Development of a rapid real-time PCR method as a tool to quantify viable Photobacterium phosphoreum bacteria in salmon (Salmo salar) steaks

Applied and Environmental Microbiology

Volumn 79, Issue 8, 2013, Pages 2612-2619

  Macé, Sabrina ^a,b,c   Mamlouk, Kelthoum ^a,b   Chipchakova, Stoyka ^a,b   Prévost, Hervé ^a,b   Joffraud, Jean Jacques ^c   Dalgaard, Paw ^d   Pilet, Marie France ^a,b   Dousset, Xavier ^a,b  

^a LUNAM UNIVERSITÉ   (France)

^b CEMAGREF   (France)

^c IFREMER   (France)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCING; CORRELATION COEFFICIENT; PHOTOBACTERIUM PHOSPHOREUM; QUANTIFICATION LIMIT; QUANTIFICATION METHODS; REAL-TIME PCR METHOD; SPECIFIC CONDUCTANCE; SPOILAGE MICROORGANISMS;

BACTERIA; GENES; RNA;

POLYMERASE CHAIN REACTION;

AZIDE; BACTERIAL DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); DRUG DERIVATIVE; PROPIDIUM IODIDE; PROPIDIUM MONOAZIDE; RNA 16S;

CORRELATION; DNA; FISH; FISH CULTURE; GENE; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REAL TIME; SAMPLING; SPECIES DIVERSITY;

ANIMAL; ARTICLE; ATLANTIC SALMON; BACTERIAL COUNT; CHEMISTRY; DNA SEQUENCE; FOOD CONTROL; FOOD HANDLING; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHOTOBACTERIUM; REAL TIME POLYMERASE CHAIN REACTION; SEA FOOD; SEQUENCE ALIGNMENT;

ANIMALS; AZIDES; BASE SEQUENCE; COLONY COUNT, MICROBIAL; DNA GYRASE; DNA, BACTERIAL; FOOD HANDLING; FOOD INSPECTION; FOOD MICROBIOLOGY; PHOTOBACTERIUM; PROPIDIUM; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SALMO SALAR; SEAFOOD; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); PHOTOBACTERIUM PHOSPHOREUM; SALMO SALAR;

EID: 84876193803     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03677-12     Document Type: Article

References (53)

