Review
BibTex RIS Cite

BIODIVERSITY OF PSEUDOMONAS, SPOILAGE CHARACTERISTICS, BIOFILM PRODUCTION, AND QUORUM SENSING SYSTEM IN MEAT AND MEAT PRODUCTS

Year 2024, Volume: 49 Issue: 4, 607 - 623, 14.08.2024

Yasemin Şefika Küçükata , Hasan Yetim , Banu Metin

https://doi.org/10.15237/gida.GD24036

Abstract

The contamination of food by spoilage microorganisms and/or pathogens is a concern in the food industry. Pseudomonas species, Gram-negative, aerobic, and psychrotrophic bacteria, can develop in food products stored at low temperatures. The species causing spoilage in raw meat include Pseudomonas fragi, Pseudomonas fluorescens, Pseudomonas putida, and Pseudomonas lundensis. Psychrotrophic pseudomonads cause bad odors, off-tastes, discoloration, and mucus production in raw meat stored under refrigeration and aerobic conditions. Some Pseudomonas species that develop in meats stored at low temperatures are strong biofilm producers. The spoilage activities of pseudomonads are linked to a cell-to-cell communication system known as quorum sensing (QS). The QS system is responsible for encoding genes related to pathogenicity by sensing population density through molecules produced under adverse conditions. Understanding the spoilage mechanisms of pseudomonads in meat is important for inhibiting their development. Research on the QS system of meat pseudomonads is limited. This review discusses the biodiversity, spoilage properties, biofilm formation abilities, and QS effects of Pseudomonas species on meat spoilage.

