Origin and ecological selection of core and food-specific bacterial communities associated with meat and seafood spoilage

ISME Journal

Volumn 9, Issue 5, 2015, Pages 1105-1118

  Chaillou, Stéphane ^a   Chaulot Talmon, Aurélie ^a   Caekebeke, Hélène ^b   Cardinal, Mireille ^c   Christieans, Souad ^d   Denis, Catherine ^e   Hélène Desmonts, Marie ^f   Dousset, Xavier ^g,h   Feurer, Carole ⁱ   Hamon, Erwann ^f   Joffraud, Jean Jacques ^c   La Carbona, Stéphanie ^e   Leroi, Françoise ^c   Leroy, Sabine ^j   Lorre, Sylvie ^k   Macé, Sabrina ^g,h   Pilet, Marie France ^g,h   Prévost, Hervé ^g,h   Rivollier, Marina ^d   Roux, Dephine ^b   Talon, Régine ^j   Zagorec, Monique ^g,h   Champomier Vergès, Marie Christine ^a   more..

^a UMR1319 MICALIS   (France)

^b Plate Forme d'Innovation Nouvelles Vagues   (France)

^c IFREMER   (France)

^d ADIV   (France)

^e Actalia   (France)

^f Aélrial   (France)

^g Ecole Nationale d'Ingenieurs des Techniques des Industries Agricoles et Alimentaires ENITIAA   (France)

^h LUNAM UNIVERSITÉ   (France)

ⁱ IFIP   (France)

^j CEMAGREF   (France)

^k Biocélane   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; CLADISTICS; DOMINANCE; FOOD SAFETY; GROWTH RATE; MICROBIAL COMMUNITY; RNA; TAXONOMY; TEMPERATURE EFFECT;

EUROPE;

ANIMALIA; BACTERIA (MICROORGANISMS); OTUS;

RNA 16S;

ANIMAL; BACTERIUM; CLASSIFICATION; DNA BARCODING; EUROPE; FOOD CONTAMINATION; FOOD CONTROL; GENETICS; MEAT; MICROBIOLOGY; MICROFLORA; POLYMERASE CHAIN REACTION; SEA FOOD;

ANIMALS; BACTERIA; DNA BARCODING, TAXONOMIC; EUROPE; FOOD CONTAMINATION; FOOD MICROBIOLOGY; MEAT; MICROBIOTA; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEAFOOD;

EID: 84928587445     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.202     Document Type: Article

References (91)

