[en] Although several studies have focused on the dynamics of bacterial food community, little is known about the variability of batch production and microbial changes that occur during storage. The aim of the study was to characterize the microbial spoilage community of minced pork meat samples, among different food production and storage, using both 16S rRNA gene sequencing and classical microbiology. Three batches of samples were obtained from four local Belgian facilities (A–D) and stored until shelf life under food wrap (FW) and modified atmosphere packaging (MAP, CO2 30%/O2 70%), at constant and dynamic temperature. Analysis of 288 samples were performed by 16S rRNA gene sequencing in combination with counts of psychrotrophic and lactic acid bacteria at 22◦C. At the first day of storage, different psychrotrophic counts were observed between the four food companies (Kruskal-Wallist test, p-value < 0.05). Results shown that lowest microbial counts were observed at the first day for industries D and A (4.2 ± 0.4 and 5.6 ± 0.1 log CFU/g, respectively), whereas industries B and C showed the highest results (7.5 ± 0.4 and 7.2 ± 0.4 log CFU/g). At the end of the shelf life, psychrotrophic counts for all food companies was over 7.0 log CFU/g. With metagenetics, 48 OTUs were assigned. At the first day, the genus Photobacterium (86.7 and 19.9% for food industries A and C, respectively) and Pseudomonas (38.7 and 25.7% for food companies B and D, respectively) were dominant. During the storage, a total of 12 dominant genera (>5% in relative abundance) were identified in MAP and 7 in FW. Pseudomonas was more present in FW and this genus was potentially replaced by Brochothrix in MAP (two-sided Welch’s t-test, p-value < 0.05). Also, a high Bray-Curtis dissimilarity in genus relative abundance was observed between food companies and batches. Although the bacteria consistently dominated the microbiota in our samples are known, results indicated that bacterial diversity needs to be addressed on the level of food companies, batches variation and food storage conditions. Present data illustrate that the combined approach provides complementary results on microbial dynamics in minced pork meat samples, considering batches and packaging variations.
Disciplines :
Food science
Author, co-author :
Cauchie, Emilie ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Delhalle, Laurent ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Tahiri, Assia ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie végétale et microbienne
Korsak Koulagenko, Nicolas ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Département de sciences des denrées alimentaires (DDA)
Burteau, Sophie
Fall, Abdoulaye Papa
Farnir, Frédéric ; Université de Liège - ULiège > Dpt. de gestion vétérinaire des Ressources Animales (DRA) > Biostatistiques et bioinformatique appliquées aux sc. vétér.
Baré, Ghislain
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Language :
English
Title :
Assessment of spoilage bacterial communities in food wrap and modified atmospheres-packed minced pork meat samples by 16S rDNA metagenetic analysis.
AFNOR, (2010). Hygiène Des Aliments, Lignes Directrices pour la Réalisation de Tests de Vieillissement Microbiologique, Aliments Périssables et très Périssables Réfrigérés, NF V01-003. France: Association française de normalisation.
Alvarez-Sieiro P., Montalban-Lopez M., Mu D., Kuipers O. P., (2016). Bacteriocins of lactic acid bacteria: extending the family. Appl. Microbiol. Biotechnol. 100 2939–2951. 10.1007/s00253-016-7343-9 26860942
Andritsos N. D., Mataragas M., Mavrou E., Stamatiou A., Drosinos E. H., (2012). The microbiological condition of minced pork prepared at retail stores in Athens. Greece. Meat Sci. 91 486–489. 10.1016/j.meatsci.2012.02.036 22459497
