Processing environment and ingredients are both sources of Leuconostoc gelidum, which emerges as a major spoiler in ready-to-eat meals

Applied and Environmental Microbiology

Volumn 81, Issue 10, 2015, Pages 3529-3541

  Pothakos, Vasileios ^a,b,c   Stellato, Giuseppina ^b   Ercolini, Danilo ^b   Devlieghere, Frank ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; LABORATORIES; LACTIC ACID; MICROORGANISMS; RNA;

ENTEROBACTERIACEAE; LACTIC ACID BACTERIA; MANUFACTURING PLANT; MICROBIAL COMMUNITIES; OPERATIONAL TAXONOMIC UNITS; PROCESSING ENVIRONMENTS; PRODUCTION BATCHES; REFRIGERATION TEMPERATURES;

BACTERIA;

BACTERIUM; COLONIZATION; FOOD PROCESSING; FOOD QUALITY; FOOD SAFETY; GENETIC ANALYSIS; GENOMICS; MICROBIAL COMMUNITY; NUCLEIC ACID ANALYSIS;

BROCHOTHRIX; ENTEROBACTERIACEAE; LACTOBACILLUS; LEUCONOSTOC GELIDUM; OTUS; PSEUDOMONAS; STREPTOCOCCACEAE;

ANALYSIS; ANIMAL; BACTERIUM; CLASSIFICATION; DEVICES; FAST FOOD; FOOD CONTAMINATION; FOOD HANDLING; FOOD SAFETY; FOOD STORAGE; GENETICS; ISOLATION AND PURIFICATION; LEUCONOSTOC; MEAT; MICROBIOLOGY; VEGETABLE;

ANIMALS; BACTERIA; FAST FOODS; FOOD CONTAMINATION; FOOD HANDLING; FOOD SAFETY; FOOD STORAGE; LEUCONOSTOC; MEAT; VEGETABLES;

EID: 84930027498     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03941-14     Document Type: Article

References (71)

1. Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M. 2002. Food spoilage-interactions between food spoilage bacteria. Int J Food Microbiol 78:79-97. http://dx.doi.org/10.1016/S0168-1605(02)00233-7.
2. Nychas G, Skandamis P, Tassou C, Koutsoumanis K. 2008. Meat spoilage during distribution. Meat Sci 78:77-89. http://dx.doi.org/10.1016/j .meatsci.2007.06.020.
3. Borch E, Kant-Muermans ML, Blixt Y. 1996. Bacterial spoilage of meat and cured meat products. Int J Food Microbiol 33:103-120. http://dx.doi .org/10.1016/0168-1605(96)01135-X.
4. Huisin't Veld J. 1996. Microbial and biochemical spoilage of foods: an overview. Int J Food Microbiol 33:1-18. http://dx.doi.org/10.1016/0168-1605(96)01139-7.
5. Pothakos V, Samapundo S, Devlieghere F. 2012. Total mesophilic counts underestimate in many cases the contamination levels of psychrotrophic lactic acid bacteria (LAB) in chilled-stored food products at the end of their shelf life. Food Microbiol 32:437-443. http://dx.doi.org/10.1016/j.fm.2012.07.011.
6. 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. http://dx.doi.org/10.1016/j .ijfoodmicro.2014.09.013.
7. Pothakos V, Snauwaert C, De Vos P, Huys G, Devlieghere F. 2014. Psychrotrophic members of Leuconostoc gasicomitatum, Leuconostoc gelidum and Lactococcus piscium dominate at the end of shelf life in packaged and chilled-stored food products in Belgium. Food Microbiol 39:61-67. http://dx.doi.org/10.1016/j.fm.2013.11.005.
8. Björkroth J, Holzapfel W. 2006. Genera Leuconostoc, Oenococcus and Weissella, p 267-319. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The prokaryotes. Springer, New York, NY.
9. Axelsson L. 2004. Lactic acid bacteria: classification and physiology. In Salminen S, von Wright A, Ouwehand A (ed), Lactic acid bacteria. Microbiological and functional aspects, 3rd ed. Marcel Dekker, New York, NY.
10. Makarova K, O'Sullivan O, O'Callaghan J, Sangrador-Vegas A, McAuliffe O, Slattery L, Kaleta P, Callanan M, Fitzgerald GF, Ross RP, Beresford T. 2006. Comparative genomics of lactic acid bacteria. Proc Natl Acad Sci U S A 103:15611-15616. http://dx.doi.org/10.1073/pnas .0607117103.
11. Björkroth J. 2005. Microbiological ecology of marinated meat products. Meat Sci 70:477-480. http://dx.doi.org/10.1016/j.meatsci.2004.07.018.
12. Vihavainen EJ, Björkroth KJ. 2009. Diversity of Leuconostoc gasicomitatum associated with meat spoilage. Int J Food Microbiol 136:32-36. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.09.010.
13. Martín A, Benito MJ, Hernández A, Pérez-Nevado F, Córdoba JJ, Córdoba MG. 2008. Characterisation of microbial deep spoilage in Iberian dry-cured ham. Meat Sci 78:475-484. http://dx.doi.org/10.1016/j .meatsci.2007.07.017.
14. Laursen BG, Leisner JJ, Dalgaard P. 2006. Carnobacterium species: effect of metabolic activity and interaction with Brochothrix thermosphacta on sensory characteristics of modified atmosphere packed shrimp. J Agric Food Chem 54:3604-3611. http://dx.doi.org/10.1021/jf053017f.
15. Ercolini D, Russo F, Torrieri E, Masi P, Villani F. 2006. Changes in the spoilage-related microbiota of beef during refrigerated storage under different packaging conditions. Appl Environ Microbiol 72:4663-4671. http://dx.doi.org/10.1128/AEM.00468-06.
16. Korkeala HJ, Björkroth JK. 1997. Microbiological spoilage and contamination of vacuum-packaged cooked sausages. J Food Prot 60:724-731.
17. Doulgeraki AI, Paramithiotis S, Kagkli DM, Nychas G-JE. 2010. Lactic acid bacteria population dynamics during minced beef storage under aerobic or modified atmosphere packaging conditions. Food Microbiol 27:1028-1034. http://dx.doi.org/10.1016/j.fm.2010.07.004.
18. Pin C, García De Fernando GD, Ordonez JA. 2002. Effect of modified atmosphere composition on the metabolism of glucose by Brochothrix thermosphacta. Appl Environ Microbiol 68:4441-4447. http://dx.doi.org /10.1128/AEM.68.9.4441-4447.2002.