Keywords

biofilm meat pseudomonas quorum sensing

References

  • Annous, B. A., Fratamico, P. M., Smith, J. L. (2009). Scientific Status Summary. Journal of Food Science, 74(1), R24–R37. https://doi.org/ 10.1111/j.1750-3841.2008.01022.x
  • Anonim, (2012). Etymologia: Pseudomonas. Emerg Infect Dis. 2012 Aug; 18(8): 1241. doi: 10.3201/eid1808.ET1808
  • Arnaut-Rollier, I., Vauterin, L., de Vos, P., Massart, D. L., Devriese, L. A., de Zutter, L., van Hoof, J. (1999). A numerical taxonomic study of the Pseudomonas flora isolated from poultry meat. Journal of Applied Microbiology, 87(1), 15–28. https://doi.org/10.1046/j.1365-2672.1999.00785.x
  • Bai, A. J., Rai, V. R. (2011). Bacterial Quorum Sensing and Food Industry. Comprehensive Reviews in Food Science and Food Safety, 10(3), 183–193. https://doi.org/10.1111/j.1541-4337.2011.00150.x
  • Bassler, B., Greenberg, E. P., Stevens, A. M. (1997). Cross-Species induction of luminescence in the quorum- sensing bacterium vibrio Harveyi. JOURNAL OF BACTERIOLOGY, 179(12), 4043–4045. https://journals.asm.org/journal/jb
  • Bertani, I., Venturi, V. (2004). Regulation of the N -Acyl Homoserine Lactone-Dependent Quorum-Sensing System in Rhizosphere Pseudomonas putida WCS358 and Cross-Talk with the Stationary-Phase RpoS Sigma Factor and the Global Regulator GacA. Applied and Environmental Microbiology, 70(9), 5493–5502. https://doi.org/ 10.1128/aem.70.9.5493-5502.2004
  • Biohaz (2016). Growth of spoilage bacteria during storage and transport of meat. EFSA Journal, 14(6). https://doi.org/10.2903/j.efsa.2016.4523
  • Blana, V. A., Nychas, G. J. E. (2014). Presence of quorum sensing signal molecules in minced beef stored under various temperature and packaging conditions. International journal of food microbiology, 173, 1-8.
  • Carpentier, B. (2009). Biofilms in red meat processing. Biofilms in the Food and Beverage Industries, 375–395. https://doi.org/10.1533/ 9781845697167.4.375
  • Cauchie, E., Delhalle, L., Taminiau, B., Tahiri, A., Korsak, N., Burteau, S., Fall, P. A., Farnir, F., Baré, G., Daube, G. (2020). Assessment of spoilage bacterial communities in food wrap and modified atmospheres-packed minced pork meat samples by 16S rdna metagenetic analysis. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.03074
  • Chen, C. C., Riadi, L., Suh, S. J., Ohman, D. E., Ju, L. K. (2005). Degradation and synthesis kinetics of quorum-sensing autoinducer in Pseudomonas aeruginosa cultivation. Journal of Biotechnology, 117(1), 1–10. https://doi.org/ 10.1016/j.jbiotec.2005.01.003
  • Chen, X., Yu, F., Li, Y., Lou, Z., Toure, S. L., Wang, H. (2020). The inhibitory activity of p-coumaric acid on quorum sensing and its enhancement effect on meat preservation. Cyta-journal of Food, 18(1), 61–67. https://doi.org/ 10.1080/19476337.2019.1701558
  • Dai, J., Li-Min, F., Wu, Y., Liu, B., Cheng, X., Yao, M., Huang, L. (2022). Effects of exogenous AHLs on the spoilage characteristics of Pseudomonas koreensis PS1. Journal of Food Science, 87(2), 819–832. https://doi.org/10.1111/ 1750-3841.16038
  • Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornelis, P., Cámara, M., Williams, P. (2007). The Pseudomonas aeruginosa 4-Quinolone Signal Molecules HHQ and PQS Play Multifunctional Roles in Quorum Sensing and Iron Entrapment. Chemistry Biology, 14(1), 87–96. https://doi.org/10.1016/j.chembiol.2006.11.014
  • Doulgeraki, A. I., Ercolini, D., Villani, F., Nychas, G. J. E. (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. International Journal of Food Microbiology, 157(2), 130–141. https://doi.org/10.1016/ j.ijfoodmicro.2012.05.020
  • Duan, K., Dammel, C., Stein, J., Rabin, H. and Surette, M.G. (2003), Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Molecular Microbiology, 50: 1477-1491.
  • Duman, M., Mulet, M., Satıcıoğlu, İ. B., Altun, S., Gomila, M., Lalucat, J., Garcı́a-Valdés, E. (2020). Pseudomonas sivasensis sp. nov. isolated from farm fisheries in Turkey. Systematic and Applied Microbiology, 43(4), 126103. https://doi.org/ 10.1016/j.syapm.2020.126103
  • Ercolini, D., Casaburi, A., Nasi, A., Ferrocino, I., di Monaco, R., Ferranti, P., Mauriello, G., Villani, F. (2010). Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. International Journal of Food Microbiology, 142(1–2), 120–131. https://doi.org/10.1016/j.ijfoodmicro.2010.06.012
  • Ercolini, Danilo, et al., 2007. Simultaneous Detection of Pseudomonas Fragi , P. Lundensis , and P. Putida from Meat by Use of a Multiplex PCR Assay Targeting the carA Gene.” Applied and Environmental Microbiology, vol. 73, no. 7, 2007, pp. 2354–59. Crossref, https://doi.org/10.1128/ aem.02603-06.
  • Ferrocino, I., Ercolini, D., Villani, F., Moorhead, S. M., Griffiths, M. W. (2009). Pseudomonas fragi Strains Isolated from Meat Do Not Produce N-Acyl Homoserine Lactones as Signal Molecules. Journal of Food Protection, 72(12), 2597–2601. https://doi.org/10.4315/0362-028x-72.12.2597
  • Fuqua, C., Parsek, M. R., Greenberg, E. P. (2001). Regulation of Gene Expression by Cell-to-Cell Communication: Acyl-Homoserine Lactone Quorum Sensing. Annual Review of Genetics, 35(1), 439–468. https://doi.org/10.1146/ annurev.genet.35.102401.090913
  • Gill, A., Greer, G., Nattress, F. (2014). MICROBIOLOGICAL ANALYSIS | Standard Methods. Encyclopedia of Meat Sciences, 306–316. https://doi.org/10.1016/b978-0-12-384731-7.00064-7
  • Girard, L., Lood, C., Rokni‐Zadeh, H., Van Noort, V., Lavigne, R., De Mot, R. (2020). Reliable identification of environmental pseudomonas isolates using the RPOD gene. Microorganisms, 8(8), 1166. https://doi.org/ 10.3390/microorganisms8081166
  • Glessner, A., Smith, R. S., Iglewski, B. H., Robinson, J. B. (1999). Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility. Journal of Bacteriology, 181(5), 1623–1629. https://doi.org/ 10.1128/jb.181.5.1623-1629.1999
  • Gülgör, G., Korukluoğlu, M. (2014). Mikroorganizmalar Arasında Çoğunluk Algılanması (Quorum Sensing) U. Ü. Zı̇raat Fakültesı̇ Dergı̇sı̇, 2014, Cilt 28, Sayı 2, 83-92
  • Hofmann, K., Huptas, C., Doll, E. V., Scherer, S., Wenning, M. (2019). Pseudomonas saxonica sp. nov., isolated from raw milk and skimmed milk concentrate. International Journal of Systematic and Evolutionary Microbiology, 70(2), 935–943. https://doi.org/10.1099/ijsem.0.003851
  • Hossain, Z. (2014). Bacteria: Pseudomonas. Encyclopedia of Food Safety, 490–500. https://doi.org/10.1016/b978-0-12-378612-8.00109-8
  • Iulietto, M. F., Sechi, P., Borgogni, E., Cenci-Goga, B. T. (2015). Meat Spoilage: A Critical Review of a Neglected Alteration Due to Ropy Slime Producing Bacteria. Italian Journal of Animal Science, 14(3), 4011. https://doi.org/10.4081/ ijas.2015.4011
  • İnat, G., Sırıken, B., Başkan, C., Erol, R., Yıldırım, T., ÇIftci, A. (2021). Quorum sensing systems and related virulence factors in Pseudomonas aeruginosa isolated from chicken meat and ground beef. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-94906-x
  • Kolbeck, S., Abele, M., Hilgarth, M., Vogel, R. F. (2021). Comparative Proteomics Reveals the Anaerobic Lifestyle of Meat-Spoiling Pseudomonas Species. Frontiers in Microbiology, 12. https://doi.org/10.3389/fmicb.2021.664061
  • Laue, B. E., Y. Jiang, S. R. Chhabra, S. Jacob, G. S. A. B. Stewart, A. Hardman, J. A. Downie, F. O’Gara, and P. Williams. 2000. The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteri- ocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HtdS, a pu- tative novel N-acylhomoserine lactone synthase. Microbiology 146:2469– 2480.
  • Li H, Li X, Song C, Zhang Y, Wang Z, Liu Z, Wei H and Yu J (2017) Autoinducer-2 Facilitates Pseudomonas aeruginosa PAO1 Pathogenicity in Vitro and in Vivo. Front. Microbiol. 8:1944.
  • Li, J., Zhao, X. (2020). Effects of quorum sensing on the biofilm formation and viable but non-culturable state. Food Research International, 137, 109742. https://doi.org/10.1016/ j.foodres.2020.109742
  • Li, T., Wang, D., Ren, L., Mei, Y., Ding, T., Li, Q., Chen, H., Lǐ, J. (2019). Involvement of Exogenous N-Acyl-Homoserine Lactones in Spoilage Potential of Pseudomonas fluorescens Isolated From Refrigerated Turbot. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.02716
  • Liao, C. (2006). Pseudomonas and related genera. Food Spoilage Microorganisms, 507–540. https://doi.org/10.1533/9781845691417.5.507
  • Lick, S., Kröckel, L., Wibberg, D., Winkler, A., Blom, J., Goesmann, A., Kalinowski, J. (2020). Pseudomonas bubulae sp. nov., isolated from beef. International Journal of Systematic and Evolutionary Microbiology, 70(1), 292–301. https://doi.org/10.1099/ijsem.0.003751
  • Liu, F., Guo, Y., Li, Y. (2006). Interactions of microorganisms during natural spoilage of pork at 5°C. Journal of Food Engineering, 72(1), 24–29. https://doi.org/10.1016/j.jfoodeng.2004.11.015
  • Liu, M., Wang, H., Griffiths, M. W. (2007). Regulation of alkaline metalloprotease promoter by N-acyl homoserine lactone quorum sensing in Pseudomonas fluorescens. Journal of Applied Microbiology, 103(6), 2174–2184. https://doi.org/ 10.1111/j.1365-2672.2007.03488.x
  • Liu, Y. J., Xie, J., Zhao, L. J., Qian, Y. F., Zhao, Y., Liu, X. (2015). Biofilm Formation Characteristics of Pseudomonas lundensis Isolated from Meat. Journal of Food Science, 80(12), M2904–M2910. https://doi.org/10.1111/1750-3841.13142
  • López-Sánchez, A., Leal-Morales, A., Jiménez-Díaz, L., Platero, A. I., Bardallo-Pérez, J., Díaz-Romero, A., Acemel, R. D., Illán, J. M., Jiménez-López, J., Govantes, F. (2016). Biofilm formation-defective mutants in Pseudomonas putida. FEMS Microbiology Letters, 363(13), fnw127. https://doi.org/10.1093/femsle/fnw127
  • Ma, Y., Shi, Q., He, Q., Gu, C. (2021). Metabolomic insights into the inhibition mechanism of methyl N-methylanthranilate: A novel quorum sensing inhibitor and antibiofilm agent against Pseudomonas aeruginosa. International Journal of Food Microbiology, 358, 109402. https://doi.org/10.1016/ j.ijfoodmicro.2021.109402
  • Mayansky, A. N., Chebotar, I. V., Rudneva, E. I., Chistyakova, V. P. (2012). Pseudomonas aeruginosa: Characteristics of the biofilm process. Molecular Genetics, Microbiology and Virology, 27(1), 1–6. https://doi.org/10.3103/ s0891416812010053
  • Mellor, G. E., Bentley, J. A., Dykes, G. A. (2011). Evidence for a role of biosurfactants produced by Pseudomonas fluorescens in the spoilage of fresh aerobically stored chicken meat. Food Microbiology, 28(5), 1101–1104. https://doi.org/10.1016/ j.fm.2011.02.003
  • Mohammed, M. H., Farghaly, R. M., Abdel-Aziz, N. M. (2023). The effect of some essential oils against biofilm producing Pseudomonas aeruginosa of meat sources. SVU- International Journal of Veterinary Sciences, 6(1), 100–115. https://doi.org/10.21608/svu.2023.174609.1239
  • Mohan, C. C., Harini, K., Sudharsan, K., Krishnan, K. R., Sarojadevi, M. (2019). Quorum quenching effect and kinetics of active compound from S. aromaticum and C. cassia fused packaging films in shelf life of chicken meat. LWT, 105, 87–102. https://doi.org/10.1016/j.lwt.2019.01.061
