Isolation and identification of some phenotypic features of Pseudomonas in poultry slaughter line
Subject Areas :
Food Hygiene
H. Jafarzadeh
1
,
H. Mirzaei
2
,
Shahram Hanifian
3
,
افشین Javadi
4
,
J. Shayegh
5
1 - Ph.D. Graduate in Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran
2 - Associate Professor, Department of Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran
3 - Associate Professor, Department of Food Science and Technology, Biotechnology Research Center, Tabriz Branch, Islamic Azad University, Tabriz, Iran
4 - Professor, Department of Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran
5 - Assistant Professor, Department of Veterinary Medicine, Faculty of Veterinary and Agriculture, Shabestar Branch, Islamic Azad University, Shabestar, Iran
Received: 2022-05-27
Accepted : 2022-08-17
Published : 2022-05-22
Keywords:
Pseudomonas,
Phonotypic features,
Poultry slaughterhouse,
Motility pattern,
Biofilm production,
Abstract :
Pseudomonas are among psychrophilic bacteria and have been reported in various studies as the predominant spoilage bacterial in slaughter carcass. The aim of this study was to track Pseudomonas spp. from different stages of the slaughter line, slaughterhouse environment and equipment and drop in the packaging. Characteristics such as pigment production, movement pattern and biofilm formation capability of the isolates were also determined. For this purpose, 108 samples were sampled from three industrial poultry slaughterhouses in Tabriz. According to the results, the highest contamination was detected in the samples of the floors, abdominal cavity of carcass and drip samples, respectively. The lowest contamination was observed in the samples related to drinking water, live chicken breast swab and scalder, respectively. The average movement of the Swimming type was significantly (p ≤ 0.001) higher than the two types of Swarming and Twitching movements. And in terms of pigment production, the dominant color was green. Moreover, most of the isolates were able to form biofilms and about 30% of the isolates had moderate and strong ability to produce biofilms. In conclusion, most of the Pseudomonas spp. contamination occurs through different parts of the slaughter line and also the equipment and environment of the slaughterhouse. Due to the biofilm production capacity of Pseudomonas isolates, the issue of proper and more effective washing and disinfection of the slaughter line and equipment is of particular importance.
References:
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Al-Dughaym, A.M. (2000). Recovery and antibiogram studies of hydrophila and P. fluorescens from naturally and experimentally infected Tilapia fishes. Pakistan Journal of Biological Sciences, 3(12): 2185-2187.
Alhamdani, R.J.M. and Al-Luaibi, Y.Y.Y. (2020). Detection of exoa Nan1 genes, the biofilm production with the effect of oyster shell and two plant extracts on Pseudomonas aeruginosa isolated from burn patient and their surrounding environment. Systematic Reviews in Pharmacy,11(12): 1483-1493.
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Burrows, L.L. (2012) Pseudomonas aeruginosa twitching motility: type IV pili in action. Annual Reviews in Microbiology, 66: 493–520.
Buzby, J.C., Wells, H.F. and Hyman, J. (2014). The estimated amount, value, and calories of postharvest food losses at the retail and consumer levels in the United States. In Economic Information Bulletin, 121: 1-33.
Caldera, L., Franzetti, L., Van Coillie, E., De Vos, P., Stragier, P., De Block, J. et al., (2016). Dentification, enzymatic spoilage characterization and proteolytic activity quantification of Pseudomonas Isolated from different foods. Food Microbiology, 54: 142-153.
Carminati, D.,Bonvini, B., Rossetti, L., Zago, M., Tidona, F. and Giraffa, G. (2019). Investigation on the presence of blue pigment-producing Pseudomonas strains along a production line of fresh mozzarella cheese Journal article: Food Control, 100, 321-328 ref. 34.
Carrascosa, C., Millán, R., Jaber, J.R., Lupiola, P., del Rosario-Quintana, C., Mauricio, C. et al., (2015). Blue pigment in fresh cheese produced by Pseudomonas fluorescens. Food Control, 54: 95-102.
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Chen, S.H., Fegan, N., Kocharunchitt, C., Bowman, J.P., Duffy, L.L. (2020). Changes of the bacterial community diversity on chicken carcasses through an Australian poultry processing line. Food Microbiology, 86:103-350.
