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Survival in food environment: Bacterial quorum sensing

Year 2021, Volume 92, Issue 1, 83 - 94, 15.01.2021
https://doi.org/10.33188/vetheder.793378

Abstract

The usage of some intracellular and intercellular signal molecules by bacteria for communication is defined as Quorum Sensing (QS). There are biosensor tests that are developed towards understanding the presence of signal molecules, which are produced by various Gram negative and Gram positive bacteria, and to determine the mechanism of biofilm formation via QS mechanism in the field of food industry. The food spoilage and biofilm formation are of significant problems that the food industry faces, and are almost impossible to overcome with traditional approaches. Since QS signals were proven to have significant roles on bacterial pathogenicity and on food spoilage, blockage of these signals in foodborne bacteria may provide steps for protection against QS related phenotypes responsible for food spoilage. In this review, information is provided on QS and its mechanism, role of signal molecules produced by food spoilage bacteria that are important for the food industry, QS and biofilm formation, detection of QS signals via biosensors, and the new research on food preservatives developed as QS inhibitors.

References

  • Açıkgöz E (2012): Quorum quenching. Orlab Online Mikrobiyol Derg TR, 10, 27-44.
  • Ammor MS, Michaelidis C, Nychas EGJ (2008): Insights into the role of quorum sensing in food spoilage. J Food Prot, 71, 1510-25.
  • Annous BA, Fratamico PM, Smith JL (2009): Quorum sensing in biofilms: why bacteria behave the way they do. J Food Sci, 74, 24–37.
  • Antunes LC, Ferreira RB (2009): Intercellular communication in bacteria. Crit Rev Microbiol, 35, 69-80.
  • Asad S, Opal SM (2008) Bench-to-bedside review: quorum sensing and the role of cell-to-cell communication during invasive bacterial infection. Crit Care, 12, 236-246.
  • Bai AJ, Rai VR (2011): Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf, 10, 184-194.
  • Bassler B (2010): Bonnie Bassler (Princeton) Part 1: Bacterial Communication via Quorum Sensing. https://www.youtube.com/watch?time_continue=17&v=saWSxLU0ME8&feature=emb_logo (date accessed: 01 09 2020)
  • Blana V, Stamatiou A, Michaelidis C, Stergiou V, Nychas EGJ (2007): Qualitative evaluation of QS compounds produced in pork and beef samples at different storage conditions; possible effect on kinetic characteristics on spoilage bacteria. Athens, Greece: Second Panhellenic Congress: Biotechnology and Food Technology.
  • Cataldi TR, Bianco G, Palazzo L, Quaranta V (2007): Occurrence of N-acyl-L-homoserine lactones in extracts of some gram-negative bacteria evaluated by gas chromatography–mass spectrometry. Anal Biochem, 361,226-35.
  • Choo JH, Rukayadi Y, Hwang JK (2006): Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol, 42,637-41.
  • Christensen AB, Riedel K, Eberl L, Flodgaard LR, Molin S, Gram L,Givskov M (2003): Quorum sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 149:471–83.
  • Costernon JW, Montanaro L, Arciola CR (2004): Biofilm in implant infections: its production and regulation. Int. Journal of Articial Organs, 28:1062-1068.
  • Czajkowski R, Jafra S (2009): Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol, 56, 1-16.
  • Davies D (2003): Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov, 2 (2), 114-122.
  • Dong YH, Zhang LH (2005): Quorum sensing and quorum-quenching enzymes. J Microbiol, 43, 101-109.
  • Federle MJ, Bassler BL (2003): Interspecies communication in bacteria. J Clin Invest, 112(9), 1291-1299.
  • Flodgaard LR, Dalgaard P, Andersen JB, Nielsen KF, Givskov M, Gram L (2005): Nonbioluminescent strains of Photobacterium phosphoreum produce the cell-to-cell communication signal N-(3-hydroxyoctanoyl)homoserine lactone. Appl Environ Microbiol 71, 2113-2120.
  • Gram L, Christensen AB, Ravn L, Molin S, Givskov M (1999): Production of acylated homoserine lactones by psychrotrophic members of the Enterobacteriaceae isolated from foods. Appl Environ Microbiol, 65, 3458-3463.
  • Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002): Food spoilage interactions between food spoilage bacteria. Intl J Food Microbiol, 78:79-97.
  • Girennavar B, Cepeda ML, Soni KA, Vikram A, Jesudhasan P, Jayaprakash GK, Pillai SD, Patil BS (2008): Grapefruit juice and its furocoumarin inhibits autoinducer signaling and biofilm formation in bacteria. Intl J Food Microbiol, 125, 204-208.
  • Gülgör G, Korukluoğlu M (2014): Mikroorganizmalar Arasında Çoğunluk Algılanması (Quorum Sensing). J Agr Fac Uludag Univ, 28(2), 83-92.
  • Gün İ, Ekinci FY (2009): Biyofilmler: yüzeylerdeki mikrobiyal yaşam. GIDA, 34, 165-173.
  • Hall-Stoodley L, Costernon JW, Stoodley P (2004): Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol, 2, 95-108.
  • Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M (2011): Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis, 15(4), 305-311.
  • Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby n, Kjellberg S, Givskov M (2002): Inhibition of Pseudomonas aeruginosa quorum sensing biofilm bacteria by a halogenated furanone compound. Microbiology, 148, 87-102.
  • Jamuna Bai A, Rai VR, Pradeepa VS (2011): Evaluation of the antimicrobial activity of three medicinal plants of South India. Malays J Microbiol, 7, 14-18.
  • 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. Intl J Food Microbiol, 81, 105-111.
  • Jorgensen LV, Huss HH, Dalgaard P (2000): The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol, 89, 920-934.
  • Karaboz İ, Sukatar A (2004): Bakterilerde sosyal davranışlar (bakterilerde iletişim mekanizmaları). Orlab On-Line Mikrobiyol Derg, 2, 23-32.
  • Liu M, Gray JM, Griffiths MW (2006): Occurrence of proteolytic activity and N-acyl-homoserine lactone signals in the spoilage of aerobically chill-stored proteinaceous raw foods. J Food Protect 69, 2729-2737.
  • Lu L, Hume ME, Pillai SD (2004): Autoinducer-2-like activity associated with foods and its interaction with food additives. J Food Protect, 67, 1457-1462.
  • Manefield M, Rasmussen TB, Hentzer M, Andersen JB, Steinberg P, Kjellberg S, Givskov M (2002): Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology, 148, 1119-1127.
  • Nouraldin AAM, Baddaour MM, Harfous AH, Essa AAM (2016): Bacteriophage-antibiotic synergism to control planktonic and biofilm producing clinical isolates of Pseudomonas aeruginosa. Alexandria J Med, 52 (2), 99-105.
  • Novick RP (2003): Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol, 48, 1429-1449.
  • Nychas GJE, Douglas LM, Sofos JN (2007): Meat, poultry, and seafood, 105-140. In: Doyle MP, Beuchat LR (Ed). Food microbiology: fundamentals and frontiers. Washington DC: ASM Press.
  • Pinto UM, de Souza VE, Martins ML, Vanetti MCD (2007): Detection of acylated homoserine lactones in gram-negative proteolytic psychrotrophic bacteria isolated from cooled raw milk. Food Control 18, 1322-1327.
  • Podbielski A, Kreikemeyer B (2004): Cell density--dependent regulation: basic principles and effects on the virulence of Gram-positive cocci, Intl J Infect Dis 8, 81-95.
  • Ragaert P, Devlieghere F, Debevere J (2007): Role of microbiological and physiological spoilage mechanisms during storage of minimally processed vegetables. Postharvest Biol Technol, 44, 185-194.
  • Rasch M, Rasmussen TB, Larsen TO, Givskov M, Gram L (2005): Effect of quorum sensing inhibitors on food spoilage, 42-43 [abstract]. In: Institute of Food Technologists Annual Meeting. Chicago: Institute of Food Technologists.
  • Ravn L, Christensen AB, Molin S, Givskov M, Gram L (2003): Influence of food preservation parameters and associated microbiota on production rate, profile and stability of acylated homoserine lactones from food-derived Enterobacteriaceae. Intl J Food Microbiol, 84, 145-156.
  • Shunmugaperumal, T (2010): Biofilm Eradication and Prevention: A Pharmaceutical Approach to Medical Device Infections, John Wiley and Sons, Inc.
  • Smith JL, Fratamico PM, Novak JS (2004): Quorum sensing: a primer for food microbiologists. J Food Protect, 67, 1053-1070.
  • Soni KA, Jesudhasan P, Cepeda M, Widmer K, Jayaprakasha GK, Patil BS, Hume ME, Pillai SD (2008): Identification of ground beef-derived fatty acid inhibitors of autoinducer-2 based cell signaling. J Food Protect, 71, 134-138.
  • Steindler L, Venturi V (2007): Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Lett Microbiol, 266, 1-9.
  • Stepaniak L (2004): Dairy enzymology. Intl J Dairy Technol, 57, 153-171.
  • Tormo MA, Marti M, Valle J, Manna AC, Cheung AL, Lasa I, Penadés JR (2005): SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol, 187(7), 2348-2356.
  • Turovskiy Y, Kashtanov D, Paskhover B, Chikindas ML (2007): Quorum sensing: fact, fiction, and everything in between. Adv Appl Microbiol, 62, 191-234.
  • Van Houdt R, Aertsen A, Jansen A, Quintana AL, Michiels CW (2004): Biofilm formation and cell-to-cell signaling in gram-negative bacteriaisolated from a food processing environment. J Appl Microbiol, 96, 177-184.
  • Vattem DA, Mihalik K, Crixell SH, McLean RJC (2007): Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia, 78, 302-310.
  • Viana ES, Campos MEM, Ponce AR, Mantovani HC, Vanetti MCD (2009): Biofilm formation and acyl homoserine lactone production in Hafnia alveiisolated from raw milk. Biol Res, 42, 427-436.
  • Vivas J, Padilla D, Real F, Bravo J, Grasso V, Aacosta F (2008): Influence of environmental conditions on biofilm formation by Hafnia alvei strains. Vet Microbiol, 129, 150-155.
  • Williams P (2007): Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology, 153, 3923-3938.