  • Monnet, V., Juillard, V., Gardan, R., 2016. Peptide conversations in gram positive bacteria. Crit. Rev. Microbiol. 42, 339–351.
  • Morimatsu, K., Eguchi, K., Hamanaka, D., Tanaka, F., Uchino, T. (2012). Effects of Temperature and Nutrient Conditions on Biofilm Formation of Pseudomonas putida. Food Science and Technology Research, 18(6), 879–883. https://doi.org/10.3136/fstr.18.879
  • Nethra, P. V., Sunooj, K. V., Aaliya, B., Navaf, M., Akhila, P. P., Sudheesh, C., Mir, S. A., Shijin, A., George, J. (2023). Critical factors affecting the shelf life of packaged fresh red meat- A review. Measurement: Food, 10, 100086. Doi: https://doi.org/10.1016/j.meafoo.2023.100086
  • Osman, K., Orabi, A., Elbehiry, A., Hanafy, M. H., Ali, A. M. (2019). Pseudomonas species isolated from camel meat: quorum sensing-dependent virulence, biofilm formation and antibiotic resistance. Future Microbiology, 14(7), 609–622. https://doi.org/10.2217/fmb-2018-0293
  • Oussalah, Mounia, et al. “Antimicrobial Effects of Selected Plant Essential Oils on the Growth of a Pseudomonas Putida Strain Isolated from Meat.” Meat Science, vol. 73, no. 2, 2006, pp. 236–44. Crossref, https://doi.org/10.1016/j.meatsci.2005.11.019.
  • Pang, X., Yuk, H. G. (2019). Effects of the colonization sequence of Listeria monocytogenes and Pseudomonas fluorescens on survival of biofilm cells under food-related stresses and transfer to salmon. Food Microbiology, 82, 142–150. https://doi.org/10.1016/j.fm.2019.02.002
  • Papadopoulou, O. S., Iliopoulos, V., Mallouchos, A., Panagou, E. Z., Chorianopoulos, N., Tassou, C. C., Nychas, G. J. E. (2020). Spoilage Potential of Pseudomonas (P. fragi, P. putida) and LAB (Leuconostoc mesenteroides, Lactobacillus sakei) Strains and Their Volatilome Profile during Storage of Sterile Pork Meat Using GC/MS and Data Analytics. Foods, 9(5), 633. https://doi.org/10.3390/foods9050633
  • Pellissery, A. J., Vinayamohan, P. G., Amalaradjou, M. A. R., Venkitanarayanan, K. (2020). Spoilage bacteria and meat quality. Meat Quality Analysis, 307–334. https://doi.org/ 10.1016/b978-0-12-819233-7.00017-3
  • Pena, R. T., Blasco, L., Ambroa, A., González-Pedrajo, B., Fernández-García, L., López, M., Bleriot, I., Bou, G., García-Contreras, R., Wood, T. K., Tomás, M. (2019). Relationship Between Quorum Sensing and Secretion Systems. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.01100
  • Pereira, Catarina S., et al. “AI-2-Mediated Signalling in Bacteria.” FEMS Microbiology Reviews, vol. 37, no. 2, 2013, pp. 156–81. Crossref, https://doi.org/10.1111/j.1574-6976.2012.00345.x.
  • Piette, J. P., Idziak, E. S. (1991). Role of flagella in adhesion of Pseudomonas fluorescens to tendon slices. Applied and Environmental Microbiology, 57(6), 1635–1639. https://doi.org/10.1128/ aem.57.6.1635-1639.1991
  • Poursina, S., Ahmadi, M., Fazeli, F., Ariaii, P. (2022). Assessment of virulence factors and antimicrobial resistance among the Pseudomonas aeruginosa strains isolated from animal meat and carcass samples. Veterinary Medicine and Science, 9(1), 315–325. https://doi.org/10.1002/ vms3.1007
  • Quintieri, L., Caputo, L., Brasca, M., Fanelli, F. (2021). Recent Advances in the Mechanisms and Regulation of QS in Dairy Spoilage by Pseudomonas spp. Foods (Basel, Switzerland), 10(12), 3088.
  • Rather, M. A., Saha, D., Bhuyan, S., Jha, A. N., Mandal, M. (2022). Quorum Quenching: A Drug Discovery Approach Against Pseudomonas aeruginosa. Microbiological Research, 264, 127173. https://doi.org/10.1016/j.micres.2022.127173
  • Raza, W., Ling, N., Liu, D., Wei, Z., Huang, Q., Shen, Q. (2016). Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiological Research, 192, 103–113. https://doi.org/10.1016/ j.micres.2016.05.014
  • Sala, C., Morar, A., Colibar, O., Morvay, A. (2012). Antibiotic resistance of gram negative bacteria isolated from meat surface biofilm. Rom. Biotechnol. Lett. 17 (4), 7483-7492
  • Salman, M. K., Abuqwider, J., Mauriello, G. (2023). Anti-Quorum sensing activity of probiotics: The mechanism and role in food and gut health. Microorganisms, 11(3), 793. https://doi.org/10.3390/microorganisms11030793
  • Schuster, M., Peter Greenberg, E. (2006). A network of networks: Quorum-sensing gene regulation in Pseudomonas aeruginosa. International Journal of Medical Microbiology, 296(2–3), 73–81.
  • Shao, L., Chen, S., Wang, H., Zhang, J., Xu, X., Wang, H. (2021). Advances in understanding the predominance, phenotypes, and mechanisms of bacteria related to meat spoilage. Trends in Food Science and Technology, 118, 822–832. https://doi.org/10.1016/j.tifs.2021.11.007
  • Sharma, G., Rao, S., Bansal, A., Dang, S., Gupta, S., Gabrani, R. (2014). Pseudomonas aeruginosa biofilm: Potential therapeutic targets. Biologicals, 42(1), 1–7. https://doi.org/10.1016/ j.biologicals.2013.11.001
  • Shirazi, J., Ain, Q., Khan, S., Jalil, A., Siddiqui, M. F., Ahmad, T., Badshah, M., Adnan, F. (2022). Targeting Acyl Homoserine Lactones (AHLs) by the quorum quenching bacterial strains to control biofilm formation in Pseudomonas aeruginosa. Saudi Journal of Biological Sciences, 29(3), 1673–1682. https://doi.org/10.1016/j.sjbs.2021.10.064
  • Smith, R. S., Iglewski, B. H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. Journal of Clinical Investigation, 112(10), 1460–1465. https://doi.org/10.1172/ jci200320364
  • Spyrelli, E. D., Özcan, O., Mohareb, F., Panagou, E. Ζ., Nychas, G. (2021). Spoilage assessment of chicken breast fillets by means of fourier transform infrared spectroscopy and multispectral image analysis. Current Research in Food Science, 4, 121–131. https://doi.org/ 10.1016/j.crfs.2021.02.007
  • Stanborough, T., Fegan, N., Powell, S. M., Singh, T., Tamplin, M., Chandry, P. S. (2018). Genomic and metabolic characterization of spoilage-associated Pseudomonas species. International Journal of Food Microbiology, 268, 61–72. https://doi.org/10.1016/j.ijfoodmicro.2018.01.005
  • Stellato, G., Utter, D. R., Voorhis, A., de Angelis, M., Eren, A. M., Ercolini, D. (2017). A Few Pseudomonas Oligotypes Dominate in the Meat and Dairy Processing Environment. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.00264
  • Tchagang, C. F., Xu, R., Overy, D., Blackwell, B., Chabot, D., Hubbard, K., Doumbou, C. L., Bromfield, E. S. P., Tambong, J. T. (2018). Diversity of bacteria associated with corn roots inoculated with Canadian woodland soils, and description of Pseudomonas aylmerense sp. nov. Heliyon, 4(8), 1–25.
  • Venturi, V. (2006). Regulation of quorum sensing inPseudomonas. FEMS Microbiology Reviews, 30(2), 274–291. https://doi.org/10.1111/j.1574-6976.2005.00012.x
  • Wagner, E. M., Fischel, K., Rammer, N., Beer, C., Palmetzhofer, A. L., Conrady, B., Roch, F. F., Hanson, B. T., Wagner, M., Rychli, K. (2021). Bacteria of eleven different species isolated from biofilms in a meat processing environment have diverse biofilm forming abilities. International Journal of Food Microbiology, 349, 109232. https://doi.org/10.1016/j.ijfoodmicro.2021.109232
  • Wang, G. Y., Wang, H. H., Han, Y. W., Xing, T., Ye, K. P., Xu, X. L., Zhou, G. H. (2017). Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ. Food Microbiology, 63, 139–146. https://doi.org/ 10.1016/j.fm.2016.11.015
  • Wang, Xin-Yun, and Jing Xie. “Quorum Sensing System-Regulated Proteins Affect the Spoilage Potential of Co-Cultured Acinetobacter Johnsonii and Pseudomonas Fluorescens From Spoiled Bigeye Tuna (Thunnus Obesus) as Determined by Proteomic Analysis.” Frontiers in Microbiology, vol. 11, 2021. Crossref, https://doi.org/10.3389/ fmicb.2020.00940.
  • Wang, Xin-Yun, ve Jing Xie. “Quorum Sensing System-Regulated Proteins Affect the Spoilage Potential of Co-Cultured Acinetobacter Johnsonii and Pseudomonas Fluorescens From Spoiled Bigeye Tuna (Thunnus Obesus) as Determined by Proteomic Analysis.” Frontiers in Microbiology, vol. 11, 2020. Crossref, https://doi.org/10.3389/ fmicb.2020.00940.
  • Wang, Y., Gao, L., Rao, X., Wang, J., Yu, H., Jiang, J., Zhou, W., Wang, J., Xiao, Y., Li, M., Zhang, Y., Zhang, K., Shen, L., Hua, Z. (2018). Characterization of lasR-deficient clinical isolates of Pseudomonas aeruginosa. Scientific Reports, 8(1). https://doi.org/10.1038/s41598-018-30813-y
  • Wen, X., Zhang, D., Li, X., Ding, T., Liang, C., Zheng, X., Yang, W., Hou, C. (2022). Dynamic changes of bacteria and screening of potential spoilage markers of lamb in aerobic and vacuum packaging. Food Microbiology, 104, 103996. https://doi.org/10.1016/j.fm.2022.103996
  • Wickramasinghe, N. N., Ravensdale, J. T., Coorey, R., Dykes, G. A., Chandry, P. S. (2021). Transcriptional profiling of biofilms formed on chilled beef by psychrotrophic meat spoilage bacterium, Pseudomonas fragi 1793. Biofilm, 3, 100045. https://doi.org/10.1016/ j.bioflm.2021.100045
  • Wickramasinghe, N. N., Ravensdale, J. T., Coorey, R., Dykes, G. A., Scott Chandry, P. (2019a). In situ characterisation of biofilms formed by psychrotrophic meat spoilage pseudomonads. Biofouling, 35(8), 840-855.
  • Wickramasinghe, N. N., Ravensdale, J., Coorey, R., Chandry, S. P., Dykes, G. A. (2019b). The Predominance of Psychrotrophic Pseudomonads on Aerobically Stored Chilled Red Meat. Comprehensive Reviews in Food Science and Food Safety, 18(5), 1622–1635. https://doi.org/10.1111/ 1541-4337.12483
  • Yi, L., Su, G., Hu, G., Peng, Q. (2016). Diversity study of microbial community in bacon using metagenomic analysis. Journal of Food Safety, 37(3), e12334. https://doi.org/10.1111/jfs.12334
  • Yin, L., Zhang, Y., Azi, F., Zhou, J., Liu, X., Dai, Y., Wang, Z., Dong, M., Xia, X. (2022). Inhibition of biofilm formation and quorum sensing by soy isoflavones in Pseudomonas aeruginosa. Food Control, 133, 108629. https://doi.org/10.1016/ j.foodcont.2021.108629
  • Zhang, L., Li, S., Liu, X., Wang, Z., Jiang, M., Wang, R., ... Shen, X. (2020). Sensing of autoinducer-2 by functionally distinct receptors in prokaryotes. Nature communications, 11(1), 1-13.
  • Zhang, W., Mi, X., Zhang, C., Yu, C., Wang, S., Ji, J., Yuan, Y., Wang, L., Liu, W., Jiang, Y. (2023a). Meat-derived Escherichia coli and Pseudomonas fragi manage to co-exist in dual-species biofilms by adjusting gene-regulated competitive strength. Food Microbiology, 109, 104122. https://doi.org/10.1016/j.fm.2022.104122
  • Zhang, Y., Wu, Q., Forsythe, S. J., Liu, C., Chen, N., Li, Y., Zhang, J., Wang, J., Ding, Y. (2023b). The cascade regulation of small RNA and quorum sensing system: Focusing on biofilm formation of foodborne pathogens in food industry. Food Bioscience, 52, 102472. https://doi.org/10.1016/ j.fbio.2023.102472
  • Zhao A, Zhu J, Ye X, Ge Y, Li J. Inhibition of biofilm development and spoilage potential of Shewanella baltica by quorum sensing signal in cell-free supernatant from Pseudomonas fluorescens. Int J Food Microbiol. 2016;230:73-80.

ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ

Year 2024, Volume: 49 Issue: 4, 607 - 623, 14.08.2024

Yasemin Şefika Küçükata , Hasan Yetim , Banu Metin

https://doi.org/10.15237/gida.GD24036

Abstract

Bozulma yapan mikroorganizmalar ve/veya patojenler gıda endüstrisinde bir endişe kaynağıdır. Pseudomonas türleri, düşük sıcaklıklarda depolanan gıda ürünlerinde gelişebilen, Gram negatif, aerobik ve psikrotrofik bakterilerdir. Çiğ ette bozulmaya sebebiyet veren türler arasında Pseudomonas fragi, Pseudomonas fluorescens, Pseudomonas putida ve Pseudomonas lundensis sayılmaktadır. Ette kötü koku, tat, renk bozulması ve mukus üretimine sebep olan psikrotrof pseudomonadlar, buzdolabı sıcaklıklarında ve aerobik şartlarda saklanan çiğ et için sorun teşkil etmektedir. Düşük sıcaklıklarda saklanan etlerde gelişen bazı Pseudomonas türleri güçlü biyofilm üreticileridir. Pseudomonadların bozulma faaliyetleri, çoğunluk algılama (Quorum Sensing, QS) olarak bilinen hücreler arası iletişim sistemi ile ilişkilidir. QS sistemi, bakterilerin olumsuz koşullara maruz kaldıklarında ürettikleri moleküller aracılığıyla çoğunluklarını algılayarak patojenite ile ilgili genlerin kodlanmasından sorumludur. Pseudomonadların ette bozulma yapma mekanizmasının anlaşılması, gelişimlerinin engellenebilmesi için önemlidir. Et pseudomonadlarının QS sistemi hakkındaki araştırmalar oldukça sınırlıdır. Bu derleme çalışmasında et pseudomonadlarının biyoçeşitliliği, bozucu özellikleri, biyofilm oluşturma yetenekleri ve QS sistemlerinin, etin bozulma süreçleri üzerindeki etkileri tartışılmıştır.

