in meat products–a review. Acta Vet Brno. 82:237–241. doi:10.2754/avb201382030237
   Web of Science ®Google Scholar
• Dykes GA, Cloete TE, Von Holy A. 1994. Identification of Leuconostoc species associated with the spoilage of vacuum-packaged Vienna sausages by DNA-DNA hybridization. Food Microbiol. 11:271–274. doi:10.1006/fmic.1994.1030
   Web of Science ®Google Scholar
• EFSA Panel on Biological Hazards (BIOHAZ). 2016. Growth of spoilage bacteria during storage and transport of meat. EFSA J. 14(6):376–414. doi:10.2903/j.efsa.2016.4523
   PubMed Web of Science ®Google Scholar
• Ercolini D, Russo F, Blaiotta G, Pepe O, Mauriello G, Villani F. 2007. Simultaneous detection of Pseudomonas fragi, P. lundensis, and P. putida from meat by use of a multiplex PCR sssay targeting the carA gene. J Appl Environ Microbiol. 73:2354–2359. doi:10.1128/AEM.02603-06
   PubMed Web of Science ®Google Scholar
• Ercolini D, Russo F, Torrieri E, Masi P, Villani F. 2006. Changes in the spoilage related microbiota of beef during refrigerated storage under different packaging conditions. J Appl Environ Microbiol. 72:4663–4671. doi:10.1128/AEM.00468-06
   PubMed Web of Science ®Google Scholar
• Fagerlind MG, Webb JS, Barraud N, McDougald D, Jansson A, Nilsson P, Harlén M, Kjelleberg S, Rice SA. 2012. Dynamic modelling of cell death during biofilm development. J Theor Biol. 295:23–36. doi:10.1016/j.jtbi.2011.10.007
   PubMed Web of Science ®Google Scholar
• Ferrocino I, Ercolini D, Villani F, Moorhead SM, Griffiths MW. 2009. Pseudomonas fragi strains isolated from meat do not produce N-acyl homoserine lactones as signal molecules. J Food Prot. 72:2597–2601. doi:10.4315/0362-028X-72.12.2597
   PubMed Web of Science ®Google Scholar
• Flemming H-C, Wingender J, Szewzyk U, SpringerLink (Online service). 2011. Biofilm highlights. 1st ed. Berlin (Germany): Springer Berlin Heidelberg.
   Google Scholar
• Giaouris E, Heir E, Hébraud M, Chorianopoulos N, Langsrud S, Møretrø T, Habimana O, Desvaux M, Renier S, Nychas G-J. 2014. Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Sci. 97:298–309. doi:10.1016/j.meatsci.2013.05.023
   PubMed Web of Science ®Google Scholar
• Gill CO, Penney N. 1977. Penetration of bacteria into meat. Appl Environ Microbiol. 33:1284–1286.
   PubMed Web of Science ®Google Scholar
• Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker‐Nielsen T. 2005. Characterization of starvation‐induced dispersion in Pseudomonas putida biofilms. J Appl Environ Microbiol. 7:894–904.
   Google Scholar
• Habimana O, Heir E, Langsrud S, Asli AW, Moretro T. 2010. Enhanced surface colonization by Escherichia coli O157:H7 in biofilms formed by an Acinetobacter calcoaceticus isolate from meat-processing environments. J Appl Environ Microbiol. 76:4557–4559. doi:10.1128/AEM.02707-09
   PubMed Web of Science ®Google Scholar
• Hasegawa T, Pearson AM, Price JF, Rampton JH, Lechowich RV. 1970. Effect of microbial microbial growth upon sarcoplasmic and urea soulble proteins from muscle. J Food Sci. 35:720–724. doi:10.1111/j.1365-2621.1970.tb01979.x
   Web of Science ®Google Scholar
• Heydorn A, Nielsen A, Hentzer M, Sternberg C, Givskov M, Ersboell B, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Int J Microbiol. 146:2395–2407.
   Google Scholar
• Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR, Albers S-V. 2015. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. Microbiol Rev. 39:649–669.
   Google Scholar
• Jay JM, Vilai JP, Hughes ME. 2003. Profile and activity of the bacterial biota of ground beef held from freshness to spoilage at 5–7 °C. Int J Food Microbiol. 81:105–111. doi:10.1016/S0168-1605(02)00189-7
   PubMed Web of Science ®Google Scholar
• Jin X, Anderson TH, Dongyeop K, Domenick TZ, Hyun K, Geelsu H. 2017. Biofilm three-dimensional architecture influences in situ pH distribution pattern on the human enamel surface. Int J Oral Sci. 9:74–79.