Gıda ortamında hayata tutunma: Bakteriyel çoğunluk algılama

Year 2021, Volume 92, Issue 1, 83 - 94, 15.01.2021
https://doi.org/10.33188/vetheder.793378

Abstract

Bakterilerin hücre içi ve hücreler arası iletişim amacı ile birtakım sinyal molekülleri kullanımına ‘Quorum Sensing (QS) / Çoğunluk Algılama’ adı verilmektedir. Gıda endüstrisi alanında, çeşitli Gram negatif ve Gram pozitif bakterilerin ürettiği sinyal moleküllerinin varlığının ve QS sistemi ile biyofilm oluşturma mekanizmalarının anlaşılmasına yönelik olarak geliştirilen biyosensör çalışmaları bulunmaktadır. Gıda bozulması ve biyofilm oluşumu, gıda endüstrisinin yüzyüze kaldığı ve geleneksel yaklaşımlarla alt edilmesi neredeyse mümkün olmayan önemli sorunlardan biri olarak karşımıza çıkmaktadır. QS sinyallerinin bakteriyel patojenite ve gıda bozulmasında önemli görevleri olmasından dolayı gıda kaynaklı bakterilerde QS sinyallerinin bloke edilmesi yolu ile gıda bozulmasından sorumlu olan QS ilişkili fenotiplere karşı korunma sağlanabilmesi yolunda adımlar atılmaktadır. Bu derleme makalesinde, QS ve mekanizması, gıda endüstrisi yönünden önem taşıyan bazı bakteriler tarafından üretilen sinyal moleküllerinin gıda bozulmasında üstlendikleri roller, QS ve biyofilm oluşumu, biyosensörler ile QS sinyallerinin tespiti, QS inhibitörleri olarak geliştirilen yeni gıda koruyucuları konusunda yapılan çalışmalar hakkında bilgi verilmiştir.