Keywords

biyofilm et pseudomonas çoğunluk algılama (quorum sensing)

References

  • Annous, B. A., Fratamico, P. M., Smith, J. L. (2009). Scientific Status Summary. Journal of Food Science, 74(1), R24–R37. https://doi.org/ 10.1111/j.1750-3841.2008.01022.x
  • Anonim, (2012). Etymologia: Pseudomonas. Emerg Infect Dis. 2012 Aug; 18(8): 1241. doi: 10.3201/eid1808.ET1808
  • Arnaut-Rollier, I., Vauterin, L., de Vos, P., Massart, D. L., Devriese, L. A., de Zutter, L., van Hoof, J. (1999). A numerical taxonomic study of the Pseudomonas flora isolated from poultry meat. Journal of Applied Microbiology, 87(1), 15–28. https://doi.org/10.1046/j.1365-2672.1999.00785.x
  • Bai, A. J., Rai, V. R. (2011). Bacterial Quorum Sensing and Food Industry. Comprehensive Reviews in Food Science and Food Safety, 10(3), 183–193. https://doi.org/10.1111/j.1541-4337.2011.00150.x
  • Bassler, B., Greenberg, E. P., Stevens, A. M. (1997). Cross-Species induction of luminescence in the quorum- sensing bacterium vibrio Harveyi. JOURNAL OF BACTERIOLOGY, 179(12), 4043–4045. https://journals.asm.org/journal/jb
  • Bertani, I., Venturi, V. (2004). Regulation of the N -Acyl Homoserine Lactone-Dependent Quorum-Sensing System in Rhizosphere Pseudomonas putida WCS358 and Cross-Talk with the Stationary-Phase RpoS Sigma Factor and the Global Regulator GacA. Applied and Environmental Microbiology, 70(9), 5493–5502. https://doi.org/ 10.1128/aem.70.9.5493-5502.2004
  • Biohaz (2016). Growth of spoilage bacteria during storage and transport of meat. EFSA Journal, 14(6). https://doi.org/10.2903/j.efsa.2016.4523
  • Blana, V. A., Nychas, G. J. E. (2014). Presence of quorum sensing signal molecules in minced beef stored under various temperature and packaging conditions. International journal of food microbiology, 173, 1-8.
  • Carpentier, B. (2009). Biofilms in red meat processing. Biofilms in the Food and Beverage Industries, 375–395. https://doi.org/10.1533/ 9781845697167.4.375
  • Cauchie, E., Delhalle, L., Taminiau, B., Tahiri, A., Korsak, N., Burteau, S., Fall, P. A., Farnir, F., Baré, G., Daube, G. (2020). Assessment of spoilage bacterial communities in food wrap and modified atmospheres-packed minced pork meat samples by 16S rdna metagenetic analysis. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.03074
  • Chen, C. C., Riadi, L., Suh, S. J., Ohman, D. E., Ju, L. K. (2005). Degradation and synthesis kinetics of quorum-sensing autoinducer in Pseudomonas aeruginosa cultivation. Journal of Biotechnology, 117(1), 1–10. https://doi.org/ 10.1016/j.jbiotec.2005.01.003
  • Chen, X., Yu, F., Li, Y., Lou, Z., Toure, S. L., Wang, H. (2020). The inhibitory activity of p-coumaric acid on quorum sensing and its enhancement effect on meat preservation. Cyta-journal of Food, 18(1), 61–67. https://doi.org/ 10.1080/19476337.2019.1701558
  • Dai, J., Li-Min, F., Wu, Y., Liu, B., Cheng, X., Yao, M., Huang, L. (2022). Effects of exogenous AHLs on the spoilage characteristics of Pseudomonas koreensis PS1. Journal of Food Science, 87(2), 819–832. https://doi.org/10.1111/ 1750-3841.16038
  • Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornelis, P., Cámara, M., Williams, P. (2007). The Pseudomonas aeruginosa 4-Quinolone Signal Molecules HHQ and PQS Play Multifunctional Roles in Quorum Sensing and Iron Entrapment. Chemistry Biology, 14(1), 87–96. https://doi.org/10.1016/j.chembiol.2006.11.014
  • Doulgeraki, A. I., Ercolini, D., Villani, F., Nychas, G. J. E. (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. International Journal of Food Microbiology, 157(2), 130–141. https://doi.org/10.1016/ j.ijfoodmicro.2012.05.020
  • Duan, K., Dammel, C., Stein, J., Rabin, H. and Surette, M.G. (2003), Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Molecular Microbiology, 50: 1477-1491.
  • Duman, M., Mulet, M., Satıcıoğlu, İ. B., Altun, S., Gomila, M., Lalucat, J., Garcı́a-Valdés, E. (2020). Pseudomonas sivasensis sp. nov. isolated from farm fisheries in Turkey. Systematic and Applied Microbiology, 43(4), 126103. https://doi.org/ 10.1016/j.syapm.2020.126103
  • Ercolini, D., Casaburi, A., Nasi, A., Ferrocino, I., di Monaco, R., Ferranti, P., Mauriello, G., Villani, F. (2010). Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. International Journal of Food Microbiology, 142(1–2), 120–131. https://doi.org/10.1016/j.ijfoodmicro.2010.06.012
  • Ercolini, Danilo, et al., 2007. Simultaneous Detection of Pseudomonas Fragi , P. Lundensis , and P. Putida from Meat by Use of a Multiplex PCR Assay Targeting the carA Gene.” Applied and Environmental Microbiology, vol. 73, no. 7, 2007, pp. 2354–59. Crossref, https://doi.org/10.1128/ aem.02603-06.
  • Ferrocino, I., Ercolini, D., Villani, F., Moorhead, S. M., Griffiths, M. W. (2009). Pseudomonas fragi Strains Isolated from Meat Do Not Produce N-Acyl Homoserine Lactones as Signal Molecules. Journal of Food Protection, 72(12), 2597–2601. https://doi.org/10.4315/0362-028x-72.12.2597
  • Fuqua, C., Parsek, M. R., Greenberg, E. P. (2001). Regulation of Gene Expression by Cell-to-Cell Communication: Acyl-Homoserine Lactone Quorum Sensing. Annual Review of Genetics, 35(1), 439–468. https://doi.org/10.1146/ annurev.genet.35.102401.090913
  • Gill, A., Greer, G., Nattress, F. (2014). MICROBIOLOGICAL ANALYSIS | Standard Methods. Encyclopedia of Meat Sciences, 306–316. https://doi.org/10.1016/b978-0-12-384731-7.00064-7
  • Girard, L., Lood, C., Rokni‐Zadeh, H., Van Noort, V., Lavigne, R., De Mot, R. (2020). Reliable identification of environmental pseudomonas isolates using the RPOD gene. Microorganisms, 8(8), 1166. https://doi.org/ 10.3390/microorganisms8081166
  • Glessner, A., Smith, R. S., Iglewski, B. H., Robinson, J. B. (1999). Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility. Journal of Bacteriology, 181(5), 1623–1629. https://doi.org/ 10.1128/jb.181.5.1623-1629.1999
  • Gülgör, G., Korukluoğlu, M. (2014). Mikroorganizmalar Arasında Çoğunluk Algılanması (Quorum Sensing) U. Ü. Zı̇raat Fakültesı̇ Dergı̇sı̇, 2014, Cilt 28, Sayı 2, 83-92
  • Hofmann, K., Huptas, C., Doll, E. V., Scherer, S., Wenning, M. (2019). Pseudomonas saxonica sp. nov., isolated from raw milk and skimmed milk concentrate. International Journal of Systematic and Evolutionary Microbiology, 70(2), 935–943. https://doi.org/10.1099/ijsem.0.003851
  • Hossain, Z. (2014). Bacteria: Pseudomonas. Encyclopedia of Food Safety, 490–500. https://doi.org/10.1016/b978-0-12-378612-8.00109-8
  • Iulietto, M. F., Sechi, P., Borgogni, E., Cenci-Goga, B. T. (2015). Meat Spoilage: A Critical Review of a Neglected Alteration Due to Ropy Slime Producing Bacteria. Italian Journal of Animal Science, 14(3), 4011. https://doi.org/10.4081/ ijas.2015.4011
  • İnat, G., Sırıken, B., Başkan, C., Erol, R., Yıldırım, T., ÇIftci, A. (2021). Quorum sensing systems and related virulence factors in Pseudomonas aeruginosa isolated from chicken meat and ground beef. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-94906-x
  • Kolbeck, S., Abele, M., Hilgarth, M., Vogel, R. F. (2021). Comparative Proteomics Reveals the Anaerobic Lifestyle of Meat-Spoiling Pseudomonas Species. Frontiers in Microbiology, 12. https://doi.org/10.3389/fmicb.2021.664061
