Impact of Lactobacillus curvatus 54M16 on microbiota composition and growth of Listeria monocytogenes in fermented sausages

Food Microbiology

Volumn 72, Issue , 2018, Pages 1-15

  Giello, Marina ^a   La Storia, Antonietta ^a   De Filippis, Francesca ^a   Ercolini, Danilo ^a   Villani, Francesco ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

16S rRNA; Anti listerial activity; Bacteriocins; Microbial community; Sausages

Indexed keywords

BACTERIOCIN;

ANALYSIS; ANIMAL; BACTERIUM; CLASSIFICATION; DRUG EFFECT; EVALUATION STUDY; FERMENTATION; FOOD PRESERVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOBACILLUS; LISTERIA MONOCYTOGENES; MEAT; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; PIG; PROCEDURES;

ANIMALS; BACTERIA; BACTERIOCINS; FERMENTATION; FOOD PRESERVATION; LACTOBACILLUS; LISTERIA MONOCYTOGENES; MEAT PRODUCTS; MICROBIOTA; SWINE;

EID: 85034066372     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2017.11.003     Document Type: Article

References (87)

1. Aasen, I.M., Markussen, S., Møretrø, T., Katla, T., Axelsson, L., Naterstad, K., Interactions of the bacteriocins sakacin P and nisin with food constituents. Int. J. Food Microbiol. 87 (2003), 35–43.
2. Andritsos, N.D., Mataragas, M., Paramithiotis, S., Eleftherios, H., Drosinos, E.H., Quantifying Listeria monocytogenes prevalence and concentration in minced pork meat and estimating performance of three culture media from presence/absence microbiological testing using a deterministic and stochastic approach. Food Microbiol. 36 (2013), 395–405.
3. Balciunas, E.M., Castillo Martinez, F.A., Todorov, S.D., de Melo Franco, B.D.G., Converti, A., de Souza Oliveira, R.P., Novel biotechnological applications of bacteriocins: a review. Food Control 32 (2013), 134–142.
4. Benjamini, Y., Hochberg, Y., Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57 (1995), 289–300.
5. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Meth. 7 (2010), 335–336.
6. Casaburi, A., De Filippis, F., Villani, F., Ercolini, D., Activities of strains of Brochothrix thermosphacta in vitro and in meat. Food Res. Int. 62 (2014), 366–374.
7. Casaburi, A., Di Martino, V., Ferranti, P., Picariello, L., Villani, F., Technological properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Control 59 (2016), 31–45.
8. Castro, M.P., Palavecino, N.Z., Herman, C., Garro, O.A., Campos, C.A., Lactic acid bacteria isolated from artisanal dry sausages: characterization of antibacterial compounds and study of the factors affecting bacteriocin production. Meat Sci. 87 (2011), 321–329.
9. Cocolin, L., Dolci, P., Rantsiou, K., Biodiversity and dynamics of meat fermentations: the contribution of molecular methods for a better comprehension of a complex ecosystem. Meat Sci. 89 (2011), 296–302.
10. Cocolin, L., Manzano, M., Cantoni, C., Comi, G., Denaturing gradient gel electrophoresis analysis of the 16S rRNA gene V1 region to monitor dynamic changes in the bacterial population during the fermentation of Italian sausages. Appl. Environ. Microbiol. 67 (2001), 5113–5121.
11. Comi, G., Urso, R., Iacumin, L., Rantsiou, K., Cattaneo, P., Cantoni, C., Cocolin, L., Characterisation of naturally fermented sausages produced in the North East of Italy. Meat Sci. 69 (2005), 381–392.
12. Cornu, M., Billoir, E., Bergis, H., Beaufort, A., Zuliani, V., Modelling microbial competition in food: application to the behavior of Listeria monocytogenes and lactic acid flora in pork meat products. Food Microbiol. 28 (2011), 639–647.
13. Corsetti, A., Settanni, L., Van Sinderen, D., Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. J. Appl. Microbiol. 96 (2004), 521–534.