Argyri A. A., Mallouchos A., Panagou E. S., Nychas G.-J. E., (2015). The dynamics of the HS/SPME-GC-MS as a tool to assess the spoilage of minced beef stored under different packaging and temperature conditions. Int. J. Food Microbiol. 193 51–58. 10.1016/j.ijfoodmicro.2014.09.020 25462923
Benson A. K., David J. R. D., Gilbreth S. E., Smith G., Nietfeldt J., Legge R., et al. (2014). Microbial successions are associated with changes in chemical profiles of a model refrigerated fresh pork sausage during an 80-day shelf life study. Appl. Environ. Microbiol. 80 5178–5194. 10.1128/AEM.00774-14 24928886
Blixt Y., Borch E., (2002). Comparison of shelf life of vacuum-packed pork and beef. Meat Sci. 60 371–378. 10.1016/S0309-1740(01)00145-0 22063640
Carrizosa E., Benito M. J., Ruiz-Moyano S., Hernandez A., del Carmen Villalobos M., Martin A., et al. (2017). Bacterial communities of fresh goat meat packaged in modified atmosphere. Food Microbiol. 65 57–63. 10.1016/j.fm.2017.01.023 28400020
Caryé M. E., Garro O., Vignolo G., (2005). Effect of storage temperature and gas permeability of packaging film on the growth of lactic acid bacteria and Brochothrix thermosphacta in cooked meat emulsions. Food Microbiol. 22 505–512. 10.1016/j.fm.2005.01.003
Casaburi A., Nasi A., Ferrocino I., Di Monaco R., Mauriello G., Villani F., et al. (2011). Spoilage-related activity of Carnobacterium maltaromaticum strains in air-storedand vacuum-packed meat. Appl. Environ. Microbiol. 77 7382–7393. 10.1128/AEM.05304-11 21784913
Casaburi A., Piombino P., Nychas G.-J., Villani F., Ercolini D., (2014). Bacterial populations and the volatilome associated to meat spoilage. Food Microbiol. 45 83–102. 10.1016/j.fm.2014.02.002 25481065
Cauchie E., Gand M., Kergourlay G., Taminiau B., Delhalle L., Korsak N., et al. (2017). The use of the 16S rRNA gene metagenetic monitoring of refrigerated food products for understanding the kinetics of microbial subpopulations at different storage temperatures: the example of white pudding. Int. J. Food Microbiol. 247 70–78. 10.1016/j.ijfoodmicro.2016.10.012 27751567
Ceugniez A., Taminiau B., Coucheney F., Jacques P., Delcenserie V., Daube G., et al. (2017). Use of a metagenetic approach to monitor the bacterial microbiota of ≪ Tomme d’Orchies ≫ cheese during the ripening process. Int. J. Food Microbiol. 247 65–69. 10.1016/j.ijfoodmicro.2016.10.034 27817942
Chaillou S., Chaulot-Talmon A., Caekebeke H., Cardinal M., Christieans S., Denis C., et al. (2015). Origin and ecological selection of core and food-specific bacterial communities associated with meat and seafood spoilage. Int. Soc. Microb. Ecol. J. 9 1105–1118. 10.1038/ismej.2014.202 25333463
Chaix E., Guillaume C., Gontard N., Guillard V., (2015). Diffusivity and solubility of CO2 in dense solid food products. J. Food Eng. 166 1–9. 10.1016/j.jfoodeng.2015.05.023
Cheng W., Sun D.-W., Cheng J.-H., (2016). Pork biogenic amine index (BAI) determination based on chemometric analysis of hyperspectral imaging data. LWT Food Sci. Technol. 73 13–19. 10.1016/j.lwt.2016.05.031
Cocolin L., Mataragas M., Bourdichon F., Doulgeraki A., Pilet M.-F., Jagadeesan B., et al. (2018). Next generation microbiological risk assessment meta-omics: the next need for integration. Int. J. Food Microbiol. 287 10–17. 10.1016/j.ijfoodmicro.2017.11.008 29157743
Cocolin L., Rantsiou K., Iacumin L., Urso R., Cantoni C., Comi G., (2004). Study of the ecology of fresh sausages and characterization of populations of lactic acid bacteria by molecular methods. Appl. Environ. Microbiol. 70 1883–1894. 10.1128/AEM.70.4.1883-1894.2004 15066777
Couvert O., Guégan S., Hézard B., Huchet V., Lintz A., Thuault D., et al. (2017). Modeling carbon dioxide effect in a controlled atmosphere and its interactions with temperature and pH on the growth of L. monocytogenes and P. fluorescens. Food Microbiol. 68 89–96. 10.1016/j.fm.2017.07.003 28800830