   PubMed Web of Science ®Google Scholar
• Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. 2010. D-amino acids trigger biofilm disassembly. Science. 328:627–629. doi:10.1126/science.1188628
   PubMed Web of Science ®Google Scholar
• Lebert I, Begot C, Lebert A. 1998. Growth of Pseudomonas fluorescens and Pseudomonas fragi in a meat medium as affected by pH (5.8–7.0), water activity (0.97–1.00) and temperature (7–25 °C). Int J Food Microbiol. 39:53–60. doi:10.1016/S0168-1605(97)00116-5
   PubMed Web of Science ®Google Scholar
• Mackey BM, Derrick CM. 1979. Contamination of the deep tissues of carcasses by bacteria present on the slaughter instruments or in the gut. J Appl Bacteriol. 46:355–366. doi:10.1111/j.1365-2672.1979.tb00832.x
   PubMedGoogle Scholar
• Mann EE, Wozniak DJ. 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev. 36:893–916. doi:10.1111/j.1574-6976.2011.00322.x
   PubMed Web of Science ®Google Scholar
• Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S, Nychas G-J, Skandamis PN, Tassou CC, Koutsoumanis KP. 2008. Meat spoilage during distribution. Meat Sci. 78:77–89.
   PubMed Web of Science ®Google Scholar
• Molin G, Trenstrom A, Ursing J. 1986. Pseudomonas lundensis, a new bacterial species isolated from meat. Int J Syst Evol Microbiol. 36:339–342.
   Google Scholar
• Nychas GJE, Skandamis PN, Tassou CC, Koutsoumanis KP. 2008. Meat spoilage during distribution. Meat Sci. 78(1):77–89. doi:10.1016/j.meatsci.2007.06.020.
   PubMed Web of Science ®Google Scholar
• Okshevsky M, Meyer RL. 2014. Evaluation of fluorescent stains for visualizing extracellular DNA in biofilms. J Microbiol Methods. 105:102–104. doi:10.1016/j.mimet.2014.07.010
   PubMed Web of Science ®Google Scholar
• Okshevsky M, Meyer RL. 2015. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol. 41:341–352. doi:10.3109/1040841X.2013.841639
   PubMed Web of Science ®Google Scholar
• Puga CH, Dahdouh E, SanJose C, Orgaz B. 2018. Listeria monocytogenes colonizes Pseudomonas fluorescens biofilms and induces matrix over-production. Front Microbiol. 9:1706. doi:10.3389/fmicb.2018.01706
   PubMed Web of Science ®Google Scholar
• Purevdorj-Gage B, Costerton WJ, Stoodley P. 2005. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Int J Microbiol. 151:1569–1576.
   Google Scholar
• Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS. 2007. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189:4223–4233. doi:10.1128/JB.00107-07
   PubMed Web of Science ®Google Scholar
• Roszak DB, Colwell RR. 1987. Survival strategies of bacteria in the natural environment. Microbiol Mol Biol Rev. 51:365–379.
   Google Scholar
• Silagyi K, Kim S-H, Lo YM, Wei C-I. 2009. Production of biofilm and quorum sensing by Escherichia coli O157:H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiol. 26:514–519. doi:10.1016/j.fm.2009.03.004
   PubMed Web of Science ®Google Scholar
• Stanborough T, Fegan N, Powell SM, Singh T, Tamplin M, Chandry PS. 2018. Genomic and metabolic characterization of spoilage-associated Pseudomonas species. Int J Food Microbiol. 268:61–72. doi:10.1016/j.ijfoodmicro.2018.01.005
   PubMed Web of Science ®Google Scholar
• Swearingen MC, Mehta A, Mehta A, Nistico L, Hill PJ, Falzarano AR, Wozniak DJ, Hall-Stoodley L, Stoodley P, Bjarnsholt T. 2016. A novel technique using potassium permanganate and reflectance confocal microscopy to image biofilm extracellular polymeric matrix reveals non-eDNA networks in Pseudomonas aeruginosa biofilms. Pathog Dis. 9:74–79.
   Google Scholar
• Trueba F, Spronsen E, Traas J, Woldringh C. 1982. Effects of temperature on the size and shape of Escherichia coli cells. Arch Microbiol. 131:235–240. doi:10.1007/BF00405885
   PubMed Web of Science ®Google Scholar
• Valentini M, Filloux A. 2016. Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem. 291:12547–12555. doi:10.1074/jbc.R115.711507
   PubMed Web of Science ®Google Scholar
• Volfson D, Cookson S, Hasty J, Tsimring LS. 2008. Biomechanical ordering of dense cell populations. Proc Natl Acad Sci USA. 105:15346–15351. doi:10.1073/pnas.0706805105
   PubMed Web of Science ®Google Scholar
• Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science. 295:1487. doi:10.1126/science.295.5559.1487
   PubMed Web of Science ®Google Scholar
• Yada RY, Skura BJ. 1982. Scanning electron microscope study of Pseudomonas fragi on intact and sarcoplasm-depleted bovine longissimus dorsi muscle. J Appl Environ Microbiol. 43:905–915.
   PubMed Web of Science ®Google Scholar
• Yan J, Nadell C, Stone H, Wingreen N, Bassler B. 2017. Extracellular-matrix-mediated osmotic pressure drives Vibrio cholerae biofilm expansion and cheater exclusion. Nat Commun. 8:327–327. doi:10.1038/s41467-017-00401-1
   PubMed Web of Science ®Google Scholar
• Yan J, Sharo AG, Stone HA, Wingreen NS, Bassler BL. 2016. Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging. Proc Natl Acad Sci USA. 113:5337–5343.
   Web of Science ®Google Scholar