Abstract
This study aimed to determine the impact of bacteria from a beef plant conveyor belt on the biofilm formation of Salmonella in dual-species cultures. Beef plant isolates (50) including 18 Gram-negative aerobes (GNA), 8 Gram-positive aerobes (GPA), 5 lactic acid bacteria (LAB), 9 Enterobacteriaceae (EB), and 10 generic Escherichia coli (GEC) were included for developing biofilms in mono- and co-culture with S. Typhimurium at 15 °C for 6 days. Five selected cultures in planktonic form and in biofilms were tested for susceptibility to two commonly used sanitizers (i.e. E-San and Perox-E Plus). In mono-cultures, ≥ 80, 67, 61, 20, and 13% of GEC, EB, GNA, LAB, and GPA, respectively, developed measurable biofilms after 2 days, while all co-culture pairings with S. Typhimurium achieved some level of biofilm production. The predominant effect of EB and only effect of GEC strains on the biofilm formation of S. Typhimurium was antagonistic, while that of Gram-positive bacteria was synergistic, with the effect being more prominent on day 6. The effect was highly variable for the GNA isolates. Six aerobic isolates that formed moderate/strong biofilms by day 2 greatly boosted the co-culture biofilm formation. Seven Gram-negative bacteria were antagonistic against the biofilm formation of the co-cultures. Both sanitizers completely inactivated the selected planktonic cultures, but were largely ineffective against biofilms. In conclusion, all beef plant isolates assessed formed biofilms when paired with S. Typhimurium. Aerobic biofilm formers may create a more favorable condition for Salmonella biofilm formation, while some beef plant isolates have potential as a biocontrol strategy for Salmonella biofilms.
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References
World Health Organization (2015) WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. https://www.who.int/foodsafety/publications/foodborne_disease/fergreport/en/. Accessed June 2018
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50:882–889. https://doi.org/10.1086/650733
Scharff RL (2012) Economic burden from health losses due to foodborne illness in the United States. J. Food Prot. 75:123–131. https://doi.org/10.4315/0362-028X.JFP-11-058
Thomas MK, Murray R, Flockhart L, Pintar K, Fazil A, Nesbitt A, Marshall B, Tataryn J, Pollari F (2015) Estimates of foodborne illness–related hospitalizations and deaths in Canada for 30 specified pathogens and unspecified agents. Foodborne Pathog. Dis. 12:820–827. https://doi.org/10.1089/fpd.2015.1966
Foley SL, Lynne AM (2008) Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J. Anim. Sci. 86:E173–E187. https://doi.org/10.2527/jas.2007-0447
EFSA (2013) Foodborne zoonotic diseases. Salmonella. https://www.efsa.europa.eu/en/topics/topic/salmonella. Accessed 10 Oct 2018
Bélanger P, Tanguay F, Hamel M, Phypers M (2015) An overview of foodborne outbreaks in Canada reported through outbreak summaries: 2008-2014. Can. Commun. Dis. Rep. 41:254–262
Hall-Stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell. Microbiol. 11:1034–1043. https://doi.org/10.1111/j.1462-5822.2009.01323.x
Van Houdt R, Michiels CW (2005) Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 156:626–633. https://doi.org/10.1016/j.resmic.2005.02.005
Wang R, Bono JL, Kalchayanand N, Shackelford S, Harhay DM (2012) Biofilm formation by Shiga toxin-producing Escherichia coli O157:H7 and non-O157 strains and their tolerance to sanitizers commonly used in the food processing environment. J. Food Prot. 75:1418–1428. https://doi.org/10.4315/0362-028X.JFP-11-427
Runkel S, Wells HC, Rowley G (2013) Living with stress: A lesson from the enteric pathogen Salmonella enterica. Adv. Appl. Microbiol. 83:87–144. https://doi.org/10.1016/B978-0-12-407678-5.00003-9
Peng D (2016) Biofilm formation of Salmonella. In: Dhanasekaran D, Thajuddin N (eds) Microbial biofilms - importance and applications. InTech, Rijeka, pp 231–249
Stepanović S, Ćirković I, Ranin L, Svabić-Vlahović M (2004) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett. Appl. Microbiol. 38:428–432. https://doi.org/10.1111/j.1472-765X.2004.01513.x
Joseph B, Otta S, Karunasagar I, Karunasagar I (2001) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64:367–372. https://doi.org/10.1016/S0168-1605(00)00466-9
Sinde E, Carballo J (2000) Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiol. 17:439–447. https://doi.org/10.1006/fmic.2000.0339
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. https://doi.org/10.1016/j.meatsci.2013.05.023
Wang R, Schmidt JW, Harhay DM, Bosilevac JM, King DA, Arthur TM (2017) Biofilm formation, antimicrobial resistance, and sanitizer tolerance of Salmonella enterica strains isolated from beef trim. Foodborne Pathog. Dis. 14:687–695. https://doi.org/10.1089/fpd.2017.2319