Dalcanton F., Pérez-Rodriguez F., Posada-Izquierdo D., de Arageo G. M.-F., Garcia-Gimeno R. M., (2013). Modelling growth of Lactobacillus plantarum and shelf life of vacuum-packaged cooked chopped pork at different temperatures. Int. J. Food Sci. Technol. 48 2580–2587. 10.1111/ijfs.12252
Dalgaard P., (1995). Qualitative and quantitative characterization of spoilage bacteria from packed fish. Int. J. Food Microbiol. 26 319–333. 10.1016/0168-1605(94)00137-U 7488527
De Filippis F., La Storia A., Villani F., Ercolini D., (2013). Exploring the sources of bacterial spoilers in beefsteaks by culture-independent high-throughput sequencing. PLoS One 8:e70222. 10.1371/journal.pone.0070222 23936168
Del Blanco A., Caro I., Quinto E. J., Mateo J., (2017). Quality changes in refrigerated stored minced pork wrapped with plastic cling film and the effect of glucose supplementation. Meat Sci. 126 55–62. 10.1016/j.meatsci.2016.12.007 28043049
Delcenserie V., Taminiau B., Delhalle L., Nezer C., Doyen P., Crevecoeur S., et al. (2014). Microbiota characterization of a Belgian protected designation of origin cheese, Herve cheese, using metagenomic analysis. J. Dairy Sci. 97 6046–6056. 10.3168/jds.2014-8225 25064656
Delhalle L., Korsak N., Taminiau B., Nezer C., Burteau S., Delcenserie V., et al. (2016). Exploring the bacterial diversity of Belgian steak tartare using metagenetics and quantitative real-time PCR analysis. J. Food Prot. 79 220–229. 10.4315/0362-028X.JFP-15-185 26818982
Den Besten H. M. W., Amézquita A., Bover-Cid S., Dagnas S., Ellouze M., Guillou S., et al. (2018). Next generation of microbiological risk assessment: potential of omics data for exposure assessment. Int. J. Food Microbio. 287 18–27. 10.1016/j.ijfoodmicro.2017.10.006 29032838
Den Besten H. M. W., Aryani D. C., Metselaar K. I., Zwietering M. H., (2017). Microbial variability in growth and heat resistance of a pathogen and a spoiler: all variabilities are equal but some are more equal than others. Int. J. Food Microbiol. 240 24–31. 10.1016/j.ijfoodmicro.2016.04.025 27207811
Doulgeraki A. I., Ercolini D., Villani F., Nychas G.-J. E., (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. Int. J. Food Microbiol. 157 130–141. 10.1016/j.ijfoodmicro.2012.05.020 22682877
Elizaquivel P., Pérez-Cataluna A., Yépez A., Aristimuno C., Jiménez E., Cocconcelli P. S., et al. (2015). Pyrosequencing vs. culture-dependent approaches to analyze lactic acid bacteria associated to chica, a traditional maize-based fermented beverage from Northwestern Argentina. Int. J. Food Microbiol. 198 9–18. 10.1016/j.ijfoodmicro.2014.12.027 25584777
Ercolini D., Ferrocino I., Nasi A., Ndagijimana M., Vernocchi P., La Storia A., et al. (2011). Monitoring of microbial metabolites and bacterial diversity in beef stored under different packaging conditions. Appl. Environ. Microbiol. 77 7372–7381. 10.1128/AEM.05521-11 21803905
Fadda S., Lopez C., Vignolo G., (2010). Role of lactic acid bacteria during meat conditioning and fermentation: peptides generated as sensorial and hygienic biomarkers. Meat Sci. 86 66–79. 10.1016/j.meatsci.2010.04.023 20619799
Fall P. A., Pilet M. F., Leduc F., Cardinal M., Duflos G., Guérin C., et al. (2012). Sensory and physicochemical evolution of tropical cooked peeled shrimp inoculated by Brochothrix thermosphacta and Lactococcus piscium CNCM I-4031 during storage at 8°C. Int. J. Food Microbiol. 152 82–90. 10.1016/j.ijfoodmicro.2011.07.015 21835482
Fougy L., Desmonts M.-H., Coeuret G., Fassel C., Hamon E., Hézard B., et al. (2016). Reducing salt in raw pork sausage increases spoilage and correlated with reduced bacterial diversity. Appl. Environ. Microbiol. 82 3928–3939. 10.1128/AEM.00323-16 27107120
Fuertez-Perez S., Hauschild P., Hilgarth M., Vogel R. F., (2019). Biodiversity of Photobacterium spp. isolated from meats. Front. Microbiol. 10:2399. 10.3389/fmicb.2019.02399 31749770