14. De Cesare, A., Mioni, R., Manfreda, G., Prevalence of Listeria monocytogenes in fresh and fermented Italian sausages and ribotyping of contaminating strains. Int. J. Food Microbiol. 120 (2007), 124–130.
15. De Filippis, F., La Storia, A., Villani, F., Ercolini, D., Exploring the sources of bacterial spoilers in beefsteaks by culture-independent high-throughput sequencing. PLoS One, 8(7), 2013, e70222.
16. De Filippis, F., Pennacchia, C., Di Pasqua, R., Fiore, A., Fogliano, V., Villani, F., Ercolini, D., Decarboxylase gene expression and cadaverine and putrescine production by Serratia proteamaculans in vitro and in beef. Int. J. Food Microbiol. 165 (2013), 332–338.
17. De Filippis, F., Pellegrini, N., Vannini, L., Jeffery, I.B., La Storia, A., Laghi, L., Serrazanetti, D.I., Di Cagno, R., Ferrocino, I., Lazzi, C., Turroni, S., Cocolin, L., Brigidi, P., Neviani, E., Gobbetti, M., O'Toole, P.W., Ercolini, D., High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut 65 (2016), 1812–1821.
18. De Filippis, F., Pellegrini, N., Laghi, L., Gobbetti, M., Ercolini, D., Unusual sub-genus associations of faecal Prevotella and Bacteroides with specific dietary patterns. Microbiome, 4, 2016, 57.
19. de Souza Barbosa, M., Todorov, S.D., Ivanova, I., Chobert, J.M., Haertl, T., de Melo Franco, B.D., Improving safety of salami by application of bacteriocins produced by an autochthonous Lactobacillus curvatus isolate. Food Microbiol. 46 (2015), 254–262.
20. Dicks, L.M.T., Mellett, F.D., Hoffman, L.C., Use of bacteriocin-producing starter cultures of Lactobacillus plantarum and Lactobacillus curvatus in production of ostrich meat salami. Meat Sci. 66 (2004), 703–708.
21. Dogan, B., Boor, K.J., Genetic diversity and spoilage potentials among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Appl. Environ. Microbiol. 69:1 (2003), 130–138.
22. Dortu, C., Huch, M., Holzapfel, W.H., Franz, C.M.A.P., Thonart, P., Anti-listerial activity of bacteriocin-producing Lactobacillus curvatus CWBI-B28 and Lactobacillus sakei CWBI-B1365 on raw beef and poultry meat. Lett. Appl. Microbiol. 47 (2008), 581–586.
23. Doulgeraki, A.I., Ercolini, D., Villani, F., Nychas, G.J., Spoilage microbiota associated to the storage of raw meat in different conditions. Int. J. Food Microbiol. 157:2 (2012), 130–141.
24. Durlu-Özkaya, F., Ayhan, K., Vural, N., Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Sci. 58:2 (2001), 163–166.
25. EFSA, The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J., 14, 2016, 4364.
26. Ercolini, D., Casaburi, A., Nasi, A., Ferrocino, I., Di Monaco, R., Ferranti, P., Mauriello, G., Villani, F., Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. Int. J. Food Microbiol. 142:1–2 (2010), 120–131.
27. Eren, A.M., Maignien, L., Sul, W.L., Murphy, L.G., Grim, S.L., Morrison, H.G., Sogin, M.L., Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Meth. Ecol. Evol. 4:12 (2013), 1111–1119.
28. Eren, M.A., Sogin, M.L., Morrison, H.G., Vineis, J.H., Fisher, J.C., Newton, R.J., McLellan, S.L., A single genus in the gut microbiome reflects host preference and specificity. ISME J. 9:1 (2015), 90–100.
29. European Commission, Commission Regulation (EC) N° 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union L338 (2005), 1–26.
30. Fontana, C., Bassi, D., López, C., Pisacane, V., Otero, M.C., Puglisi, E., Rebecchi, A., Cocconcelli, P.S., Vignolo, G., Microbial ecology involved in the ripening of naturally fermented llama meat sausages. A focus on lactobacilli diversity. Int. J. Food Microbiol. 236 (2016), 17–25.
31. Galvez, A., Abriouel, H., Benomar, N., Lucas, R., Microbial antagonists to food-borne pathogens and biocontrol. Curr. Opin. Biotechnol. 21 (2010), 142–148.
32. Gao, Y., Li, D., Liu, X., Lactobacillus sakei C2 as starter culture in fermented sausages. Food Control 35 (2014), 1–6.