Chiesa, F., Lomonaco, S., Nucera, D., Garoglio, D., Dalmasso, A. and Civera, T. (2014). Distribution of Pseudomonas species in a dairy plant affected by occasional blue discoloration. Italian Journal of Food Safety, 3(4): 1722.
Costerton, J. (2001). Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends in Microbiology, 9(2): 50-52.
Cude, W.N., Mooney, J., Tavanaei, A.A., Hadden, M.K., Frank, A.M., Gulvik, C.A et al., (2012). Production of the antimicrobial secondary metabolite indigoidine contributesto435 competitive surface colonization by the marine roseobacter Phaeobacter strain Y4I. Applied and Environmental Microbiology, 78;4771-4780.
Darzins, A. (1993). The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric single-domain response regulator CheY. Journal of Bacteriology, 175: 5934–5944.
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Déziel, E., Comeau, Y., Villemur, (2001). Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. Journal of Bacteriology, 183(4): 1195-1204.
Djordjevic, D., Wiedmann, M., Mclandsborough, L. (2002). Microtiter plate assay for assessment of listeria monocytogens biofilm formation. Applied and Environmental Microbiology, 68(6): 2950-2958.
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Handley, A., Park, S.H., Kim, S.A., Ricke, S. (2018). Microbiome profiles of commercial broilers through evisceration and immersion chilling during poultry slaughter and the identification of potential indicator microorganisms. Frontiers in Microbiology, 9: 1-11.
Jay J.M., Loessner M.J., Golden D.A. (2005). Modern Food M 7th edition. Springer Science, USA.
Keskin, D. and Ekmekçi, S. (2007). Investigation of the incidence of Pseudomonas in foods., Hacettepe Journal of Biology and Chemistry, 35 (3): 181-186.
Martin, N.H., Murphy, S.C., Ralyea, R.D., Wiedmann, M., Boor, K.J. (2011). When cheese gets the blues: Pseudomonas fluorescens as the causative agent of cheese spoilage. Journal of Dairy Science, 94(6): 3176-3183.
Mead G.C. (2005). Food safety control in the poultry industry. Woodhead Publishing Limited, USA. https://www.elsevier.com/books/food-safety-control-in-the-poultry-industry/mead/978-1-85573-954-3.
Muner Otton, L., da Silva Campos, M., Meneghetti, K.L., Corção, G. (2017). Influence of twitching and swarming motilities on biofilm formation in Pseudomonas Archives of Microbiology, 199: 677-682.
Nucera, D.M., Lomonaco, S., Morra, P., Ortoffi, M.F., Giaccone, D., Grassi, M.A. (2016). Dissemination and persistence of Pseudomonas in small-scale dairy farms. Italian Journal of Food Safety, 5(2), 91-94.
Rashid, M. H. and Kornberg, A. (2000). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 97(9): 4885–4890.
Reverchon, S., Rouanet, C., Expert, D. and Nasser, W. (2002). Characterization of indigoidine biosynthetic genes in erwinia chrysanthemi and role of this blue pigment in pathogenicity. Journal of Bacteriology, 184(3): 654–665.
Rossi, C., Serio, A., Chaves-Lopez, C., Anniballi, F., Auricchio, B., Goffredo, E. et al., (2018). Biofilm formation, pigment production and motility in Pseudomonas isolated from the dairy industry. Food Control, 86; 241-248.
Rossi, Ch., Chaves-López, C., Serio, A., Goffredo, E., Goga, B.T.C. and Paparella, A. (2016). Influence of incubation conditions on biofilm formation by Pseudomonas fluorescens isolated from dairy products and dairy manufacturing plants. Italian Journal of Food Safety, 5: 154-157.
· Stanborough, T., Fegan, N., Powell, S.M., Singh, T., Tamplin, M. and Chandry, P.S. (2018). Genomic and metabolic characterization of spoilage-associated Pseudomonas species. International Journal of Food Microbiology, 268: 61-72.
· ́Toole G.A. and Kolter R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple con-vergent signaling pathways: a genetic analysis. Molecular Microbiology, 28: 449–461.