Galimberti A., Bruno A., Mezzasalma V., De Mattia F., Bruni I., Labra M., (2015). Emerging DNA-based technologies to characterize food ecosystems. Food Res. Int. 69 424–433. 10.1016/j.foodres.2015.01.017
Garnier L., Valence F., Pawtowski A., Auhustsinava-galerne L., Frotté N., Baroncelli R., et al. (2017). Diversity of spoilage fungi associated with various French dairy products. Int. J. Food Microbiol. 241 191–197. 10.1016/j.ijfoodmicro.2016.10.026 27794247
Garofalo C., Bancalari E., Milanovic V., Cardinali F., Osimani A., Sardaro M. L. S., et al. (2017). Study of the bacterial diversity of foods: PCR-DGGE versus LH-PCR. Int. J. Food Microbiol. 242 24–36. 10.1016/j.ijfoodmicro.2016.11.008 27866041
Geeraerts W., Pothakos V., De Vuyst L., Leroy F., (2017). Diversity of the dominant bacterial species on sliced cooked pork products at expiration date in the Belgian retail. Food Microbiol. 65 236–243. 10.1016/j.fm.2017.03.007 28400008
Ghasemi-Varnamkhasti M., Apetrei C., Lozano J., Anyogu A., (2018). Potential use of electronic noses, electronic tongues and biosensors as multisensory systems for spoilage examination in foods. Trends Food Sci. Technol. 80 71–92. 10.1016/j.tifs.2018.07.018
Greppi A., Ferrocino I., La Storia A., Rantsiou K., Ercolini D., Cocolin L., (2015). Monitoring of the microbiota of fermented sausages by culture independent rRNA-based approaches. Int. J. Food Microbiol. 212 67–75. 10.1016/j.ijfoodmicro.2015.01.016 25724303
Gu G., Ottesen A., Bolten S., Ramachandran P., Reed E., Rideout S., et al. (2018). Shifts in spinach microbial communities after chlorine washing and storage at compliant and abusive temperatures. Food Microbiol. 73 73–84. 10.1016/j.fm.2018.01.002 29526229
Guillard V., Couvert O., Stahl V., Hanin A., Denis C., Huchet V., et al. (2016). Validation of a predictive model coupling gas transfer and microbial growth in fresh food packed under modified atmosphere. Food Microbiol. 58 43–55. 10.1016/j.fm.2016.03.011 27217358
Hahne J., Isele D., Berning J., Lipski A., (2019). The contribution of fast growing, psychrotrophic microorganisms on biodiversity of refrigerated raw cow’s milk with high bacterial counts and their food spoilage potential. Food Microbiol. 79 11–19. 10.1016/j.fm.2018.10.019 30621865
Holm E. S., Schäfer A., Koch A. G., Petersen M. A., (2013). Investigation of spoilage in saveloy samples inoculated with four potential spoilage bacteria. Meat Sci. 93 687–695. 10.1016/j.meatsci.2012.11.016 23261532
Jastrzębska A., Kowalska S., Szłyk E., (2016). Studies of levels of biogenic amines in meat samples in relation to the content of additives. Food Addit. Contam. Part A hem. Anal. Control Expo Risk Assess 33 27–40. 10.1080/19440049.2015.1111525 26515667
Kariyawasam K. M. G. M. M., Jeewanthi R. K. C., Lee N.-K., Paik H.-D., (2019). Characterization of cottage cheese unsing Weissella cibaria D30: physicochemical, antioxidant, and antilisterial properties. J. Dairy Sci. 102 3887–3893. 10.3168/jds.2018-15360 30827567
Kato Y., Sakala R. M., Hayashidani H., Kiuchi A., Kaneuchi C., Ogawa M., (2000). Lactobacillus algidus sp. nov., a psychrophilic lactic acid bacterium isolated from vacuum-packaged refrigerated beef. Int. J. Syst. Envol. Microbiol. 50 1143–1149. 10.1099/00207713-50-3-1143 10843056
Kaur M., Shang H., Tamplin M., Ross T., Bowman J. P., (2017). Culture-dependent and culture-independent assessment of spoilage community growth on VP lamb meat from packaging to past end of shelf-life. Food Microbiol. 68 71–80. 10.1016/j.fm.2017.06.015 28800828
Kembel S. W., Wu M., Eisen J. A., Green J. L., (2012). Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLOS Comput. Biol. 8 1–11. 10.1371/journal.pcbi.1002743.g001