  • Laue, B. E., Y. Jiang, S. R. Chhabra, S. Jacob, G. S. A. B. Stewart, A. Hardman, J. A. Downie, F. O’Gara, and P. Williams. 2000. The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteri- ocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HtdS, a pu- tative novel N-acylhomoserine lactone synthase. Microbiology 146:2469– 2480.
  • Li H, Li X, Song C, Zhang Y, Wang Z, Liu Z, Wei H and Yu J (2017) Autoinducer-2 Facilitates Pseudomonas aeruginosa PAO1 Pathogenicity in Vitro and in Vivo. Front. Microbiol. 8:1944.
  • Li, J., Zhao, X. (2020). Effects of quorum sensing on the biofilm formation and viable but non-culturable state. Food Research International, 137, 109742. https://doi.org/10.1016/ j.foodres.2020.109742
  • Li, T., Wang, D., Ren, L., Mei, Y., Ding, T., Li, Q., Chen, H., Lǐ, J. (2019). Involvement of Exogenous N-Acyl-Homoserine Lactones in Spoilage Potential of Pseudomonas fluorescens Isolated From Refrigerated Turbot. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.02716
  • Liao, C. (2006). Pseudomonas and related genera. Food Spoilage Microorganisms, 507–540. https://doi.org/10.1533/9781845691417.5.507
  • Lick, S., Kröckel, L., Wibberg, D., Winkler, A., Blom, J., Goesmann, A., Kalinowski, J. (2020). Pseudomonas bubulae sp. nov., isolated from beef. International Journal of Systematic and Evolutionary Microbiology, 70(1), 292–301. https://doi.org/10.1099/ijsem.0.003751
  • Liu, F., Guo, Y., Li, Y. (2006). Interactions of microorganisms during natural spoilage of pork at 5°C. Journal of Food Engineering, 72(1), 24–29. https://doi.org/10.1016/j.jfoodeng.2004.11.015
  • Liu, M., Wang, H., Griffiths, M. W. (2007). Regulation of alkaline metalloprotease promoter by N-acyl homoserine lactone quorum sensing in Pseudomonas fluorescens. Journal of Applied Microbiology, 103(6), 2174–2184. https://doi.org/ 10.1111/j.1365-2672.2007.03488.x
  • Liu, Y. J., Xie, J., Zhao, L. J., Qian, Y. F., Zhao, Y., Liu, X. (2015). Biofilm Formation Characteristics of Pseudomonas lundensis Isolated from Meat. Journal of Food Science, 80(12), M2904–M2910. https://doi.org/10.1111/1750-3841.13142
  • López-Sánchez, A., Leal-Morales, A., Jiménez-Díaz, L., Platero, A. I., Bardallo-Pérez, J., Díaz-Romero, A., Acemel, R. D., Illán, J. M., Jiménez-López, J., Govantes, F. (2016). Biofilm formation-defective mutants in Pseudomonas putida. FEMS Microbiology Letters, 363(13), fnw127. https://doi.org/10.1093/femsle/fnw127
  • Ma, Y., Shi, Q., He, Q., Gu, C. (2021). Metabolomic insights into the inhibition mechanism of methyl N-methylanthranilate: A novel quorum sensing inhibitor and antibiofilm agent against Pseudomonas aeruginosa. International Journal of Food Microbiology, 358, 109402. https://doi.org/10.1016/ j.ijfoodmicro.2021.109402
  • Mayansky, A. N., Chebotar, I. V., Rudneva, E. I., Chistyakova, V. P. (2012). Pseudomonas aeruginosa: Characteristics of the biofilm process. Molecular Genetics, Microbiology and Virology, 27(1), 1–6. https://doi.org/10.3103/ s0891416812010053
  • Mellor, G. E., Bentley, J. A., Dykes, G. A. (2011). Evidence for a role of biosurfactants produced by Pseudomonas fluorescens in the spoilage of fresh aerobically stored chicken meat. Food Microbiology, 28(5), 1101–1104. https://doi.org/10.1016/ j.fm.2011.02.003
  • Mohammed, M. H., Farghaly, R. M., Abdel-Aziz, N. M. (2023). The effect of some essential oils against biofilm producing Pseudomonas aeruginosa of meat sources. SVU- International Journal of Veterinary Sciences, 6(1), 100–115. https://doi.org/10.21608/svu.2023.174609.1239
  • Mohan, C. C., Harini, K., Sudharsan, K., Krishnan, K. R., Sarojadevi, M. (2019). Quorum quenching effect and kinetics of active compound from S. aromaticum and C. cassia fused packaging films in shelf life of chicken meat. LWT, 105, 87–102. https://doi.org/10.1016/j.lwt.2019.01.061
  • Monnet, V., Juillard, V., Gardan, R., 2016. Peptide conversations in gram positive bacteria. Crit. Rev. Microbiol. 42, 339–351.
  • Morimatsu, K., Eguchi, K., Hamanaka, D., Tanaka, F., Uchino, T. (2012). Effects of Temperature and Nutrient Conditions on Biofilm Formation of Pseudomonas putida. Food Science and Technology Research, 18(6), 879–883. https://doi.org/10.3136/fstr.18.879
  • Nethra, P. V., Sunooj, K. V., Aaliya, B., Navaf, M., Akhila, P. P., Sudheesh, C., Mir, S. A., Shijin, A., George, J. (2023). Critical factors affecting the shelf life of packaged fresh red meat- A review. Measurement: Food, 10, 100086. Doi: https://doi.org/10.1016/j.meafoo.2023.100086
  • Osman, K., Orabi, A., Elbehiry, A., Hanafy, M. H., Ali, A. M. (2019). Pseudomonas species isolated from camel meat: quorum sensing-dependent virulence, biofilm formation and antibiotic resistance. Future Microbiology, 14(7), 609–622. https://doi.org/10.2217/fmb-2018-0293
  • Oussalah, Mounia, et al. “Antimicrobial Effects of Selected Plant Essential Oils on the Growth of a Pseudomonas Putida Strain Isolated from Meat.” Meat Science, vol. 73, no. 2, 2006, pp. 236–44. Crossref, https://doi.org/10.1016/j.meatsci.2005.11.019.
  • Pang, X., Yuk, H. G. (2019). Effects of the colonization sequence of Listeria monocytogenes and Pseudomonas fluorescens on survival of biofilm cells under food-related stresses and transfer to salmon. Food Microbiology, 82, 142–150. https://doi.org/10.1016/j.fm.2019.02.002
  • Papadopoulou, O. S., Iliopoulos, V., Mallouchos, A., Panagou, E. Z., Chorianopoulos, N., Tassou, C. C., Nychas, G. J. E. (2020). Spoilage Potential of Pseudomonas (P. fragi, P. putida) and LAB (Leuconostoc mesenteroides, Lactobacillus sakei) Strains and Their Volatilome Profile during Storage of Sterile Pork Meat Using GC/MS and Data Analytics. Foods, 9(5), 633. https://doi.org/10.3390/foods9050633
  • Pellissery, A. J., Vinayamohan, P. G., Amalaradjou, M. A. R., Venkitanarayanan, K. (2020). Spoilage bacteria and meat quality. Meat Quality Analysis, 307–334. https://doi.org/ 10.1016/b978-0-12-819233-7.00017-3
  • Pena, R. T., Blasco, L., Ambroa, A., González-Pedrajo, B., Fernández-García, L., López, M., Bleriot, I., Bou, G., García-Contreras, R., Wood, T. K., Tomás, M. (2019). Relationship Between Quorum Sensing and Secretion Systems. Frontiers in Microbiology, 10. https://doi.org/10.3389/ fmicb.2019.01100
  • Pereira, Catarina S., et al. “AI-2-Mediated Signalling in Bacteria.” FEMS Microbiology Reviews, vol. 37, no. 2, 2013, pp. 156–81. Crossref, https://doi.org/10.1111/j.1574-6976.2012.00345.x.
  • Piette, J. P., Idziak, E. S. (1991). Role of flagella in adhesion of Pseudomonas fluorescens to tendon slices. Applied and Environmental Microbiology, 57(6), 1635–1639. https://doi.org/10.1128/ aem.57.6.1635-1639.1991
  • Poursina, S., Ahmadi, M., Fazeli, F., Ariaii, P. (2022). Assessment of virulence factors and antimicrobial resistance among the Pseudomonas aeruginosa strains isolated from animal meat and carcass samples. Veterinary Medicine and Science, 9(1), 315–325. https://doi.org/10.1002/ vms3.1007
  • Quintieri, L., Caputo, L., Brasca, M., Fanelli, F. (2021). Recent Advances in the Mechanisms and Regulation of QS in Dairy Spoilage by Pseudomonas spp. Foods (Basel, Switzerland), 10(12), 3088.
  • Rather, M. A., Saha, D., Bhuyan, S., Jha, A. N., Mandal, M. (2022). Quorum Quenching: A Drug Discovery Approach Against Pseudomonas aeruginosa. Microbiological Research, 264, 127173. https://doi.org/10.1016/j.micres.2022.127173