· Vithanage, N.R., Dissanayake, M., Bolge, G., Palombo, E.A., Yeager, T.R., Datta, N. (2016). Biodiversity of culturable psychrotrophic microbiota in raw milk attributable to refrigeration conditions, seasonality and their spoilage potential. International Dairy Journal, 57: 80-90.
_||_
z, D.M. (2015). Detection of Pseudomonas in chicken and fish sold in markets of Assiut City, Egypt. Journal of Food Quality and Hazards Control, 2: 86-89.
Al-Dughaym, A.M. (2000). Recovery and antibiogram studies of hydrophila and P. fluorescens from naturally and experimentally infected Tilapia fishes. Pakistan Journal of Biological Sciences, 3(12): 2185-2187.
Alhamdani, R.J.M. and Al-Luaibi, Y.Y.Y. (2020). Detection of exoa Nan1 genes, the biofilm production with the effect of oyster shell and two plant extracts on Pseudomonas aeruginosa isolated from burn patient and their surrounding environment. Systematic Reviews in Pharmacy,11(12): 1483-1493.
Anand, S., Singh, D., Avadhanula, M., Marka, S. (2014). Development and control of bacterial biofilms on dairy processing membranes. Comprehensive Reviews in Food Sciense Food Safety, 13(1): 18-33.
Bremner H.A. (2002). Safety and quality issues in fish processing. Woodhead Publishing Limited, Boca Raton. URL: https://www.elsevier.com/books/safety-and-quality-issues-in-fish-processing/bremner/978-1-85573-552-1.
Bryers, J.D. (2000). Biofilms2:Process analysis and applications. ISBN: 978-0-471-29656-0.
Burrows, L.L. (2012) Pseudomonas aeruginosa twitching motility: type IV pili in action. Annual Reviews in Microbiology, 66: 493–520.
Buzby, J.C., Wells, H.F. and Hyman, J. (2014). The estimated amount, value, and calories of postharvest food losses at the retail and consumer levels in the United States. In Economic Information Bulletin, 121: 1-33.
Caldera, L., Franzetti, L., Van Coillie, E., De Vos, P., Stragier, P., De Block, J. et al., (2016). Dentification, enzymatic spoilage characterization and proteolytic activity quantification of Pseudomonas Isolated from different foods. Food Microbiology, 54: 142-153.
Carminati, D.,Bonvini, B., Rossetti, L., Zago, M., Tidona, F. and Giraffa, G. (2019). Investigation on the presence of blue pigment-producing Pseudomonas strains along a production line of fresh mozzarella cheese Journal article: Food Control, 100, 321-328 ref. 34.
Carrascosa, C., Millán, R., Jaber, J.R., Lupiola, P., del Rosario-Quintana, C., Mauricio, C. et al., (2015). Blue pigment in fresh cheese produced by Pseudomonas fluorescens. Food Control, 54: 95-102.
Carrascosa, C., Martínez, R., Esther Sanjuán, E., Rafael Millán, R., Rosario-Quintana, C., Acosta, F. et al., (2020). Identification of the Pseudomonas fluorescens group as being responsible for blue pigment on fresh cheese. Journal of Dairy Science, 104(6):6548–6558.
Chen, S.H., Fegan, N., Kocharunchitt, C., Bowman, J.P., Duffy, L.L. (2020). Changes of the bacterial community diversity on chicken carcasses through an Australian poultry processing line. Food Microbiology, 86:103-350.
Chiesa, F., Lomonaco, S., Nucera, D., Garoglio, D., Dalmasso, A. and Civera, T. (2014). Distribution of Pseudomonas species in a dairy plant affected by occasional blue discoloration. Italian Journal of Food Safety, 3(4): 1722.
Costerton, J. (2001). Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends in Microbiology, 9(2): 50-52.
Cude, W.N., Mooney, J., Tavanaei, A.A., Hadden, M.K., Frank, A.M., Gulvik, C.A et al., (2012). Production of the antimicrobial secondary metabolite indigoidine contributesto435 competitive surface colonization by the marine roseobacter Phaeobacter strain Y4I. Applied and Environmental Microbiology, 78;4771-4780.
Darzins, A. (1993). The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric single-domain response regulator CheY. Journal of Bacteriology, 175: 5934–5944.