1. Argyri AA, Doulgeraki AI, Blana VA, Panagou E, Nychas GJE. (2001). Potential of simple HPLC-based approach for the identification of the spoilage status of minced beef stored at various temperature and packaging systems. Int J Food Microbiol 150: 25-33
2. Baele M, Vancanneyt M, Devriese LA, Lefebvre K, Swings J, Haesebrouck F. (2003). Lactobacillus ingluviei sp. nov., isolated from theintestinal tract of pigeons. Int J Syst Evol Microbiol 53: 133-136
3. Banat IM, Marchant R, Rahman TJ. (2004). Geobacillus debilis sp. nov., a novel obligately thermophilic bacterium isolated from a cool soil environment, and reassignment of Bacillus pallidus to Geobacillus pallidus comb. nov. Int J Syst Evol Microbiol 54: 2197-2201
4. Barott KL, Rodriguez-Brito B, Janouskovec J, Marhaver KL, Smith JE, Keeling P et al. (2011). Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13: 1192-1204
5. Borch E, Kant-Muermans ML, Blixt Y. (1996). Bacterial spoilage of meat and cured meat products. Int J Food Microbiol 33: 103-120
6. Boziaris IS, Stamatiou AP, Nychas GJE. (2012). Microbial aspects and shelf life of processed seafood products. J Sci Food Agric 93: 1184-1190
7. Broekaert K, Heyndrickx M, Herman L, Devlieghere F, Vlaemynck G. (2011). Seafood quality analysis: Molecular identification of dominant microbiota afterice storage on several general growth media. Food Microbiol 28: 1162-1169
8. Broekaert K, Heyndrickx M, Herman L, Devlieghere F, Vlaemynck G. (2013). Molecular identification of the microbiota of peeled and unpeeled brown shrimp (Crangon crangon) during storage on ice and at 7.5 degrees C. Food Microbiol 36: 123-134
9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-Throughput community sequencing data. Nat Methods 7: 335-336
10. Chao A. (1984). Nonparametric estimation of the number of classes in a population. Scand J Stat 11: 783-791
11. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145
12. 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
13. Dalgaard P. (1995). Qualitative and quantitative characterization of spoilage bacteria from packed fish. Int J Food Micriobiol 19: 283-294
14. Dalgaard P. (1998). Methods to determine the freshness of fish in research and industry. In Evaluation of fish freshness 166-174
15. Dixon P. (2003). VEGAN, a package of R functions for community ecology. J Veg Sci 14: 927-930
16. Doulgeraki AI, Ercolini D, Villani F, Nychas GJ. (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157: 130-141
17. Emborg J, Laursen BG, Rathjen T, Dalgaard P. (2002). Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmosphere-packed salmon (Salmo salar) at 2 degreesC. J Appl Microbiol 92: 790-799
18. EUFOMA (2014). The EU Fish market. http: //ec.europa. eu/fisheries/market-observatory/documents/10157/bf18cf2c-1b33-440d-8870-e05b2644b58b
19. 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
20. Ercolini D, Russo F, Nasi A, Ferranti P, Villani F. (2009). Mesophilic and psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Appl Environ Microbiol 75: 1990-2001
21. Funaro CF, Kronauer DJ, Moreau CS, Goldman-Huertas B, Pierce NE, Russell JA. (2011). Army ants harbor a host-specific clade of Entomoplasmatales bacteria. Appl Environ Microbiol 77: 346-350
22. Gram L, Huss HH. (1996). Microbiological spoilage of fish and fish products. Int J Food Microbiol. 33: 121-137
23. Gill CO, Tan KH. (1980). Effect of Carbon dioxide on growth of meat spoilage bacteria. Appl Environ Microbiol 39: 317-319
24. Gouy M, Guindon S, Gascuel O. (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224
25. Gram L, Dalgaard P. (2002). Fish spoilage bacteria-problems and solutions. Curr Opin Biotechnol 13: 262-266
26. Guindon Sp, Dufayard J-Fo, Lefort V, Anisimova M, Hordijk W, Gascuel O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59: 307-321
27. Guri M, Durand L, Cueff-Gauchard V, Zbinden M, Crassous P, Shillito B et al. (2012). Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. ISME J 6: 597-609
28. Hamady M, Lozupone C, Knight R. (2010). Fast UniFrac: facilitating high-Throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27
29. Hansen GH, Olafsen JA. (1999). Bacterial interactions in eraly life stages of marine cold water fish. Microb Ecol 38: 1-26
30. Hovda MB, Lunestad BT, Sivertsvik M, Rosnes JT. (2007). Characterisation of the bacterial flora of modified atmosphere packaged farmed Atlantic cod (Gadus morhua) by PCR-DGGE of conserved 16S rRNA gene regions. Int J Food Microbiol 117: 68-75
31. Ismail SAS, Deak T, Abd El-Rahman HA, Yassien MAM, Beuchat LR. (2000). Presence and changes in population of yeasts on raw and processed poultry products stored at refrigerated temperature. Int J Food Microbiol 62: 113-121
32. Jaffrès E. Sohier D, Pilet MF, Prévost H, Joffraud JJ, Dousset X. 2009). Study of the bacterial ecosystem in tropical cooked and peeled shrimps using a polyphasic approach. Int J Food Microbiol 131 20-29