33. Garriga, M., Aymerich, T., The microbiology of fermentation and ripening. Toldrá, Fidel, (eds.) Handbook of Fermented Meat and Poultry, second ed., 2015, John Wiley & Sons, Ltd, 107–115.
34. Gevers, D., Huys, G., Swings, J., Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol. Lett. 205 (2001), 31–36.
35. Greppi, A., Ferrocino, I., La Storia, A., Rantsiou, K., Ercolini, D., Cocolin, L., Monitoring of the microbiota of fermented sausages by culture independent rRNA-based approaches. Int. J. Food Microbiol. 212 (2015), 67–75.
36. Han, E.J., Lee, N.K., Choi, S.Y., Paik, H.D., Short communication: bacteriocin KC24 produced by Lactococcus lactis KC24 from kimchi and its antilisterial effect in UHT milk. J. Dairy Sci. 96 (2013), 101–104.
37. Huang, Y., Ye, K., Yu, K., Wang, K., Zhou, G., The potential influence of two Enterococcus faecium on the growth of Listeria monocytogenes. Food Control 67 (2016), 18–24.
38. ISO (International Organization for Standardization), ISO 11290-1:1996. Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Listeria Monocytogenes - Part 1: Detection Method. (LI). 1996.
39. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., Glöckner, F.O., Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res., 41(1), 2013, e1, 10.1093/nar/gks808.
40. Kingcha, Y., Tosukhowong, A., Zendo, T., Roytrakul, S., Luxananil, P., Chareonpornsook, K., Valyasevi, R., Sonomoto, K., Visessanguan, W., Anti-listeria activity of Pediococcus pentosaceus BCC 3772 and application as starter culture for Nham, a traditional fermented pork sausage. Food Control 25 (2012), 190–196.
41. Koskey, A.M., Fisher, J.C., Eren, A.M., Ponce-Terashima, R., Reis, M.G., Blanton, R.E., McLellan, S.L., Blautia and Prevotella sequences distinguish human and animal fecal pollution in Brazil surface waters. Environ. Microbiol. 6:6 (2014), 696–704.
42. Lee, H.M., Lee, Y., A differential medium for lactic acid-producing bacteria in a mixed culture. Lett. Appl. Microbiol. 46 (2008), 676–681.
43. Leroy, F., Lievens, K., De Vuyst, L., Modelling bacteriocin resistance and inactivation of Listeria innocua LMG 13568 by Lactobacillus sakei CTC 494 under sausage fermentation conditions. Appl. Environ. Microbiol. 71 (2005), 7567–7570.
44. Macwana, S.J., Muriana, P.M., A ‘bacteriocin PCR array’ for identification of bacteriocin-related structural genes in lactic acid bacteria. J. Microbiol. Meth. 88 (2012), 197–204.
45. Magoc, T., Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:21 (2011), 2957–2963.
46. Martín, B., Garriga, M., Hugas, M., Aymerich, T., Genetic diversity and safety aspects of Enterococci from slightly fermented sausages. J. Appl. Microbiol. 98 (2005), 1177–1190.
47. Martins, E.A., Germano, P.M.L., Listeria monocytogenes in ready-to-eat, sliced, cooked ham and salami products, marketed in the city of São Paulo, Brazil: occurrence, quantification, and serotyping. Food Control 22 (2011), 297–302.
48. Mataragas, M., Bellio, A., Rovetto, F., Astegiano, S., Greci, C., Hertel, C., Decastelli, L., Cocolin, L., Quantification of persistence of the food-borne pathogens Listeria monocytogenes and Salmonella enterica during manufacture of Italian fermented sausages. Food Control 47 (2015), 552–559.
49. Mataragas, M., Zwietering, M.H., Skandamis, P.N., Drosinos, E.H., Quantitative microbiological risk assessment as a tool to obtain useful information for risk managers - specific application to Listeria monocytogenes and ready-to-eat meat products. Int. J. Food Microbiol. 141 (2010), S170–S179.
50. Mauriello, G., Villani, F., Bacteriocins in plastics. Lagaròn, J.M., Zapata, M.J.O., Lopez-Rubio, A., (eds.) Antimicrobial Polymers, first ed., 2012, John Wiley & Sons, Inc, 117–158.
51. McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., Andersen, G.L., Knight, R., Hugenholtz, P., An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:3 (2012), 610–618.
52. Mellefont, L.A., McMeekin, T.A., Ross, T., Effect of relative inoculum concentration on Listeria monocytogenes growth in co-culture. Int. J. Food Microbiol. 121 (2008), 157–168.
53. Meloni, D., Presence of Listeria monocytogenes in mediterranean-style dry fermented sausages. Foods 4 (2015), 34–50.
54. Messens, W., Leroy, F., De Vuyst, L., Modelling growth and bacteriocin production by Lactobacillus curvatus LTH 1174 in response to temperature and pH values used for European sausage fermentation processes. Int. J. Food Microbiol. 81 (2003), 41–52.
55. Minayo, G., Gutierrez-Fernandez, A.J., de la Torre, A.H., The effect of the pediocin PA-1 produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens in Spanish dry-fermented sausages and frankfurters. Food Control 21 (2010), 679–685.
56. Mirhosseini, M., Nahvi, I., Emtiazi, G., Tavassoli, M., Characterisation of anti-Listeria monocytogenes bacteriocins from Enterococcus faecium strains isolated from dairy products. International J. Dairy Technol. 63 (2013), 55–61.
57. Nilsson, L., Hansen, T.B., Garrido, P., Buchrieser, C., Glaser, Knøchel S., Gram, L., Gravesen, A., Growth inhibition of Listeria monocytogenes by a non bacteriocinogenic Carnobacterium piscicola. J. Appl. Microbiol. 98 (2005), 172–183.
58. Nychas, G.J., Skandamis, P.N., Tassou, C.C., Koutsomanis, K.P., Meat spoilage during distribution. Meat Sci. 78:1–2 (2008), 77–89.
59. Papadimitriou, K., Pot, B., Tsakalidou, E., How microbes adapt to a diversity of food niches. Curr. Opi. Food Sci. 2 (2015), 29–35.
60. Peccio, A., Autio, T., Korkeala, H., Rosmini, R., Trevisani, M., Listeria monocytogenes occurrence and characterization in meat-producing plants. Lett. Appl. Microbiol. 37 (2003), 234–238.
61. Petruzzelli, A., Blasi, G., Masini, L., Calza, L., Duranti, A., Santarelli, S., Fisichella, S., Pezzotti, G., Aquilanti, L., Osimani, A., Tonucci, F., Occurrence of Listeria monocytogenes in salami manufactured in the Marche Region (Central Italy). J. Vet. Med. Sci. 72 (2010), 499–502.
62. Pleasants, A.B., Soboleva, T.K., Dykes, G.A., Jones, R.J., Filippov, A.E., Modelling of the growth of populations of Listeria monocytogenes and a bacteriocin-producing strain of Lactobacillus in pure and mixed cultures. Food Microbiol. 18 (2001), 605–615.
63. Połka, J., Rebecchi, A., Pisacane, V., Morelli, L., Puglisi, E., Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16S rRNA amplicons. Food Microbiol. 46 (2015), 342–356.
64. Puolanne, E., Petäjä-Kanninen, E., Toldrá, Fidel, (eds.) Principles of Meat Fermentation Handbook of Fermented Meat and Poultry, second ed., 2015, John Wiley & Sons, Ltd.
65. Ravyts, F., Barbuti, S., Frustoli, M.A., Parolari, G., Saccani, G., De Vuyst, L., Leroy, F., Competitiveness and antibacterial potential of bacteriocin-producing starter Cultures in different types of fermented sausages. J. Food Prot. 71 (2008), 1817–1827.
66. Remiger, A., Ehrmann, M.A., Vogel, R.F., Identification of bacteriocin-encoding genes in lactobacilli by polymerase chain reaction (PCR). Syst. Appl. Microbiol. 19 (1996), 28–34.
67. Rossetti, L., Giraffa, G., Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. J. Microbiol. Meth. 63 (2005), 135–144.
68. Saraoui, T., Fall, P.A., Leroi, F., Antignac, J.-P., Chéreau, S., Pilet, M.F., Inhibition mechanism of Listeria monocytogenes by a bioprotective bacteria Lactococcus piscium CNCM I-4031. Food Microbiol. 53 (2016), 70–78.
69. Schillinger, U., Kaya, M., LÏcke, F.K., Behaviour of Listeria monocytogenes in meat and its control by a bacteriocin-producing strain of Lactobacillus sake. J. Appl. Bacteriol. 70 (1991), 473–478.