Kim E., Cho Y., Lee Y., Han S.-K., Kim C.-G., Choo D.-W., et al. (2017). A proteomic approach for rapid identification of Weissella species isolated from Korean fermented foods on MALDI-TOF MS supplemented with an in-house database. Int. J. Food Microbiol. 243 9–15. 10.1016/j.ijfoodmicro.2016.11.027 27936381
Koort J., Murros A., Coenye T., Eerola S., Vandamme P., Sukura A., et al. (2005). Lactobacillus oligofermentans sp. nov., associated with spoilage of modified-atmosphere-packaged poultry products. Appl. Environ. Microbiol. 71 4400–4406. 10.1128/AEM.71.8.4400-4406.2005 16085830
Korsak N., Taminiau B., Hupperts C., Delhalle L., Nezer C., Delcenserie V., et al. (2017). Assessment of bacterial superficial contamination in classical or ritually slaughtered cattle using metagenetics and microbial analysis. Int. J. Food Microbiol. 247 79–86. 10.1016/j.ijfoodmicro.2016.10.013 27756497
Koutsoumanis K., Stamatiou A., Skandamis P., Nychas G.-J. E., (2006). Development of a microbial model for the combined effect of temperature and pH on spoilage of ground meat, and validation of the model under dynamic temperature conditions. Appl. Environ. Microbiol. 72 124–134. 10.1128/AEM.72.1.124-134.2006 16391034
Koutsoumanis K. P., Stamatiou A. P., Drosinos E. H., Nychas G.-J. E., (2008). Control of spoilage microorganisms in minced pork by a self-developed modified atmosphere induced by the respiratory activity of meat microflora. Food Microbiol. 25 915–921. 10.1016/j.fm.2008.05.006 18721682
Lee M., Song J. H., Jung M. Y., Lee S. H., Chang J. Y., (2017). Large-scale targeted metagenomics analysis of bacterial ecological changes in 88 kimchi samples during fermentation. Food Microbiol. 66 173–183. 10.1016/j.fm.2017.05.002 28576366
Li M., Tian L., Zhao G., Zhang Q., Gao X., Huang X., et al. (2014). Formation of biogenic amines and growth of spoilage-related microorganisms in pork stored under different packaging conditions applying PCA. Meat Sci. 96 843–848. 10.1016/j.meatsci.2013.09.023 24200579
Li N., Zhang Y., Wu Q., Gu Q., Chen M., Zhang Y., et al. (2019). High-throughput sequencing analysis of bacterial community composition and quality characteristics in refrigerated pork during storage. Food Microbiol. 83 86–94. 10.1016/j.fm.2019.04.013 31202422
Li Q., Zhang L., Luo Y., (2018). Changes in microbial communities and quality attributes of white muscle and dark muscle from common carp (Cyprinus carpio) during chilled and freeze-chilled storage. Food Microbiol. 73 237–244. 10.1016/j.fm.2018.01.011 29526208
Liu F., Yang R.-Q., Li Y.-F., (2006). Correlations between growth parameters of spoilage micro-organisms and shelf-life of pork stored under air and modified atmosphere at -2, 4 and 10°C. Food Microbiol. 23 578–583. 10.1016/j.fm.2005.10.002 16943054
Liu X., Ji L., Wang X., Li J., Shu J., Sun A., (2018). Role of RpoS in stress resistance, quorum sensing and spoilage potential of Pseudomonas fluorescens. Int. J. Food Microbiol. 270 31–38. 10.1016/j.ijfoodmicro.2018.02.011 29471265
Liu Z., Li J., Wei B., Huang T., Xiao Y., Peng Z., et al. (2019). Bacterial community and composition in Jiang-shui and Suan-cai revealed by high-throughput sequencing of 16S rRNA. Int J Food Microbiol. 306:108271. 10.1016/j.ijfoodmicro.2019.108271 31377413
Louca S., Doebeli M., Parfrey L. W., (2018). Correcting for 16S rRNA gene copy numbers in microbiome surveys remains an unsolved problem. Microbiome 6 1–12. 10.1186/s40168-018-0420-9 29482646
Mann E., Wetzels S. U., Pinior B., Metzler-Zebeli B. U., Wagner M., Schmitz-Esser S., (2016). Psychrophile spoilers dominate the bacterial microbiome in musculature samples of slaughter pigs. Meat Sci. 117 36–40. 10.1016/j.meatsci.2016.02.034 26943946
Mansur A. R., Song E.-J., Cho Y.-S., Nam Y.-D., Choi Y.-S., Kim D.-O., et al. (2019). Comparative evaluation of spoilage-related bacterial diversity and metabolite profiles in chilled beef stored under air and vacuum packaging. Food Microbiol. 77 166–172. 10.1016/j.fm.2018.09.006 30297047