  • Raza, W., Ling, N., Liu, D., Wei, Z., Huang, Q., Shen, Q. (2016). Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiological Research, 192, 103–113. https://doi.org/10.1016/ j.micres.2016.05.014
  • Sala, C., Morar, A., Colibar, O., Morvay, A. (2012). Antibiotic resistance of gram negative bacteria isolated from meat surface biofilm. Rom. Biotechnol. Lett. 17 (4), 7483-7492
  • Salman, M. K., Abuqwider, J., Mauriello, G. (2023). Anti-Quorum sensing activity of probiotics: The mechanism and role in food and gut health. Microorganisms, 11(3), 793. https://doi.org/10.3390/microorganisms11030793
  • Schuster, M., Peter Greenberg, E. (2006). A network of networks: Quorum-sensing gene regulation in Pseudomonas aeruginosa. International Journal of Medical Microbiology, 296(2–3), 73–81.
  • Shao, L., Chen, S., Wang, H., Zhang, J., Xu, X., Wang, H. (2021). Advances in understanding the predominance, phenotypes, and mechanisms of bacteria related to meat spoilage. Trends in Food Science and Technology, 118, 822–832. https://doi.org/10.1016/j.tifs.2021.11.007
  • Sharma, G., Rao, S., Bansal, A., Dang, S., Gupta, S., Gabrani, R. (2014). Pseudomonas aeruginosa biofilm: Potential therapeutic targets. Biologicals, 42(1), 1–7. https://doi.org/10.1016/ j.biologicals.2013.11.001
  • Shirazi, J., Ain, Q., Khan, S., Jalil, A., Siddiqui, M. F., Ahmad, T., Badshah, M., Adnan, F. (2022). Targeting Acyl Homoserine Lactones (AHLs) by the quorum quenching bacterial strains to control biofilm formation in Pseudomonas aeruginosa. Saudi Journal of Biological Sciences, 29(3), 1673–1682. https://doi.org/10.1016/j.sjbs.2021.10.064
  • Smith, R. S., Iglewski, B. H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. Journal of Clinical Investigation, 112(10), 1460–1465. https://doi.org/10.1172/ jci200320364
  • Spyrelli, E. D., Özcan, O., Mohareb, F., Panagou, E. Ζ., Nychas, G. (2021). Spoilage assessment of chicken breast fillets by means of fourier transform infrared spectroscopy and multispectral image analysis. Current Research in Food Science, 4, 121–131. https://doi.org/ 10.1016/j.crfs.2021.02.007
  • Stanborough, T., Fegan, N., Powell, S. M., Singh, T., Tamplin, M., Chandry, P. S. (2018). Genomic and metabolic characterization of spoilage-associated Pseudomonas species. International Journal of Food Microbiology, 268, 61–72. https://doi.org/10.1016/j.ijfoodmicro.2018.01.005
  • Stellato, G., Utter, D. R., Voorhis, A., de Angelis, M., Eren, A. M., Ercolini, D. (2017). A Few Pseudomonas Oligotypes Dominate in the Meat and Dairy Processing Environment. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.00264
  • Tchagang, C. F., Xu, R., Overy, D., Blackwell, B., Chabot, D., Hubbard, K., Doumbou, C. L., Bromfield, E. S. P., Tambong, J. T. (2018). Diversity of bacteria associated with corn roots inoculated with Canadian woodland soils, and description of Pseudomonas aylmerense sp. nov. Heliyon, 4(8), 1–25.
  • Venturi, V. (2006). Regulation of quorum sensing inPseudomonas. FEMS Microbiology Reviews, 30(2), 274–291. https://doi.org/10.1111/j.1574-6976.2005.00012.x
  • Wagner, E. M., Fischel, K., Rammer, N., Beer, C., Palmetzhofer, A. L., Conrady, B., Roch, F. F., Hanson, B. T., Wagner, M., Rychli, K. (2021). Bacteria of eleven different species isolated from biofilms in a meat processing environment have diverse biofilm forming abilities. International Journal of Food Microbiology, 349, 109232. https://doi.org/10.1016/j.ijfoodmicro.2021.109232
  • Wang, G. Y., Wang, H. H., Han, Y. W., Xing, T., Ye, K. P., Xu, X. L., Zhou, G. H. (2017). Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ. Food Microbiology, 63, 139–146. https://doi.org/ 10.1016/j.fm.2016.11.015
  • Wang, Xin-Yun, and Jing Xie. “Quorum Sensing System-Regulated Proteins Affect the Spoilage Potential of Co-Cultured Acinetobacter Johnsonii and Pseudomonas Fluorescens From Spoiled Bigeye Tuna (Thunnus Obesus) as Determined by Proteomic Analysis.” Frontiers in Microbiology, vol. 11, 2021. Crossref, https://doi.org/10.3389/ fmicb.2020.00940.
  • Wang, Xin-Yun, ve Jing Xie. “Quorum Sensing System-Regulated Proteins Affect the Spoilage Potential of Co-Cultured Acinetobacter Johnsonii and Pseudomonas Fluorescens From Spoiled Bigeye Tuna (Thunnus Obesus) as Determined by Proteomic Analysis.” Frontiers in Microbiology, vol. 11, 2020. Crossref, https://doi.org/10.3389/ fmicb.2020.00940.
  • Wang, Y., Gao, L., Rao, X., Wang, J., Yu, H., Jiang, J., Zhou, W., Wang, J., Xiao, Y., Li, M., Zhang, Y., Zhang, K., Shen, L., Hua, Z. (2018). Characterization of lasR-deficient clinical isolates of Pseudomonas aeruginosa. Scientific Reports, 8(1). https://doi.org/10.1038/s41598-018-30813-y
  • Wen, X., Zhang, D., Li, X., Ding, T., Liang, C., Zheng, X., Yang, W., Hou, C. (2022). Dynamic changes of bacteria and screening of potential spoilage markers of lamb in aerobic and vacuum packaging. Food Microbiology, 104, 103996. https://doi.org/10.1016/j.fm.2022.103996
  • Wickramasinghe, N. N., Ravensdale, J. T., Coorey, R., Dykes, G. A., Chandry, P. S. (2021). Transcriptional profiling of biofilms formed on chilled beef by psychrotrophic meat spoilage bacterium, Pseudomonas fragi 1793. Biofilm, 3, 100045. https://doi.org/10.1016/ j.bioflm.2021.100045
  • Wickramasinghe, N. N., Ravensdale, J. T., Coorey, R., Dykes, G. A., Scott Chandry, P. (2019a). In situ characterisation of biofilms formed by psychrotrophic meat spoilage pseudomonads. Biofouling, 35(8), 840-855.
  • Wickramasinghe, N. N., Ravensdale, J., Coorey, R., Chandry, S. P., Dykes, G. A. (2019b). The Predominance of Psychrotrophic Pseudomonads on Aerobically Stored Chilled Red Meat. Comprehensive Reviews in Food Science and Food Safety, 18(5), 1622–1635. https://doi.org/10.1111/ 1541-4337.12483
  • Yi, L., Su, G., Hu, G., Peng, Q. (2016). Diversity study of microbial community in bacon using metagenomic analysis. Journal of Food Safety, 37(3), e12334. https://doi.org/10.1111/jfs.12334
  • Yin, L., Zhang, Y., Azi, F., Zhou, J., Liu, X., Dai, Y., Wang, Z., Dong, M., Xia, X. (2022). Inhibition of biofilm formation and quorum sensing by soy isoflavones in Pseudomonas aeruginosa. Food Control, 133, 108629. https://doi.org/10.1016/ j.foodcont.2021.108629
  • Zhang, L., Li, S., Liu, X., Wang, Z., Jiang, M., Wang, R., ... Shen, X. (2020). Sensing of autoinducer-2 by functionally distinct receptors in prokaryotes. Nature communications, 11(1), 1-13.
  • Zhang, W., Mi, X., Zhang, C., Yu, C., Wang, S., Ji, J., Yuan, Y., Wang, L., Liu, W., Jiang, Y. (2023a). Meat-derived Escherichia coli and Pseudomonas fragi manage to co-exist in dual-species biofilms by adjusting gene-regulated competitive strength. Food Microbiology, 109, 104122. https://doi.org/10.1016/j.fm.2022.104122
  • Zhang, Y., Wu, Q., Forsythe, S. J., Liu, C., Chen, N., Li, Y., Zhang, J., Wang, J., Ding, Y. (2023b). The cascade regulation of small RNA and quorum sensing system: Focusing on biofilm formation of foodborne pathogens in food industry. Food Bioscience, 52, 102472. https://doi.org/10.1016/ j.fbio.2023.102472
  • Zhao A, Zhu J, Ye X, Ge Y, Li J. Inhibition of biofilm development and spoilage potential of Shewanella baltica by quorum sensing signal in cell-free supernatant from Pseudomonas fluorescens. Int J Food Microbiol. 2016;230:73-80.
There are 87 citations in total.