70. Schmieder, R., Edwards, R., Quality control and preprocessing of metagenomics datasets. Bioinformatics 27:6 (2011), 863–864.
71. StataCorp, Stata Statistical Software: Release 13. 2013, StataCorp LP, College Station, TX.
72. Stellato, G., La Storia, A., De Filippis, F., Borriello, G., Villani, F., Ercolini, D., Overlap of spoilage-associated microbiota between meat and meat processing environment in small-scale and large-scale retail distribution. Appl. Environ. Microbiol. 82:13 (2016), 4045–4054.
73. Stellato, G., Utter, D.R., Voorhis, A., De Angelis, M., Eren, A.M., Ercolini, D., A few Pseudomonas oligotypes dominate in the meat and dairy processing environment. Front. Microbiol., 8, 2017, 264.
74. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30:12 (2013), 2725–2729.
75. Thévenot, D., Delignette-Muller, M.L., Christieans, S., Vernozy-Rozand, C., Fate of Listeria monocytogenes in experimentally contaminated French sausages. Int. J. Food Microbiol. 101 (2005), 189–200.
76. Thévenot, D., Dernburg, A., Vernozy-Roland, C., An updated review of Listeria monocytogenes in the pork meat industry and its products. J. Appl. Microbiol. 101 (2006), 7–17.
77. Urso, R., Rantsiou, K., Cantoni, C., Comi, G., Cocolin, L., Technological characterization of a bacteriocin-producing Lactobacillus sakei and its use in fermented sausages production. Int. J. Food Microbiol. 110 (2006), 232–239.
78. Vaughan, A., Eijsink, V.G., Van Sinderen, D., Functional characterization of a composite bacteriocin locus from malt isolate Lactobacillus sakei 5. Appl. Environ. Microbiol. 69 (2003), 7194–7203.
79. Vaughan, A., O’ Mahony, J., Vincent, G.H., Eijsink, V.G.H., O’ Connell-Motherway, M., Douwe van Sinderen, D., Transcriptional analysis of bacteriocin production by malt isolate Lactobacillus sakei 5. FEMS Microbiol. Lett. 235 (2004), 377–384.
80. Verluyten, J., Messens, W., De Vuyst, L., The curing agent sodium nitrite, used in the production of fermented sausages, is less inhibiting to the bacteriocin-producing meat starter culture Lactobacillus curvatus LTH 1174 under anaerobic conditions. Appl. Environ. Microbiol. 69 (2003), 3833–3839.
81. Vignolo, G., Castellano, P., Fadda, S., Bioprotective cultures. Toldrá, Fidel, (eds.) Handbook of Fermented Meat and Poultry, second ed., 2015, John Wiley & Sons, Ltd, 129–138.
82. Villani, F., Casaburi, A., Pennacchia, C., Filosa, L., Russo, F., Ercolini, D., The microbial ecology of the Soppressata of Vallo di Diano, a traditional dry fermented sausage from Southern Italy, and in vitro and in situ selection of autochthonous starter cultures. Appl. Environ. Microbiol. 73 (2007), 5453–5463.
83. Villani, F., Pepe, O., Mauriello, G., Salzano, G., Moschetti, G., Coppola, S., Antilisterial activity of thermophilin 347, a bacteriocin produced by Streptococcus thermophilus. Int. J. Food Microbiol. 25 (1995), 179–190.
84. Wang, S., Weller, D., Falardeau, J., Strawn, L.K., Mardones, F.O., Adell, A.D., Switt, A.I.M., Food safety trends: From globalization of whole genome sequencing to application of new tools to prevent foodborne diseases. Trends Food Sci. Technol. 57 (2016), 188–198.
85. Weisburg, W.G., Barns, S.M., Pelletier, D.A., Lane, D.J., 16S Ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173 (1991), 697–703.
86. Woraprayote, W., Malila, Y., Sorapukdee, S., Swetwiwathan, A., Benjakul, S., Visessanguan, W., Bacteriocins from lactic acid bacteria and their applications in meat and meat products. Meat Sci. 120 (2016), 118–132.
87. Zhang, J., Liu, G., Li, P., Qu, Y., Pentocin 31-1, a novel meat-borne bacteriocin and its application as biopreservative in chill-stored tray-packaged pork meat. Food Control 21 (2010), 198–202.