Martins W. F., Longhi D. A., Costa Menezes N. M., da Silva Camargo A. P., Borges Laurindo J., Falcaoet al. (2016). Predicting growth of Weissella viridescens in culture medium under dynamic temperature conditions. Procedia Food Sci. 7 37–40. 10.1016/j.profoo.2016.02.082
Moretro T., Moen B., Heir E., Hansen A. A., Langsrud S., (2016). Contamination of salmon fillets and processing plants with spoilage bacteria. Int. J. Food Microbiol. 237 98–108. 10.1016/j.ijfoodmicro.2016.08.016 27552347
Nalbantoglu U., Cakar A., Dogan H., Abaci N., Ustek D., Sayood K., et al. (2014). Metagenomic analysis of the microbial community in kefir grains. Food Microbiol. 41 42–51. 10.1016/j.fm.2014.01.014 24750812
Nieminen T. T., Dalgaard P., Björkroth J., (2016). Volatile organic compounds and Photobacterium phosphoreum associated with spoilage of modified-atmosphere-packaged raw pork. Int. J. Food Microbiol. 218 86–95. 10.1016/j.ijfoodmicro.2015.11.003 26623935
Nieminen T. T., Koskinen K., Laine P., Hultman J., Säde E., Paulin L., et al. (2012). Comparison of microbial communities in marinated and unmarinated broiler meat by metagenomics. Int. J. Food Microbiol. 157 142–149. 10.1016/j.ijfoodmicro.2012.04.016 22626965
Nieminen T. T., Nummela M., Björkroth J., (2015). Packaging gas selects lactic acid bacterial communities on raw pork. J. Appl. Microbiol. 119 1310–1316. 10.1111/jam.12890 26152532
Nychas G. J. E., Skandamis P. N., Tassou C. C., Koutsoumanis K. P., (2008). Meat spoilage during distribution. Meat Sci. 78 77–89. 10.1016/j.meatsci.2007.06.020 22062098
Odeyemi O. A., Burke C. M., Bolch C. C. J., Stanley R., (2018). Spoilage microbial community profiling by 16S rRNA amplicon sequencing of modified atmospohere packaged live mussels stored ar 4°C. Food Res. Int. 121 568–576. 10.1016/j.foodres.2018.12.017 31108782
Papageorgiou M., Lambropoulou D., Morrison C., Klodzinska E., Namiesnik J., Plotka-Wasylka J., (2018). Literature update of analytical methods for biogenic amines determination in food and beverages. Trends Analyt. Chem. 98 128–142. 10.1016/j.trac.2017.11.001
Parente E., Cocolin L., De Filippis F., Zotta T., Ferrocino I., O’Sullivan O., et al. (2016). FoodMicrobionet: a database for the visualization and exploration of food bacterial communities based on network analysis. Int. J. Food Microbiol. 219 28–37. 10.1016/j.ijfoodmicro.2015.12.001 26704067
Parks D. H., Tyson G. W., Hugenholtz P., Beiko R. G., (2014). STAMP: statistical analysis of taxonomic and functional profiles. Bioinform. 30 3123–3124. 10.1093/bioinformatics/btu494 25061070
Parlapani F. F., Michailidou S., Pasentsis K., Argiriou A., Krey G., Boziaris I. S., (2018). A meta-barcoding approach to assess and compare the storage temperature-dependent bacterial diversity of gilt-head sea bream (Sparus aurata) originating from fish farms from two geographically distinct areas of Greece. Int. J. Food Microbiol. 278 36–43. 10.1016/j.ijfoodmicro.2018.04.027 29698856
Pennacchia C., Ercolini D., Villani F., (2009). Development of a real-time PCA assay for the specific detection of Brochothrix thermosphacta in fresh and spoiled raw meat. Int. J. Food Microbiol. 134 230–236. 10.1016/j.ijfoodmicro.2009.07.005 19651454
Pennacchia C., Ercolini D., Villani F., (2011). Spoilage-related microbiota associated with chilled beef stored in air or vacuum pack. Food Microbiol. 28 84–93. 10.1016/j.fm.2010.08.010 21056779
Peruzy M. F., Murru N., Yu Z., Cnockaert M., Joossens M., Proroga Y. T. R., et al. (2019). Determination of the microbiological contamination in minced pork by culture dependent and 16S amplicon sequencing analysis. Int. J. Food Microbiol. 290 27–35. 10.1016/j.ijfoodmicro.2018.09.025 30292676