Del Olmo, A., Calzada, J., Nuñez, M. (2018). The blue discoloration of fresh cheeses: A worldwide defect associated to specific contamination by Pseudomonas fluorescens. Food Control, 86, 359-366.
Déziel, E., Comeau, Y., Villemur, (2001). Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. Journal of Bacteriology, 183(4): 1195-1204.
Djordjevic, D., Wiedmann, M., Mclandsborough, L. (2002). Microtiter plate assay for assessment of listeria monocytogens biofilm formation. Applied and Environmental Microbiology, 68(6): 2950-2958.
Donlan, R.M., Costerton, J. (2002). Biofilms: Survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Review, 15(2): 167-193.
Günseren, F., Mamıkoğlu, L., Öztürk, S., Yücesoy, M., Biberoğlu, K., Yuluğ, N et al., (1999). A surveillance study of antimicrobial resistance of gram-negative bacteria isolated from intensive care units in eight hospitals in Turkey. The Journal of Antimicrobial Chemotherapy, 43(3): 373- 378.
Handley, A., Park, S.H., Kim, S.A., Ricke, S. (2018). Microbiome profiles of commercial broilers through evisceration and immersion chilling during poultry slaughter and the identification of potential indicator microorganisms. Frontiers in Microbiology, 9: 1-11.
Jay J.M., Loessner M.J., Golden D.A. (2005). Modern Food M 7th edition. Springer Science, USA.
Keskin, D. and Ekmekçi, S. (2007). Investigation of the incidence of Pseudomonas in foods., Hacettepe Journal of Biology and Chemistry, 35 (3): 181-186.
Martin, N.H., Murphy, S.C., Ralyea, R.D., Wiedmann, M., Boor, K.J. (2011). When cheese gets the blues: Pseudomonas fluorescens as the causative agent of cheese spoilage. Journal of Dairy Science, 94(6): 3176-3183.
Mead G.C. (2005). Food safety control in the poultry industry. Woodhead Publishing Limited, USA. https://www.elsevier.com/books/food-safety-control-in-the-poultry-industry/mead/978-1-85573-954-3.
Muner Otton, L., da Silva Campos, M., Meneghetti, K.L., Corção, G. (2017). Influence of twitching and swarming motilities on biofilm formation in Pseudomonas Archives of Microbiology, 199: 677-682.
Nucera, D.M., Lomonaco, S., Morra, P., Ortoffi, M.F., Giaccone, D., Grassi, M.A. (2016). Dissemination and persistence of Pseudomonas in small-scale dairy farms. Italian Journal of Food Safety, 5(2), 91-94.
Rashid, M. H. and Kornberg, A. (2000). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 97(9): 4885–4890.
Reverchon, S., Rouanet, C., Expert, D. and Nasser, W. (2002). Characterization of indigoidine biosynthetic genes in erwinia chrysanthemi and role of this blue pigment in pathogenicity. Journal of Bacteriology, 184(3): 654–665.
Rossi, C., Serio, A., Chaves-Lopez, C., Anniballi, F., Auricchio, B., Goffredo, E. et al., (2018). Biofilm formation, pigment production and motility in Pseudomonas isolated from the dairy industry. Food Control, 86; 241-248.
Rossi, Ch., Chaves-López, C., Serio, A., Goffredo, E., Goga, B.T.C. and Paparella, A. (2016). Influence of incubation conditions on biofilm formation by Pseudomonas fluorescens isolated from dairy products and dairy manufacturing plants. Italian Journal of Food Safety, 5: 154-157.
· Stanborough, T., Fegan, N., Powell, S.M., Singh, T., Tamplin, M. and Chandry, P.S. (2018). Genomic and metabolic characterization of spoilage-associated Pseudomonas species. International Journal of Food Microbiology, 268: 61-72.
· ́Toole G.A. and Kolter R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple con-vergent signaling pathways: a genetic analysis. Molecular Microbiology, 28: 449–461.
· Vithanage, N.R., Dissanayake, M., Bolge, G., Palombo, E.A., Yeager, T.R., Datta, N. (2016). Biodiversity of culturable psychrotrophic microbiota in raw milk attributable to refrigeration conditions, seasonality and their spoilage potential. International Dairy Journal, 57: 80-90.