1. Gram L, Huss HH. 1996. Microbiological spoilage of fish and fish products. Int. J. Food Microbiol. 33:121-137
2. Sivertsvik M, Jeksrud J, Rosnes JT. 2002. A review of modified atmosphere packaging of fish and fishery products-significance of microbial growth, activities and safety. Int. J. Food Sci. Technol. 37:107-127
3. 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
4. Dalgaard P. 2000. Fresh and lightly preserved seafood, p 110-139. In Man CD, Jones AA (ed), Shelf life evaluation of foods, 2nd ed. Aspen Publishing, Inc., Frederick, MD.
5. Dalgaard P. 1995. Qualitative and quantitative characterization of spoilage bacteria from packed fish. Int. J. Food Microbiol. 26:319-333
6. Dalgaard P, Gram L, Huss HH. 1993. Spoilage and shelf-life of cod fillets packed in vacuum or modified atmospheres. Int. J. Food Microbiol. 19:283-294
7. Dalgaard P, Mejholm O, Christiansen TJ, Huss HH. 1997. Importance of Photobacterium phosphoreum in relation to spoilage of modified atmosphere-packed fish products. Lett. Appl. Microbiol. 24:373-378
8. 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 degrees C. J. Appl. Microbiol. 92:790-799.
9. Hansen AA, Morkore T, Rudi K, Rodbotten M, Bjerke F, Eie T. 2009. Quality changes of prerigor filleted Atlantic salmon (Salmo salar L.) packaged in modified atmosphere using CO2 emitter, traditional MAP, and vacuum. J. Food Sci. 74:M242-M249.
10. Hovda MB, Sivertsvik M, Lunestad BT, Lorentzen G, Rosnes JT. 2007. Characterisation of the dominant bacterial population in modified atmosphere packaged farmed halibut (Hippoglossus hippoglossus) based on 16S rDNA-DGGE. Food Microbiol. 24:362-371
11. Macé S, Cornet J, Chevalier F, Cardinal M, Pilet Dousset M-FX, Joffraud J-J. 2012. Characterisation of the spoilage microbiota in raw salmon (Salmo salar) steaks stored under vacuum or modified atmosphere packaging combining conventional methods and PCR-TTGE. Food Microbiol. 30:164-172
12. Reynisson E, Lauzon HL, Magnusson H, Jonsdottir R, Olafsdottir G, Marteinsson V, Hreggvidsson GO. 2009. Bacterial composition and succession during storage of North-Atlantic cod (Gadus morhua) at superchilled temperatures. BMC Microbiol. 9:250.
13. Dalgaard P. 2006. Microbiology of marine muscle foods, p 53-51-53-20. In Hui YH (ed), Handbook of food science, technology and engineering, vol 1. Taylor & Francis, CRC Press, Boca Raton, FL.
14. Van Spreekens K. 1974. The suitability of Long and Hammer's medium for the enumeration of more fastidious bacteria from fresh fishery products. Arch. Lebensmittelhyg. 25:213-219
15. López-Caballero ME, Goncalves A, Nunes ML. 2002. Effect of CO2/O2-containing modified atmosphere on packed deepwater shrimp (Parapenaeus longirostris). Eur. Food Res. Technol. 214:192-197
16. Ast JC, Dunlap PV. 2005. Phylogenetic resolution and habitat specificity of members of the Photobacterium phosphoreum species group. Environ. Microbiol. 7:1641-1654
17. Urbanczyk H, Ast JC, Dunlap PV. 2011. Phylogeny, genomics, and symbiosis of Photobacterium. FEMS Microbiol. Rev. 35:324-342
18. Dalgaard P, Madsen HL, Samieian N, Emborg J. 2006. Biogenic amine formation and microbial spoilage in chilled garfish (Belone belone belone)- effect of modified atmosphere packaging and previous frozen storage. J. Appl. Microbiol. 101:80-95
19. Dalgaard P, Mejlholm O, Huss HH. 1996. Conductance method for quantitative determination of Photobacterium phosphoreum in fish products. J. Appl. Microbiol. 81:57-64
20. Wolffs P, Norling B, Radström P. 2005. Risk assessment of false-positive quantitative real-time PCR results in food, due to detection of DNA originating from dead cells. J. Microbiol. Methods 60:315-323.
21. Nocker A, Cheung Camper C-YAK. 2006. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Methods 67:310-320.
22. Josefsen MH, Löfström C, Hansen TB, Christensen LS, Olsen JE, Hoorfar J. 2010. Rapid quantification of viable Campylobacter bacteria on chicken carcasses, using real-time PCR and propidium monoazide treatment, as a tool for quantitative risk assessment. Appl. Environ. Microbiol. 76:5097-5104
23. Pan Y, Breidt F. 2007. Enumeration of viable Listeria monocytogenes cells by real-time PCR with propidium monoazide and ethidium monoazide in the presence of dead cells. Appl. Environ. Microbiol. 73:8028-8031
24. Mamlouk K, Macé S, Guilbaud M, Jaffrès E, Ferchichi M, Prévost H, Pilet Dousset M-FX. 2012. Quantification of viable Brochothrix thermosphacta in cooked shrimp and salmon by real-time PCR. Food Microbiol. 30:173-179
25. Pennacchia C, Ercolini D, Villani F. 2009. Development of a real-time PCR assay for the specific detection of Brochothrix thermosphacta in fresh and spoiled raw meat. Int. J. Food Microbiol. 134:230-236
26. Zhu R-G, Li T-P, Jia Y-F, Song L-F. 2012. Quantitative study of viable Vibrio parahaemolyticus cells in raw seafood using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 90:262-266.
27. Robert-Pillot A, Copin S, Gay M, Malle P, Quilici ML. 2010. Total and pathogenic Vibrio parahaemolyticus in shrimp: fast and reliable quantification by real-time PCR. Int. J. Food Microbiol. 143:190-197