Chuah L-O, Shamila Syuhada A-K, Mohamad Suhaimi I, Farah Hanim T, Rusul G (2018) Genetic relatedness, antimicrobial resistance and biofilm formation of Salmonella isolated from naturally contaminated poultry and their processing environment in northern Malaysia. Food Res. Int. 105:743–751. https://doi.org/10.1016/j.foodres.2017.11.066
Yang X, Wang H, He A, Tran F (2018) Biofilm formation and susceptibility to biocides of recurring and transient Escherichia coli isolated from meat fabrication equipment. Food Control. https://doi.org/10.1016/j.foodcont.2018.02.050
Wang R, Kalchayanand N, King DA, Luedtke BE, Bosilevac JM, Arthur TM (2014) Biofilm formation and sanitizer resistance of Escherichia coli O157:H7 strains isolated from "high event period" meat contamination. J. Food Prot. 77:1982–1987. https://doi.org/10.4315/0362-028X.JFP-14-253
Wang H, He A, Yang X (2018) Dynamics of microflora on conveyor belts in a beef fabrication facility during sanitation. Food Control 85:42–47. https://doi.org/10.1016/j.foodcont.2017.09.017
Møretrø T, Langsrud S, Heir E (2013) Bacteria on meat abattoir process surfaces after sanitation: characterisation of survival properties of Listeria monocytogenes and the commensal bacterial flora. Adv. Microbiol. 3:255–264. https://doi.org/10.4236/aim.2013.33037
Giaouris ED, Heir E, Desvaux M, Hébraud M, Møretrø T, Langsrud S, Doulgeraki A, Nychas G-J, Kacániová M, Czaczyk K, Ölmez H, Simões M (2015) Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front. Microbiol. 6. https://doi.org/10.3389/fmicb.2015.00841
Marouani-Gadri N, Augier G, Carpentier B (2009) Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection — influence of isolated strains on biofilm formation by Sakaï and EDL 933 E. coli O157:H7. Int. J. Food Microbiol. 133:62–67. https://doi.org/10.1016/j.ijfoodmicro.2009.04.028
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons Ltd., Hoboken
Visvalingam J, Ells TC, Yang X (2017) Impact of persistent and non-persistent generic Escherichia coli and Salmonella sp. recovered from a beef packing plant on biofilm formation by E. coli O157. J. Appl. Microbiol. 123:1512–1521. https://doi.org/10.1111/jam.13591
Yang X, Wang H, He A, Tran F (2017) Microbial efficacy and impact on the population of Escherichia coli of a routine sanitation process for the fabrication facility of a beef packing plant. Food Control 71:353–357. https://doi.org/10.1016/j.foodcont.2016.07.016
Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, ĆIrković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891–899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
Wakisaka Y, KoizuMI K, Nishimoto Y (1982) A preferential isolation procedure for asporogenous gram-positive bacteria. J. Antibiot. 35:441–449. https://doi.org/10.7164/antibiotics.35.441
Ren D, Madsen JS, Sørensen SJ, Burmølle M (2014) High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J. 9:81–89. https://doi.org/10.1038/ismej.2014.96
Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 22:84–91. https://doi.org/10.1016/j.tim.2013.12.004
Soni KA, Oladunjoye A, Nannapaneni R, Schilling MW, Silva JL, Mikel B, Bailey RH (2013) Inhibition and inactivation of Salmonella typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol. J. Food Prot. 76:205–212. https://doi.org/10.4315/0362-028x.Jfp-12-196
Vidal De Oliveira DC, Fernandes Júnior A, Kaneno R, Silva MG, Araújo Júnior JP, Cirone Silva NC, Mores Rall VL (2014) Ability of Salmonella spp. to produce biofilm is dependent on temperature and surface material. Foodborne Pathog. Dis. 11:478–483. https://doi.org/10.1089/fpd.2013.1710
Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N (2016) Environmental factors that shape biofilm formation. Biosci. Biotechnol. Biochem. 80:7–12. https://doi.org/10.1080/09168451.2015.1058701
Leriche V, Carpentier B (1995) Viable but nonculturable salmonella typhimurium in single- and binary-species biofilms in response to chlorine treatment. J. Food Prot. 58:1186–1191. https://doi.org/10.4315/0362-028x-58.11.1186
Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F (2011) Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27:1017–1032. https://doi.org/10.1080/08927014.2011.626899
Pang XY, Yang YS, Yuk HG (2017) Biofilm formation and disinfectant resistance of Salmonella sp. in mono- and dual-species with Pseudomonas aeruginosa. J. Appl. Microbiol. 123:651–660. https://doi.org/10.1111/jam.13521
Wang R, Kalchayanand N, Schmidt JW, Harhay DM (2013) Mixed biofilm formation by Shiga toxin–producing Escherichia coli and Salmonella enterica serovar typhimurium enhanced bacterial resistance to sanitization due to extracellular polymeric substances. J. Food Prot. 76:1513–1522. https://doi.org/10.4315/0362-028X.JFP-13-077