Details

Primary Language Turkish
Subjects Food Engineering, Meat Technology, Food Microbiology
Journal Section Articles
Authors

Yasemin Şefika Küçükata 0000-0002-2316-1507

Hasan Yetim 0000-0002-5388-5856

Banu Metin 0000-0002-3203-0058

Publication Date August 14, 2024
Submission Date March 28, 2024
Acceptance Date June 12, 2024
Published in Issue Year 2024 Volume: 49 Issue: 4

Cite

APA Küçükata, Y. Ş., Yetim, H., & Metin, B. (2024). ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ. Gıda, 49(4), 607-623. https://doi.org/10.15237/gida.GD24036
AMA Küçükata YŞ, Yetim H, Metin B. ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ. The Journal of Food. August 2024;49(4):607-623. doi:10.15237/gida.GD24036
Chicago Küçükata, Yasemin Şefika, Hasan Yetim, and Banu Metin. “ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ”. Gıda 49, no. 4 (August 2024): 607-23. https://doi.org/10.15237/gida.GD24036.
EndNote Küçükata YŞ, Yetim H, Metin B (August 1, 2024) ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ. Gıda 49 4 607–623.
IEEE Y. Ş. Küçükata, H. Yetim, and B. Metin, “ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ”, The Journal of Food, vol. 49, no. 4, pp. 607–623, 2024, doi: 10.15237/gida.GD24036.
ISNAD Küçükata, Yasemin Şefika et al. “ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ”. Gıda 49/4 (August 2024), 607-623. https://doi.org/10.15237/gida.GD24036.
JAMA Küçükata YŞ, Yetim H, Metin B. ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ. The Journal of Food. 2024;49:607–623.
MLA Küçükata, Yasemin Şefika et al. “ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ”. Gıda, vol. 49, no. 4, 2024, pp. 607-23, doi:10.15237/gida.GD24036.
Vancouver Küçükata YŞ, Yetim H, Metin B. ET VE ET ÜRÜNLERİNDE PSEUDOMONAS BİYOÇEŞİTLİLİĞİ, BOZUCU ÖZELLİKLERİ, BİYOFİLM ÜRETİMİ VE ÇOĞUNLUK ALGILAMA (QUORUM SENSING) SİSTEMİ. The Journal of Food. 2024;49(4):607-23.
 Download Cover Image

by-nc.png

GIDA Dergisi Creative Commons Atıf-Gayri Ticari 4.0 (CC BY-NC 4.0) Uluslararası Lisansı ile lisanslanmıştır. 

GIDA / The Journal of FOOD is licensed under a Creative Commons Attribution-Non Commercial 4.0 International (CC BY-NC 4.0).

https://creativecommons.org/licenses/by-nc/4.0/