33. Jaffrès E, Lalanne V, Mace S, Cornet J, Cardinal M, Serot T et al. 2011). Sensory characteristics of spoilage and volatile compounds associated with bacteria isolated from cooked and peeled tropical shrimps using SPMEGC-MS analysis. Int J Food Microbiol 147 195-202
34. Fredrickson J, Romine MF, Beliaev AF JM, Driscoll ME, Gardner TS et al. (2008). Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6: 592-603
35. Jackson TC, Marshall DL, Acuff GR, Dickson JS. (2001). Meat, poultry and seafood. In Doyle MP et al. (ed) Food Microbiology: Fundamentals and Frontiers, 2nd edn. ASM press: Washington, D.C., USA 91-109
36. Jami E, Israel A, Kotser A, Mizrahi I. (2013). Exploring the bovine rumen bacterial community from birth to adulthood. ISME J 7: 1069-1079
37. Jiang Y, Gao F, Xu X, Ye K, Zhou G. (2011). Changes in the composition of the bacterial flora on tray-packagedpork during chilled storage analyzed by PCR-DGGE and real-Time PCR. J Food Sci 76: M27-M33
38. Joffraud JJ, Cardinal M, Cornet J, Chasles JS, Leon S, Gigout F et al. (2006). Effect of bacterial interactions on the spoilage of cold-smoked salmon. Int J Food Microbiol 112: 51-61
39. Kanerva M. (2013). Meat consumption in Europe. Issues, trends and debateshttp: //www.academia.edu/2486553/Meat-consumption-in-Europe-Issues-Trends-And-debates
40. Kato Y, Sakala RM, 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 Evol Microbiol 50: 1143-1149
41. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H et al. (2012). Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62: 716-721
42. Kostanjsek R, Strus J, Avgustin G. (2007). "Candidatus Bacilloplasma, "a novel lineage of Mollicutes associated with the hindgut wall of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). Appl Environ Microbiol 73: 5566-5573
43. Labadie J. (1999). Consequences of packaging on bacterial growth.Meat is an ecological niche. Meat Sci 52: 299-305
44. Lane DJ. (1991). 16S/23S rRNA sequencing. In. Stackebrandt E, Goodfellow M (eds) Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons: New York, NY, USA, pp 115-175
45. Leisner JJ, Laursen BG, Prevost H, Drider D, Dalgaard P. (2007). Carnobacterium: positive and negative effects in the environment and in foods. FEMS Microbiol Rev 31: 592-613
46. Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. (2010). Comparative analysis of the bacterial microbiota of the human Nostril and Oropharynx. MBio 1: e00129-10
47. Leroi F, Joffraud JJ, Chevalier F, Cardinal M. (1998). Study of the microbial ecology of cold-smoked salmon during storage at 81C. Int J Food Microbiol 39: 111-121
48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079
49. Li W, Godzik A. (2006). Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659
50. Lu J, Sanchez S, Hofacre C, Maurer JJ, Harmon BG, Lee MD. (2003). Evaluation of broiler litter with reference to the microbial composition as assessed by using 16S rRNA and functional gene markers. Appl Environ Microbiol 69: 901-908
51. Lu XM, Lu PZ, Zhang H. (2013). Bacterial communities in manures of piglets and adult pigs bred with different feeds revealed by 16S rDNA 454 pyrosequencing. Appl Microbiol Biotechnol. 98: 2657-2665
52. Lun Z-R, Wang Q-P, Chen X-G, Li A-X, Zhu X-Q. (2007). Streptococcus suis: An emerging zoonotic pathogen. Lancet Infect Dis 7: 201-209
53. MacéS, Joffraud JJ, Cardinal M, Malcheva M, Cornet J, Lalanne V et al. (2013). Evaluation of the spoilage potential of bacteria isolated from spoiled raw salmon (Salmo salar) fillets stored under modified atmosphere packaging. Int J Food Microbiol 160: 227-238
54. Marchant R, Banat IM, Rahman TJ, Berzano M. (2002). What are high-Temperature bacteria doing in cold environments?. Trends Microbiol 10: 120-121
55. Matamoros S ,Leroi F. Cardinal M. Gigout F. Kasbi Chadli F. Cornet J. et al. 2009. Psychrotrophic lactic acid bacteria used to improve the safety and quality of vacuum-packaged cooked and peeled tropical shrimp and cold-smoked salmon J Food Prot 72 365-374
56. Mejlhom O, Bøknaes N, Dalgaard P. (2005). Shelf life and safety aspects of chilled cooked and peeled shrimps (Pandalus borealis) in modified atmospherepackaging. J Appl Microbiol 99: 66-76
57. Munoz R, Yarza P, Ludwig W, Euzeby J, Amann R, Schleifer KH et al. (2011). Release LTPs104 of the All-Species Living Tree. Syst Appl Microbiol 34: 169-170
58. Nechitaylo TY, Timmis KN, Golyshin PN. (2009). 'Candidatus Lumbricincola', a novel lineage of uncultured Mollicutes from earthworms of family Lumbricidae. Environ Microbiol 11: 1016-1026
59. NF V01-003. (2010). Food safety - Guidelines for implementing microbiological durability tests-Chilled perishable and highly perishable foodstuffs. http: //www.boutique.afnor.org/norme/nf-v01-003/hygienedes-Aliments-lignes-directrices-pour-la-realisationde-Tests-de-vieillissement-microbiologique-Alimentsperissables-/article/675928/fa163631