Chylkova T, Cadena M, Ferreiro A, Pitesky M (2017) Susceptibility of Salmonella biofilm and planktonic bacteria to common disinfectant agents used in poultry processing. J. Food Prot. 80:1072–1079. https://doi.org/10.4315/0362-028X.JFP-16-393
Aliyar F, Ifigenia G, SJ N (2013) Biofilm formation of O157 and non-O157 Shiga toxin-producing Escherichia coli and multidrug-resistant and susceptible Salmonella typhimurium and Newport and their inactivation by sanitizers. J. Food Sci. 78:M880–M886. https://doi.org/10.1111/1750-3841.12123
Røder HL, Raghupathi PK, Herschend J, Brejnrod A, Knøchel S, Sørensen SJ, Burmølle M (2015) Interspecies interactions result in enhanced biofilm formation by co-cultures of bacteria isolated from a food processing environment. Food Microbiol. 51:18–24. https://doi.org/10.1016/j.fm.2015.04.008
Pang X, Yuk H-G (2018) Effect of Pseudomonas aeruginosa on the sanitizer sensitivity of Salmonella Enteritidis biofilm cells in chicken juice. Food Control 86:59–65. https://doi.org/10.1016/j.foodcont.2017.11.012
Nijland R, Hall MJ, Burgess JG (2010) Dispersal of biofilms by secreted, matrix degrading bacterial DNase. PLoS One 5:e15668. https://doi.org/10.1371/journal.pone.0015668
Ramasubbu N, Thomas LM, Ragunath C, Kaplan JB (2005) Structural analysis of dispersin B, a biofilm-releasing glycoside hydrolase from the periodontopathogen Actinobacillus actinomycetemcomitans. J. Mol. Biol. 349:475–486. https://doi.org/10.1016/j.jmb.2005.03.082
Gerstel U, Park C, Römling U (2003) Complex regulation of csgD promoter activity by global regulatory proteins. Mol. Microbiol. 49:639–654. https://doi.org/10.1046/j.1365-2958.2003.03594.x
Chorianopoulos NG, Giaouris ED, Kourkoutas Y, Nychas G-JE (2010) Inhibition of the early stage of Salmonella enterica serovar Enteritidis biofilm development on stainless steel by cell-free supernatant of a Hafnia alvei culture. Appl. Environ. Microbiol. 76:2018–2022. https://doi.org/10.1128/aem.02093-09
Jahid IK, Han NR, Srey S, Ha S-D (2014) Competitive interactions inside mixed-culture biofilms of Salmonella typhimurium and cultivable indigenous microorganisms on lettuce enhance microbial resistance of their sessile cells to ultraviolet C (UV-C) irradiation. Food Res. Int. 55:445–454. https://doi.org/10.1016/j.foodres.2013.11.042
Makovcova J, Babak V, Kulich P, Masek J, Slany M, Cincarova L (2017) Dynamics of mono- and dual-species biofilm formation and interactions between Staphylococcus aureus and gram-negative bacteria. Microb. Biotechnol. 10:819–832. https://doi.org/10.1111/1751-7915.12705
Chen D, Zhao T, Doyle MP (2015) Single- and mixed-species biofilm formation by Escherichia coli O157:H7 and Salmonella, and their sensitivity to levulinic acid plus sodium dodecyl sulfate. Food Control 57:48–53. https://doi.org/10.1016/j.foodcont.2015.04.006
Esteves CLC, Jones BD, Clegg S (2005) Biofilm formation by Salmonella enterica Serovar typhimurium and Escherichia coli on epithelial cells following mixed inoculations. Infect. Immun. 73:5198–5203. https://doi.org/10.1128/iai.73.8.5198-5203.2005
Habimana O, Møretrø T, Langsrud S, Vestby LK, Nesse LL, Heir E (2010) Micro ecosystems from feed industry surfaces: a survival and biofilm study of Salmonella versus host resident flora strains. BMC Vet. Res. 6:48. https://doi.org/10.1186/1746-6148-6-48
Jones K, Bradshaw SB (1997) Synergism in biofilm formation between Salmonella enteritidis and a nitrogen-fixing strain of Klebsiella pneumoniae. J. Appl. Microbiol. 82:663–668. https://doi.org/10.1111/j.1365-2672.1997.tb03600.x
Gkana EN, Giaouris ED, Doulgeraki AI, Kathariou S, Nychas G-JE (2017) Biofilm formation by Salmonella typhimurium and Staphylococcus aureus on stainless steel under either mono- or dual-species multi-strain conditions and resistance of sessile communities to sub-lethal chemical disinfection. Food Control 73:838–846. https://doi.org/10.1016/j.foodcont.2016.09.038
Acknowledgements
Technical assistance provided by Danielle St. Jean and Anita Gosh was gratefully acknowledged.
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Funding for this study was provided by Agriculture and Agri-Food Canada through A-base funding (A-1637 and A-1603).
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Visvalingam, J., Zhang, P., Ells, T.C. et al. Dynamics of Biofilm Formation by Salmonella Typhimurium and Beef Processing Plant Bacteria in Mono- and Dual-Species Cultures. Microb Ecol 78, 375–387 (2019). https://doi.org/10.1007/s00248-018-1304-z
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DOI: https://doi.org/10.1007/s00248-018-1304-z