References

  • Açıkgöz E (2012): Quorum quenching. Orlab Online Mikrobiyol Derg TR, 10, 27-44.
  • Ammor MS, Michaelidis C, Nychas EGJ (2008): Insights into the role of quorum sensing in food spoilage. J Food Prot, 71, 1510-25.
  • Annous BA, Fratamico PM, Smith JL (2009): Quorum sensing in biofilms: why bacteria behave the way they do. J Food Sci, 74, 24–37.
  • Antunes LC, Ferreira RB (2009): Intercellular communication in bacteria. Crit Rev Microbiol, 35, 69-80.
  • Asad S, Opal SM (2008) Bench-to-bedside review: quorum sensing and the role of cell-to-cell communication during invasive bacterial infection. Crit Care, 12, 236-246.
  • Bai AJ, Rai VR (2011): Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf, 10, 184-194.
  • Bassler B (2010): Bonnie Bassler (Princeton) Part 1: Bacterial Communication via Quorum Sensing. https://www.youtube.com/watch?time_continue=17&v=saWSxLU0ME8&feature=emb_logo (date accessed: 01 09 2020)
  • Blana V, Stamatiou A, Michaelidis C, Stergiou V, Nychas EGJ (2007): Qualitative evaluation of QS compounds produced in pork and beef samples at different storage conditions; possible effect on kinetic characteristics on spoilage bacteria. Athens, Greece: Second Panhellenic Congress: Biotechnology and Food Technology.
  • Cataldi TR, Bianco G, Palazzo L, Quaranta V (2007): Occurrence of N-acyl-L-homoserine lactones in extracts of some gram-negative bacteria evaluated by gas chromatography–mass spectrometry. Anal Biochem, 361,226-35.
  • Choo JH, Rukayadi Y, Hwang JK (2006): Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol, 42,637-41.
  • Christensen AB, Riedel K, Eberl L, Flodgaard LR, Molin S, Gram L,Givskov M (2003): Quorum sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 149:471–83.
  • Costernon JW, Montanaro L, Arciola CR (2004): Biofilm in implant infections: its production and regulation. Int. Journal of Articial Organs, 28:1062-1068.
  • Czajkowski R, Jafra S (2009): Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol, 56, 1-16.
  • Davies D (2003): Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov, 2 (2), 114-122.
  • Dong YH, Zhang LH (2005): Quorum sensing and quorum-quenching enzymes. J Microbiol, 43, 101-109.
  • Federle MJ, Bassler BL (2003): Interspecies communication in bacteria. J Clin Invest, 112(9), 1291-1299.
  • Flodgaard LR, Dalgaard P, Andersen JB, Nielsen KF, Givskov M, Gram L (2005): Nonbioluminescent strains of Photobacterium phosphoreum produce the cell-to-cell communication signal N-(3-hydroxyoctanoyl)homoserine lactone. Appl Environ Microbiol 71, 2113-2120.
  • Gram L, Christensen AB, Ravn L, Molin S, Givskov M (1999): Production of acylated homoserine lactones by psychrotrophic members of the Enterobacteriaceae isolated from foods. Appl Environ Microbiol, 65, 3458-3463.
  • Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002): Food spoilage interactions between food spoilage bacteria. Intl J Food Microbiol, 78:79-97.
  • Girennavar B, Cepeda ML, Soni KA, Vikram A, Jesudhasan P, Jayaprakash GK, Pillai SD, Patil BS (2008): Grapefruit juice and its furocoumarin inhibits autoinducer signaling and biofilm formation in bacteria. Intl J Food Microbiol, 125, 204-208.
  • Gülgör G, Korukluoğlu M (2014): Mikroorganizmalar Arasında Çoğunluk Algılanması (Quorum Sensing). J Agr Fac Uludag Univ, 28(2), 83-92.
  • Gün İ, Ekinci FY (2009): Biyofilmler: yüzeylerdeki mikrobiyal yaşam. GIDA, 34, 165-173.
  • Hall-Stoodley L, Costernon JW, Stoodley P (2004): Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol, 2, 95-108.
  • Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M (2011): Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis, 15(4), 305-311.
  • Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby n, Kjellberg S, Givskov M (2002): Inhibition of Pseudomonas aeruginosa quorum sensing biofilm bacteria by a halogenated furanone compound. Microbiology, 148, 87-102.
  • Jamuna Bai A, Rai VR, Pradeepa VS (2011): Evaluation of the antimicrobial activity of three medicinal plants of South India. Malays J Microbiol, 7, 14-18.
  • 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. Intl J Food Microbiol, 81, 105-111.
  • Jorgensen LV, Huss HH, Dalgaard P (2000): The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol, 89, 920-934.
  • Karaboz İ, Sukatar A (2004): Bakterilerde sosyal davranışlar (bakterilerde iletişim mekanizmaları). Orlab On-Line Mikrobiyol Derg, 2, 23-32.
  • Liu M, Gray JM, Griffiths MW (2006): Occurrence of proteolytic activity and N-acyl-homoserine lactone signals in the spoilage of aerobically chill-stored proteinaceous raw foods. J Food Protect 69, 2729-2737.