19. Doulgeraki AI, Ercolini D, Villani F, Nychas G-JE. 2012. Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157:130-141. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.05.020.
20. Ercolini D. 2013. High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbial ecology. Appl Environ Microbiol 79:3148-3155. http://dx.doi.org/10.1128/AEM .00256-13.
21. Nieminen TT, Koskinen K, Laine P, Hultman J, Säde E, Paulin L, Paloranta A, Johansson P, Björkroth J, Auvinen P. 2012. Comparison of microbial communities in marinated and unmarinated broiler meat by metagenomics. Int J Food Microbiol 157:142-149. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.04.016.
22. 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. Int J Food Microbiol 142:120-131. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.06.012.
23. Casaburi A, Nasi A, Ferrocino I, Di Monaco R, Mauriello G, Villani F, Ercolini D. 2011. Spoilage-related activity of Carnobacterium maltaromaticum strains in air-stored and vacuum-packed meat. Appl Environ Microbiol 77:7382-7393. http://dx.doi.org/10.1128/AEM.05304-11.
24. Casaburi A, De Filippis F, Villani F, Ercolini D. 2014. Activities of strains of Brochothrix thermosphacta in vitro and in meat. Food Res Int 62:366-374. http://dx.doi.org/10.1016/j.foodres.2014.03.019.
25. Pothakos V, Nyambi C, Zhang B-Y, Papastergiadis A, De Meulenaer B, Devlieghere F. 2014. Spoilage potential of psychrotrophic lactic acid bacteria (LAB) species: Leuconostoc gelidum subsp. gasicomitatum and Lactococcus piscium, on sweet bell pepper (SBP) simulation medium under different gas compositions. Int J Food Microbiol 178:120-129. http://dx .doi.org/10.1016/j.ijfoodmicro.2014.03.012.
26. García-Gimeno RM, Zurera-Cosano G. 1997. Determination of readyto-eat vegetable salad shelf life. Int J Food Microbiol 36:31-38. http://dx .doi.org/10.1016/S0168-1605(96)01238-X.
27. Gutierrez J, Rodriguez G, Barry-Ryan C, Bourke P. 2008. Efficacy of plant essential oils against foodborne pathogens and spoilage bacteria associated with ready-to-eat vegetables: antimicrobial and sensory screening. J Food Prot 71:1846-1854.
28. Jacxsens L, Devlieghere F, Van der Steen C, Debevere J. 2001. Effect of high oxygen modified atmosphere packaging on microbial growth and sensorial qualities of fresh-cut produce. Int J Food Microbiol 71:197-210. http://dx.doi.org/10.1016/S0168-1605(01)00616-X.
29. Koo OK, Mertz AW, Akins EL, Sirsat SA, Neal JA, Morawicki R, Crandall PG, Ricke SC. 2013. Analysis of microbial diversity on deli slicers using polymerase chain reaction and denaturing gradient gel electrophoresis technologies. Lett Appl Microbiol 56:111-119. http://dx.doi .org/10.1111/lam.12021.
30. Ralyea RD, Wiedmann M, Boor KJ. 1998. Bacterial tracking in a dairy production system using phenotypic and ribotyping methods. J Food Prot 61:1336-1340.
31. Andreani NA, Martino ME, Fasolato L, Carraro L, Montemurro F, Mioni R, Bordin P, Cardazzo B. 2014. Tracking the blue: a MLST approach to characterise the Pseudomonas fluorescens group. Food Microbiol 39:116-126. http://dx.doi.org/10.1016/j.fm.2013.11.012.
32. Vangay P, Fugett EB, Sun Q, Wiedmann M. 2013. Food microbe tracker:a web-based tool for storage and comparison of food-associated microbes. J Food Prot 76:283-294. http://dx.doi.org/10.4315/0362-028X.JFP-12-276.
33. Björkroth KJ, Korkeala HJ. 1996. Evaluation of Lactobacillus sake contamination in vacuum-packaged sliced cooked meat products by ribotyping. J Food Prot 59:398-401.
34. Björkroth KJ, Korkeala HJ. 1997. Use of rRNA gene restriction patterns to evaluate lactic acid bacterium contamination of vacuum-packaged sliced cooked whole-meat product in a meat processing plant. Appl Environ Microbiol 63:448-453.