Pinter M. D., Harter T., McCarthy M. J., Augustine M. P., (2014). Toward using NMR to screen for spoiled tomatoes stored in 1,000 L, aseptically sealed, metal-lined totes. Sensors 14 4167–4176. 10.3390/s140304167 24594611
Pinu F. R., (2016). Early detection of food pathogens and food spoilage microorganisms: application of metabolomics. Trends Food Sci. Technol. 54 213–215. 10.1016/j.tifs.2016.05.018
Polka J., Rebecchi A., Pisacana V., Morelli L., Puglisi E., (2015). Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16S rRNA amplicons. Food Microbiol. 46 342–356. 10.1016/j.fm.2014.08.023 25475305
Porcellato D., Aspholm M., Skeie S. B., Monshaugen M., Brendehaug J., Mellegard H., (2018). Microbial diversity of consumption milk during processing and storage. Int. J. Food Microbiol. 266 21–30. 10.1016/j.ijfoodmicro.2017.11.004 29161642
Pothakos V., Devlieghere F., Villani F., Björkroth J., Ercolini D., (2015). Lactic acid bacteria and their controversial role in fresh meat spoilage. Meat Sci. 109 66–74. 10.1016/j.meatsci.2015.04.014 25972087
Pothakos V., Taminiau B., Huys G., Nezer C., Daube G., Devlieghere F., (2014). Psychrotrophic lactic acid bacteria associated with production batch recalls and sporadic cases of early spoilage in Belgium between 2010 and 2014. Int. J. Food Microbiol. 191 157–163. 10.1016/j.ijfoodmicro.2014.09.013 25268325
Pruesse E., Peplies J., Glïckner F. O., (2012). SINA: accurate high-throughput multiple sequence aligment of ribosomal RNA genes. Bioinformatics 28 1823–1829. 10.1093/bioinformatics/bts252 22556368
R Core Team (2019). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at: https://www.R-project.org/
Rahkila R., Nieminen T., Johansson P., Säde E., Björkroth J., (2012). Characterization and evaluation of the spoilage potential of Lactococcus piscium isolates from modified atmosphere packaged meat. Int. J. Food Microbiol. 156 50–59. 10.1016/j.ijfoodmicro.2012.02.022 22445914
Raimondi S., Nappi M. R., Sirangelo T. M., Leonardi A., Amaretti A., Ulrici A., et al. (2018). Bacterial community of industrial raw sausage packaged in modified atmosphere throughout the shelf life. Int. J. Food Microbiol. 280 78–86. 10.1016/j.ijfoodmicro.2018.04.041 29783046
Reid R., Fanning S., Whyte P., Kerry J., Lindqvist R., Yu Z., et al. (2017). The microbiology of beef carcasses and primals during chilling and commercial storage. Food Microbiol. 61 50–57. 10.1016/j.fm.2016.08.003 27697169
Riquelme C., Câmara S., Enes Dapkevicius M., de L. N., Vinuesa P., da Silva C. C. G., et al. (2015). Characterization of the bacterial biodiversity in Pico cheese (an artisanal Azorean food). Int. J. Food Microbiol. 192 86–94. 10.1016/j.ijfoodmicro.2014.09.031 25440551
Robertson C. E., Harris J. K., Wagner B. D., Granger D., Browne K., Tatem B., et al. (2013). Explicet: graphical used interface software for metadata-driven management, analysis and visualization of microbiome data. Bioinformatics 29 3100–3101. 10.1093/bioinformatics/btt526 24021386
Rotabakk B. T., Birkeland S., Jeksrud W. K., Sivertsvik M., (2006). Effect of modified atmosphere packaging and soluble gas stabilization on the shelf life of skinless chicken breast fillets. J. Food Sci. 71 124–131. 10.1111/j.1365-2621.2006.tb08915.x
Rouger A., Moriceau N., Prévost H., Remenant B., Zagorec M., (2018). Diversity of bacterial communities in French chicken cuts stored under modified atmosphere packaging. Food Microbiol. 70 7–16. 10.1016/j.fm.2017.08.013 29173642
Rouger A., Remenant B., Prévost H., Zagorec M., (2017). A method to isolate bacterial communities and characterize ecosystems from food products: validation and utilization in as a reproductible chicken meat model. Int. J. Food Microbiol. 247 38–47. 10.1016/j.ijfoodmicro.2016.04.028 27184973