  • Lu L, Hume ME, Pillai SD (2004): Autoinducer-2-like activity associated with foods and its interaction with food additives. J Food Protect, 67, 1457-1462.
  • Manefield M, Rasmussen TB, Hentzer M, Andersen JB, Steinberg P, Kjellberg S, Givskov M (2002): Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology, 148, 1119-1127.
  • Nouraldin AAM, Baddaour MM, Harfous AH, Essa AAM (2016): Bacteriophage-antibiotic synergism to control planktonic and biofilm producing clinical isolates of Pseudomonas aeruginosa. Alexandria J Med, 52 (2), 99-105.
  • Novick RP (2003): Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol, 48, 1429-1449.
  • Nychas GJE, Douglas LM, Sofos JN (2007): Meat, poultry, and seafood, 105-140. In: Doyle MP, Beuchat LR (Ed). Food microbiology: fundamentals and frontiers. Washington DC: ASM Press.
  • Pinto UM, de Souza VE, Martins ML, Vanetti MCD (2007): Detection of acylated homoserine lactones in gram-negative proteolytic psychrotrophic bacteria isolated from cooled raw milk. Food Control 18, 1322-1327.
  • Podbielski A, Kreikemeyer B (2004): Cell density--dependent regulation: basic principles and effects on the virulence of Gram-positive cocci, Intl J Infect Dis 8, 81-95.
  • Ragaert P, Devlieghere F, Debevere J (2007): Role of microbiological and physiological spoilage mechanisms during storage of minimally processed vegetables. Postharvest Biol Technol, 44, 185-194.
  • Rasch M, Rasmussen TB, Larsen TO, Givskov M, Gram L (2005): Effect of quorum sensing inhibitors on food spoilage, 42-43 [abstract]. In: Institute of Food Technologists Annual Meeting. Chicago: Institute of Food Technologists.
  • Ravn L, Christensen AB, Molin S, Givskov M, Gram L (2003): Influence of food preservation parameters and associated microbiota on production rate, profile and stability of acylated homoserine lactones from food-derived Enterobacteriaceae. Intl J Food Microbiol, 84, 145-156.
  • Shunmugaperumal, T (2010): Biofilm Eradication and Prevention: A Pharmaceutical Approach to Medical Device Infections, John Wiley and Sons, Inc.
  • Smith JL, Fratamico PM, Novak JS (2004): Quorum sensing: a primer for food microbiologists. J Food Protect, 67, 1053-1070.
  • Soni KA, Jesudhasan P, Cepeda M, Widmer K, Jayaprakasha GK, Patil BS, Hume ME, Pillai SD (2008): Identification of ground beef-derived fatty acid inhibitors of autoinducer-2 based cell signaling. J Food Protect, 71, 134-138.
  • Steindler L, Venturi V (2007): Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Lett Microbiol, 266, 1-9.
  • Stepaniak L (2004): Dairy enzymology. Intl J Dairy Technol, 57, 153-171.
  • Tormo MA, Marti M, Valle J, Manna AC, Cheung AL, Lasa I, Penadés JR (2005): SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol, 187(7), 2348-2356.
  • Turovskiy Y, Kashtanov D, Paskhover B, Chikindas ML (2007): Quorum sensing: fact, fiction, and everything in between. Adv Appl Microbiol, 62, 191-234.
  • Van Houdt R, Aertsen A, Jansen A, Quintana AL, Michiels CW (2004): Biofilm formation and cell-to-cell signaling in gram-negative bacteriaisolated from a food processing environment. J Appl Microbiol, 96, 177-184.
  • Vattem DA, Mihalik K, Crixell SH, McLean RJC (2007): Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia, 78, 302-310.
  • Viana ES, Campos MEM, Ponce AR, Mantovani HC, Vanetti MCD (2009): Biofilm formation and acyl homoserine lactone production in Hafnia alveiisolated from raw milk. Biol Res, 42, 427-436.
  • Vivas J, Padilla D, Real F, Bravo J, Grasso V, Aacosta F (2008): Influence of environmental conditions on biofilm formation by Hafnia alvei strains. Vet Microbiol, 129, 150-155.
  • Williams P (2007): Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology, 153, 3923-3938.

Details

Primary Language Turkish
Subjects Veterinary
Journal Section Review / Invited Paper
Authors

Gonca TÜLÜCE
ERCİYES ÜNİVERSİTESİ, VETERİNER FAKÜLTESİ
0000-0003-2280-1725
Türkiye


Seran TEMELLİ
ULUDAĞ ÜNİVERSİTESİ, VETERİNER FAKÜLTESİ
0000-0002-8869-4929
Türkiye


Ayşegül EYİGÖR (Primary Author)
ULUDAĞ ÜNİVERSİTESİ, VETERİNER FAKÜLTESİ
0000-0002-2707-3117
Türkiye

Publication Date January 15, 2021
Application Date September 10, 2020
Acceptance Date November 2, 2020
Published in Issue Year 2021, Volume 92, Issue 1

Cite

Vancouver Tülüce G. , Temelli S. , Eyigör A. Gıda ortamında hayata tutunma: Bakteriyel çoğunluk algılama. Veteriner Hekimler Derneği Dergisi. 2021; 92(1): 83-94.

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