28. Elizaquível P, Sánchez G, Selma MV, Aznar R. 2012. Application of propidium monoazide-qPCR to evaluate the ultrasonic inactivation of Escherichia coli O157:H7 in fresh-cut vegetable wash water. Food Microbiol. 30:316-320
29. Macé S, Joffraud Cardinal J-JM, Malcheva M, Cornet J, Lalanne V, Chevalier F, Sérot T, Pilet Dousset M-FX. 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
30. Dalgaard P, Manfio GP, Goodfellow M. 1997. Classification of Photobacteria associated with spoilage of fish products by numerical taxonomy and pyrolysis mass spectrometry. Zentralbl. Bakteriol. 285:157-168
31. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98
32. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T. 2012. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134.
33. Klein D, Janda P, Steinborn R, Müller M, Salmons B, Günzburg WH. 1999. Proviral load determination of different feline immunodeficiency virus isolates using real-time polymerase chain reaction: influence of mismatches on quantification. Electrophoresis 20:291-299.
34. Union du mareyage Français (UMF). 2010. Guide des bonnes pratiques et application de l'HACCP (J. officiel référence no. 5941/2010). Fonds européens pour la pêche et FranceAgrimer, Paris, France.
35. Matamoros S, André S, Hue I, Prévost H, Pilet MF. 2010. Identification of lactic acid bacteria involved in the spoilage of pasteurized "foie gras" products. Meat Sci. 85:467-471
36. Juste A, Thomma B, Lievens B. 2008. Recent advances in molecular techniques to study microbial communities in food-associated matrices and processes. Food Microbiol. 25:745-761
37. Postollec F, Falentin H, Pavan S, Combrisson J, Sohier D. 2011. Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 28:848-861
38. Nordstrom JL, Vickery MCL, Blackstone GM, Murray SL, DePaola A. 2007. Development of a multiplex real-time PCR assay with an internal amplification control for the detection of total and pathogenic Vibrio parahaemolyticus bacteria in oysters. Appl. Environ. Microbiol. 73:5840-5847
39. Bjornsdottir-Butler K, Jones JL, Benner R, Burkhardt W, III. 2011. Development of a real-time PCR assay with an internal amplification control for detection of Gram-negative histamine-producing bacteria in fish. Food Microbiol. 28:356-363
40. Bjornsdottir-Butler K, Jones JL, Benner RA, Jr, Burkhardt W, III. 2011. Quantification of total and specific gram-negative histamine-producing bacteria species in fish using an MPN real-time PCR method. Food Microbiol. 28:1284-1292
41. Reynisson E, Lauzon HL, Magnusson H, & Óli Hreggvidsson G, Marteinsson VT. 2008. Rapid quantitative monitoring method for the fish spoilage bacteria Pseudomonas. J. Environ. Monit. 10:1357-1362
42. Nocker A, Sossa-Fernandez P, Burr MD, Camper AK. 2007. Use of propidium monoazide for live/dead distinction in microbial ecology. Appl. Environ. Microbiol. 73:5111-5117
43. Martin B, Jofré A, Garriga M, Pla M, Aymerich T. 2006. Rapid quantitative detection of Lactobacillus sakei in meat and fermented sausages by real-time PCR. Appl. Environ. Microbiol. 72:6040-6048
44. Takahashi H, Kimura B, Tanaka Y, Shinozaki J, Suda T, Fujii T. 2009. Real-time PCR and enrichment culture for sensitive detection and enumeration of Escherichia coli. J. Microbiol. Methods 79:124-127.
45. Rodríguez-Lázaro D, Jofré A, Aymerich T, Hugas M, Pla M. 2004. Rapid quantitative detection of Listeria monocytogenes in meat products by realtime PCR. Appl. Environ. Microbiol. 70:6299-6301
46. Afssa. 2008. Avis de l'Agence française de sécurité sanitaire des aliments concernant les références applicables aux denrées alimentaires en tant que critères indicateurs d'hygiène des procédés. Saisine liée no. 2006-SA-0215, Saisine no. 2007-SA-0174. Afssa, Maison-Alfort, France.
47. Emborg J, Laursen BG, Dalgaard P. 2005. Significant histamine formation in tuna (Thunnus albacares) at 2°C-effect of vacuum- and modified atmosphere-packaging on psychrotolerant bacteria. Int. J. Food Microbiol. 101:263-279
48. Kanki M, Yoda T, Ishibashi M, Tsukamoto T. 2004. Photobacterium phosphoreum caused a histamine fish poisoning incident. Int. J. Food Microbiol. 92:79-87
49. Jorgensen LV, Huss HH, Dalgaard P. 2000. The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J. Appl. Microbiol. 89:920-934
50. Dalgaard P, Buch P, Silberg S. 2002. Seafood Spoilage Predictor-development and distribution of a product specific application software. Int. J. Food Microbiol. 73:343-349
51. Ranieri ML, Ivy RA, Mitchell WR, Call E, Masiello SN, Wiedmann M, Boor KJ. 2012. Real-time PCR detection of Paenibacillus spp. in raw milk to predict shelf life performance of pasteurized fluid milk products. Appl. Environ. Microbiol. 78:5855-5863
52. 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
53. Nieminen T, Bjorkroth J, Dalgaard P. 2012. Volatile compounds and microbiota associated with the spoilage of high-oxygen modified atmosphere-packaged raw pork meat, poster 273. Abstr. FOODMICRO 2012-23rd International ICFMH Symposium, Istanbul, Turkey, 3 to 7 September 2012.