Saraiva C., Fontes M. C., Patarata L., Martins C., Cadavez V., Gonzalas-Barron U., (2016). Modelling the kinetics of Listeria monocytogenes in refrigerated fresh beef under different packaging atmospheres. Food Sci. Technol. 66 664–671. 10.1016/j.lwt.2015.11.026
Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 7537–7541. 10.1128/AEM.01541-09 19801464
Silbande A., Adenet S., Chopin C., Cornet J., Smith-Ravin J., Rochefort K., et al. (2018). Effect of vacuum and modified atmosphere packaging on the microbiological, chemical and sensory properties of tropical red drum (Sciaenops acellatus) fillets stored at 4°C. Int. J. Food Microbiol. 266 31–41. 10.1016/j.ijfoodmicro.2017.10.015 29161643
Silbande A., Adenet S., Smith-Ravin J., Joffraud J.-J., Rochefort K., Leroi F., (2016). Quality assessment of ice-stored tropical yellowfin tuna (Thunnu albacares) and influence of vacuum and modified atmosphere packaging. Food Microbiol. 60 62–72. 10.1016/j.fm.2016.06.016 27554147
Simpson R., Carevic E., (2004). Designing a modified atmosphere packaging system for foodservice portions on nonrespiring foods: optimal gas mixture and food/headspace ratio. Foodserv. Res. Int. 14 257–272. 10.1111/j.1745-4506.2004.tb00194.x
Singh V. P., (2018). Recent approaches in food bio-preservation – a review. Open Vet. J. 8 104–111. 10.4314/ovj.v8i1.16 29721439
Spanu C., Piras F., Mocci A. M., Nieddu G., De Santis E. P. L., Scarano C., (2018). Use of Carnobacterium spp. protective culture in MAP packed Ricotta fresca cheese to control Pseudomonas spp. Food Microbiol. 74 50–56. 10.1016/j.fm.2018.02.020 29706337
Stanborough T., Fegan N., Powell S. M., Tamplin M., Chandry P. S., (2017). Insight into the genome of Brochothrix thermosphacta, a problematic meat spoilage bacterium. Appl. Environ. Microbiol. 83 1–20. 10.1128/AEM.02786-16 27986732
Stefanovic E., Fitzgerald G., McAulliffe O., (2017). Advances in the genomics and metabolomics of dairy lactobacilli: a review. Food Microbiol. 61 33–49. 10.1016/j.fm.2016.08.009 27697167
Stellato G., La Storia A., De Filippis F., Borriello G., Villani F., Ercoloni D., (2016). Overlap of spoilage-associated microbiota between meat and the meat processing environment in small-scale and large-scale retail distributions. Appl. Environ. Microbiol. 82 4045–4054. 10.1128/AEM.00793-16 27129965
Stoddard S. F., Smith B. J., Hein R., Roller B. R. K., Schmidt T. M., (2015). rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 43 593–598. 10.1093/nar/gku1201 25414355
Stoops J., Ruyters S., Busschaert P., Spaepen R., Verreth C., Claes J., et al. (2015). Bacterial community dynamics during colt storage of minced meat packaged under modified atmosphere and supplemented with different preservatives. Food Microbiol. 48 192–199. 10.1016/j.fm.2014.12.012 25791008
Vester Lauritsen C., Kjeldgaard J., Ingmer H., Bisgaard M., Christensen H., (2019). Microbiota emcompassing putative spoilage bacteria in retail packaged broiler meat and commercial broiler abattoir. Int. J. Food Microbiol. 300 14–21. 10.1016/j.ijfoodmicro.2019.04.003 30991234
Woraprayote W., Malila Y., Sorapukdee S., Swetwiwathana A., Benjakul S., Visessanguan W., (2016). Bacteriocins from lactic acid bacteria and their applications in meat and meat products. Meat Sci. 120 118–132. 10.1016/j.meatsci.2016.04.004 27118166
Yoon S. H., Ha S. M., Kwon S., Lim J., Kim Y., Seo H., et al. (2017). Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol. 67 1613–1617. 10.1099/ijsem.0.001755 28005526
Zhao F., Zhou G., Ye K., Wang S., Xu X., Li C., (2015). Microbial changes in vacuum-packed chilled pork during storage. Meat Sci. 100 145–149. 10.1016/j.meatsci.2014.10.004 25460118
Zotta T., Parente E., Ianniello R. G., De Filippis F., Ricciardi A., (2019). Dynamics of bacterial communities and interaction networks in thawed fish fillets during chilled storage in air. Int. J. Food Microbiol. 293 102–113. 10.1016/j.ijfoodmicro.2019.01.008 30677559