60. Nicholson WL, Krivushin K, Gilichinsky D, Schuerger AC. (2013). Growth of Carnobacterium spp. from permafrost under low pressure, temperature, and anoxic atmosphere has implications for Earth microbes on Mars. Proc Natl Acad Sci USA 110: 666-671
61. Nieminen TT, Koskinen K, Laine P, Hultman J, Sade 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
62. Nielsen DS, Jacobsen T, Jespersen L, Granly Koch A, Arneborg N. (2008). Occurence of growth yeasts in processed meat products - Implications for potential spoilage. Meat Sci 80: 919-926
63. Nychas G-JE, Skandamis PN, Tassou CC, Koutsoumanis KP. (2008). Meat spoilage during distribution. Meat Sci 78: 77-89
64. Olofsson TC, Ahrne S, Molin G. (2007). The bacterial flora of vacuum-packed cold-smoked salmon stored at 7 degrees C, identified by direct 16S rRNA gene analysis and pure culture technique. J Appl Microbiol 103: 109-119
65. Olsson C, Ahrne S, Pettersson B, Molin G. (2003). The bacterial flora of fresh and chill-stored pork: Analysis by cloning and sequencing of 16S rRNA genes. Int J Food Microbiol 83: 245-252
66. Patsias A, Chouliara I, Badeka A, Savvaidis IN, Kontonimas MG. (2006). Shelf-life of a chilled precooked chicken product stored in air andunder modified atmospheres: microbiological, chemical, sensory attributes. Food Microbiol 23: 423-429
67. Petersen LM, Tisa LS. (2013). Friend or foe?. A review of the mechanisms that drive Serratia towards diverse lifestyles. Can J Microbiol 59: 627-640
68. Pothakos V, Snauvaert C, De Vos P, Huys G, Devlieghere F. (2014). Psychrothrophic 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
69. Pruesse E, Peplies J, Glockner FO. (2012). SINA: Accurate high-Throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829
70. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al. (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596
71. R Development Core Team (2010). R. a language and environment for statistical computing. R Foundation for Statistical Computing: Vienna, Austria
72. Rahkila R, Nieminen T, Johansson P, Sade E, Bjorkroth 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
73. Reynisson E, Lauzon HL, Magnusson H, Jonsdottir R, Olafsdottir G, Marteinsson V et al. (2009). Bacterial composition and succession during storage of North-Atlantic cod (Gadus morhua) at superchilled temperatures. BMC Microbiol 9: 250
74. Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T et al. (2008). Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10: 727-737
75. Rodrigues DF, Ivanova N, He Z, HuebnerM, Zhou J, Tiedje JM. (2008). Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: A genome and transcriptome approach. BMC Genomics 9: 547
76. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K et al. (2011). Evidence for a core gut microbiota in the zebrafish. ISME J 5: 1595-1608
77. Rudi K, Maugeste T, Hannevick SE, Nissen H. (2004). Explorative multivariate analyses of 16S rRNA gene data from microbial communities in modifiedatmosphere-packed salmon and coalfish. Appl Environ Microbiol 70: 5010-5018
78. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106: 21 236-21241
79. Russell J.A. Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106: 21 236-21241
80. Sade E, Murros A, Bjorkroth J. (2013). Predominant enterobacteria on modified-Atmosphere packaged meat and poultry. Food Microbiol 34: 252-258
81. Sakala RM, Kato Y, Hayashidani H, Murakami M, Kaneuchi C, Ogawa M. (2002). Lactobacillus fuchuensis sp. nov., isolated from vacuum-packaged refrigerated beef. Int J Syst Evol Microbiol 52: 1151-1154
82. Sammon JW. (1969). A nonlinear mapping for data structure analysis. IEEE Trans Comput 18: 401-402
83. Schommer NN, Gallo RL. (2013). Structure and function of the human skin microbiome. Trends Microbiol 21: 660-668
84. Schuerger AC, Ulrich R, Berry BJ, Nicholson WL. (2013). Growth of Serratia liquefaciens under 7 mbar, 0 degrees C, and CO2-enriched anoxic atmospheres. Astrobiology 13: 115-131
85. Stohr R, Waberski A, Liesack W, Volker H, Wehmeyer U, Thomm M. (2001). Hydrogenophilus hirschii sp. nov., a novel thermophilic hydrogen-oxidizing beta-proteobacterium isolated from Yellowstone National Park. Int J Syst Evol Microbiol 51: 481-488
86. Sullam KE, Essinger SD, Lozupone CA, O'Connor MP, Rosen GL, Knight R et al. (2012). Environmental and ecological factors that shape the gut bacterial communities of fish: A meta-Analysis. Mol Ecol 21: 3363-3378
87. Suzuki R, Shimodaira H. (2006). Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 12: 1540-1542
88. Venables WN, Ripley BD. (2002). Modern Applied Statistics with S, 4th edn Springer: New York, NY, USA
89. Wong S, Rawls JF. (2012). Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21: 3100-3102
90. Wright ES, Yilmaz LS, Noguera DR. (2011). DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78: 717-725
91. Ye L, Zhang T, Wang TT, Fang ZW. (2012). Microbial structures, functions, and metabolic pathways in wastewater treatment bioreactors revealed using high-Throughput sequencing. Environ Sci Technol 46: 13244-13252