35. Lundström H-S, Björkroth KJ. 2011. Lactic acid bacteria associated with pig skin at pre-and post-scalding slaughter stages. Arch Lebensmittelhyg 62:26-31. http://dx.doi.org/10.2376/0003-925X-62-26.
36. Samelis J, Kakouri A, Georgiadou KG, Metaxopoulos J. 1998. Evaluation of the extent and type of bacterial contamination at different stages of processing of cooked ham. J Appl Microbiol 84:649-660. http://dx.doi .org/10.1046/j.1365-2672.1998.00392.x.
37. Vasilopoulos C, De Maere H, De Mey E, Paelinck H, De Vuyst L, Leroy F. 2010. Technology-induced selection towards the spoilage microbiota of artisan-type cooked ham packed under modified atmosphere. Food Microbiol 27:77-84. http://dx.doi.org/10.1016/j.fm.2009.08.008.
38. Pothakos V, Snauwaert C, De Vos P, Huys G, Devlieghere F. 2014. Monitoring psychrotrophic lactic acid bacteria contamination in a readyto-eat vegetable salad production environment. Int J Food Microbiol 185:7-16. http://dx.doi.org/10.1016/j.ijfoodmicro.2014.05.009.
39. De Filippis F, La Storia A, Villani F, Ercolini D. 2013. Exploring the sources of bacterial spoilers in beefsteaks by culture-independent highthroughput sequencing. PLoS One 8:e70222. http://dx.doi.org/10.1371/journal.pone.0070222.
40. Ercolini D, De Filippis F, La Storia A, Iacono M. 2012. "Remake" by high-throughput sequencing of the microbiota involved in the production of water buffalo mozzarella cheese. Appl Environ Microbiol 78:8142-8145. http://dx.doi.org/10.1128/AEM.02218-12.
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
42. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinfo rmatics/btq461.
43. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261-5267. http://dx.doi.org/10.1128/AEM .00062-07.
44. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610-618. http://dx.doi.org/10.1038/ismej.2011.139.
45. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814-821. http://dx.doi.org/10.1038/nbt.2676.
46. Xu Z, Malmer D, Langille MGI, Way SF, Knight R. 2014. Which is more important for classifying microbial communities: who's there or what they can do? ISME J 8:2357-2359. http://dx.doi.org/10.1038/ismej.2014.157.
47. Singh P, Wani AA, Saengerlaub S, Langowski H-C. 2011. Understanding critical factors for the quality and shelf life of MAP fresh meat: a review. Crit Rev Food Sci Nutr 51:146-177. http://dx.doi.org/10.1080/10408390903531384.
48. Stellato G, La Storia A, Cirillo T, Ercolini D. 2014. Bacterial biogeographical patterns in a cooking centre for hospital foodservice. Int J Food Microbiol 193:99-108. http://dx.doi.org/10.1016/j.ijfoodmicro.2014.10.018.
49. Gould GW. 1996. Methods for preservation and extension of shelf life. Int J Food Microbiol 33:51-64. http://dx.doi.org/10.1016/0168-1605(96)01133-6.
50. Gould GW. 2000. Preservation: past, present and future. Br Med Bull 56:84-96. http://dx.doi.org/10.1258/0007142001902996.
51. Abadias M, Usall J, Anguera M, Solsona C, Viñas I. 2008. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 123:121-129. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.12.013.
52. Doyle ME. 2007. Microbial food spoilage-losses and control strategies. Food Research Institute Briefings. Food Research Institute, University of Wisconsin-Madison, Madison, WI.
53. Vasilopoulos C, De Vuyst L, Leroy F. 11 October 2013. Shelf-life reduction as an emerging problem in cooked hams underlines the need for improved preservation techniques. Crit Rev Food Sci Nutr. http://dx.doi .org/10.1080/10408398.2012.695413.
54. Ercolini D, Russo F, Blaiotta G, Pepe O, Mauriello G, Villani F. 2007. Simultaneous detection of Pseudomonas fragi, P. lundensis, and P. putida from meat by use of a multiplex PCR assay targeting the carA gene. Appl Environ Microbiol 73:2354-2359. http://dx.doi.org/10.1128/AEM.02603-06.
55. Vihavainen EJ, Björkroth KJ. 2007. Spoilage of value-added, high-oxygen modified-atmosphere packaged raw beef steaks by Leuconostoc gasicomitatum and Leuconostoc gelidum. Int J Food Microbiol 119:340-345. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.08.029.
56. Jääskeläinen E, Johansson P, Kostiainen O, Nieminen T, Schmidt G, Somervuo P, Mohsina M, Vanninen P, Auvinen P, Björkroth J. 2013. Significance of heme-based respiration in meat spoilage caused by Leuconostoc gasicomitatum. Appl Environ Microbiol 79:1078-1085. http://dx.doi.org/10.1128/AEM.02943-12.
57. Lyhs U, Koort J, Lundström H-S, Björkroth KJ. 2004. Leuconostoc gelidum and Leuconostoc gasicomitatum strains dominated the lactic acid bacterium population associated with strong slime formation in an acetic-acid herring preserve. Int J Food Microbiol 90:207-218. http://dx .doi.org/10.1016/S0168-1605(03)00303-9.
58. Vihavainen EJ, Murros AE, Björkroth KJ. 2008. Leuconostoc spoilage of vacuum-packaged vegetable sausages. J Food Prot 71:2312-2315.
59. Nieminen TT, Vihavainen E, Paloranta A, Lehto J, Paulin L, Auvinen P, Solismaa M, Björkroth KJ. 2011. Characterization of psychrotrophic bacterial communities in modified atmosphere-packed meat with terminal restriction fragment length polymorphism. Int J Food Microbiol 144:360-366. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.10.018.
60. Björkroth KJ, Geisen R, Schillinger U, Weiss N, De Vos P, Holzapfel WH, Korkeala HJ, Vandamme P. 2000. Characterization of Leuconostoc gasicomitatum sp. nov., associated with spoiled raw tomato-marinated broiler meat strips packaged under modified-atmosphere conditions. Appl Environ Microbiol 66:3764-3772. http://dx.doi.org/10.1128/AEM .66.9.3764-3772.2000.
61. Jeong SH, Lee SH, Jung JY, Choi EJ, Jeon CO. 2013. Microbial succession and metabolite changes during long-term storage of kimchi. J Food Sci 78:M763-M769. http://dx.doi.org/10.1111/1750-3841.12095.
62. Cho J, Lee D, Yang C, Jeon J, Kim J, Han H. 2006. Microbial population dynamics of kimchi, a fermented cabbage product. FEMS Microbiol Lett 257:262-267. http://dx.doi.org/10.1111/j.1574-6968.2006.00186.x.
63. Matsui H, Tsuchiya R, Isobe Y, Narita M. 2013. Analysis of bacterial community structure in saba-narezushi (narezushi of mackerel) by 16S rRNA gene clone library. J Food Sci Technol 50:791-796. http://dx.doi.org /10.1007/s13197-011-0382-4.
64. Björkroth J, Korkeala H. 1997. Ropy slime-producing Lactobacillus sake strains possess a strong competitive ability against a commercial biopreservative. Int J Food Microbiol 38:117-123. http://dx.doi.org/10.1016/S0168-1605(97)00097-4.
65. Nerbrink E, Borch E. 1993. Evaluation of bacterial contamination at separate processing stages in emulsion sausage production. Int J Food Microbiol 20:37-44. http://dx.doi.org/10.1016/0168-1605(93)90058-O.
66. 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. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.02.022.
67. Pothakos V. 2014. Psychrotrophic lactic acid bacteria (LAB) as a source of fast spoilage occurring on packaged and cold-stored food products. Ph.D. dissertation. Ghent University, Ghent, Belgium.
68. Scott TM, Rose JB, Jenkins TM, Samuel R, Lukasik J, Farrah SR. 2002. Microbial source tracking: current methodology and future directions. Appl Environ Microbiol 68:5796-5803. http://dx.doi.org/10.1128/AEM .68.12.5796-5803.2002.
69. Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A. 2014. Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev 38:1-40. http://dx.doi.org/10.1111/1574-6976.12031.
70. Foley SL, Lynne AM, Nayak R. 2009. Molecular typing methodologies for microbial source tracking and epidemiological investigations of Gramnegative bacterial foodborne pathogens. Infect Genet Evol 9:430-440. http://dx.doi.org/10.1016/j.meegid.2009.03.004.
71. Säde E. 2011. Leuconostoc spoilage of refrigerated, packaged foods. Doctoral dissertation. Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland.