Comparison of Bacterial Profiles of Fish between Storage Conditions at Retails Using DGGE and Banding Pattern Analysis: Consumer’s Perspective — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Comparison of Bacterial Profiles of Fish between Storage Conditions at Retails Using DGGE and Banding Pattern Analysis: Consumer’s Perspective
Department of Food Science & Technology, The Ohio State University, Columbus, USA
,
College of Public Health, Division of Environmental Health Sciences, The Ohio State University, Columbus, USA
,
Department of Animal Sciences, The Ohio State University, Columbus, USA.
,
Department of Food Science & Technology, The Ohio State University, Columbus, USA; 2College of Public Health, Division of Environmental Health Sciences, The Ohio State University, Columbus, USA
1 Department of Food Science & Technology, The Ohio State University, Columbus, USA
2 College of Public Health, Division of Environmental Health Sciences, The Ohio State University, Columbus, USA
3 Department of Animal Sciences, The Ohio State University, Columbus, USA.
4 Department of Food Science & Technology, The Ohio State University, Columbus, USA; 2College of Public Health, Division of Environmental Health Sciences, The Ohio State University, Columbus, USA
Bacterial profiles between storage conditions (frozen vs fresh) were compared using PCR-DGGE and banding pattern analysis. Salmon and tuna were collected and the bacteria cells were separated from fish cells using a somatic cell re-leasing agent. The results demonstrated that some were indigenous waterborne bacteria. However, the majority were identified as spoilage bacteria, pathogens and potential fecal contamination bacteria. Banding pattern analysis showed that the storage conditions were a significant factor in clustering bacteria. Frozen fish showed a smaller number of bac-terial species than fresh samples. Freezing seemed to play a role as a selective pressure by inactivating some microor-ganisms while favoring resistant ones to low temperature. The bacterial profiles seemed to be more influenced by afterharvest practices than the original environmental contamination. These findings provide consumers insight into fish quality, potential health risks of raw fish consumption, and the impact of storage conditions on bacterial group of raw fish.
KeywordsFishPCR-DGGEBacterial ProfilesStorage
A. Bener, M. Al-Ali and G. F. Hoffmann, “Vitamin D Deficiency in Healthy Children in a Sunny Country: Associated Factors,” International Journal of Food Sciences, Vol. 60, No. S5, 2009, pp. 60-70. doi:10.1080/09637480802400487
L. A. Colangelo, K. He, M. A. Whooley, M. L. Daviglus and K. Liu, “Higher Dietary Intake of Long-Chain ω-3 Polyunsaturated Fatty Acids Is Inversely Associated with Depressive Symptoms in Women,” Nutrition, Vol. 25, No. 10, 2009, pp. 1011-1019. doi:10.1016/j.nut.2008.12.008
F. Feldhusen, “The Role of Seafood in Bacterial Foodborne Diseases,” Microbes and Infection, Vol. 2, No. 13, 2000, pp. 1651-1660.
D. Hwang, Y. Huang, K. Lin, T. Chen, S. Lin, L. Chen and H. Hsieh, “Investigation of Hygienic Quality and Freshness of Marketed Fresh Seafood in Northern Taiwan,” Food Hygiene and Safety Science, Vol. 45, No. 5, 2000, pp. 225-230. doi:10.3358/shokueishi.45.225
S. Hielm, M. Lindstrom and H. Korkeala, “Food Safety in Seafood; Epidemiological Concerns Related to Geography of Fishing Grounds,” In: F. J. M. Smulders and J. D. Collins, Eds., Food Safety Assurance and Veterinary Public Health, Vol. 1 Food Safety Assurance in the PreHarvest Phase, Academic Publishers, Wageningen, 2000, pp. 229-246.
Hong Kong Food and Environmental Hygiene Department, “An Evaluation of Sushi and Sashimi Microbiological Surveillance 1997-1999,” 2000. http://www.cfs.gov.hk/english/programme/programme_rafs/files/ss_ras2_eng.pdf
Marler Clark Website, “Sushi King Salmonella Outbreak – Arkansas” 2006. http://www.marlerclark.com/case_news/view/sushi-king-salmonella-outbreak-arkansas
M. C. Nesheim and A. L. Yaktine, “Seafood Choices: Balancing Benefits and Risks,” National Academies Press, Washington DC, 2007.
L. ?vre?s, L. Forney, F. L. Daae and V. Torsvik, “Distribution of Bacterioplankton in Meromictic Lake S?lenvannet, as Determined by Denaturing Gradient Gel Electrophoresis of PCR-Amplified Gene Fragments Coding for 16S rRNA,” Applied and Environmental Microbiology, Vol. 63, No. 9, 1997, pp. 3367-3373.
G. Muyzer and K. Smalla, “Application of Denaturing Gradient Gel Electrophoresis (DGGE) and Temperature Gradient Gel Electrophoresis (TGGE) in Microbial Ecology,” Antonie van Leeuwenhoek, Vol. 73, No. 1, 1998, pp. 127-141. doi:10.1023/A:1000669317571
M. B. Hovda, B. T. Lunestad, M. Sivertsvik and J. T. Rosnes, “Characterisation of the Bacterial Flora of Modified Atmosphere Packaged Farmed Atlantic Cod (Gadus morhua) by PCR-DGGE of Conserved 16S rRNA Gene Regions,” International Journal of Food Microbiology, Vol. 117, No. 1, 2007, pp. 68-75. doi:10.1016/j.ijfoodmicro.2007.02.022
I. Huber, B. Spanggaard, K. F. Appel, L. Rossen, T. Nielsen and L. Gram, “Phylogenetic Analysis and in Situ Identification of the Intestinal Microbial Community of Rainbow Trout (Oncorhynchus mykiss, Walbaum),” Journal of Applied Microbiology, Vol. 96, No. 1, 2004, pp. 117132. doi:10.1046/j.1365-2672.2003.02109.x
A. L. N. Aminin, F. M. Warganegara, P. Aditiawati and Akhmaloka, “Simple Enrichment and Independent Cultures to Expand Bacterial Community Analysis from Gedongsongo Hot Spring,” Journal of Bioscience and Bioengineering, Vol. 106, No. 2, 2008, pp. 211-214. doi:10.1263/jbb.106.211
V. G. Fukuda, I. M. Parkhomenko, L. Y. Brovko and N. N. Ugarova, “Improved Bioluminescent Enzyme Immunoassay for the Rapid Detection of Salmonella in Chicken Meat Samples,” Letters in Applied Microbiology, Vol. 41, 2005, pp. 379-384. doi:10.1111/j.1472-765X.2005.01783.x
R. Mihaescu, D. Levy and L. Pachter, “Why NeighborJoining Works,” Algorithmica, Vol. 54, No. 1, 2009, pp. 1-24. doi:10.1007/s00453-007-9116-4
S. F. Altschul, T. L. Madden, A. A. Schaffer, J. Zhang, W. Miller and D. J. Lipman, “Gapped BLAST and PSIBLAST: A New Generation of Protein Database Search Programs,” Nucleic Acids Research, Vol. 25, No. 17, 1997, pp. 3389-3444. doi:10.1093/nar/25.17.3389
K. C. Kain and M. Kelly, “Clinical Features, Epidemiology, and Treatment of Plesiomonas shigelloides Diarrhea,” Journal of Clinical Microbiology, Vol. 27, No. 5, 1989, pp. 998-1001.
M. E. Pavan, R. J. Franco, J. M. Rodriguez, P. Gadaleta, S. L. Abbott, M. Janda and J. Zorzopulos, “Phylogenetic Relationships of the Genus Kluyvera: Transfer of Enterobacter intermedius Izard et al. 1980 to the Genus Kluyvera as Kluyvera intermedia comb. nov. and Reclassification of Kluyvera cochleae as a Later Synonym of K. Intermedia,” International Journal of Systematic and Evolutionary Microbiology, Vol. 55, No. 1, 2005, 437-442. doi:10.1099/ijs.0.63071-0
K. E. Ashelford, J. C. Fry, M. J. Bailey and M. J. Day, “Characterization of Serratia Isolates from Soil, Ecological Implications and Transfer of Serratia proteamaculans subsp. quinovora Grimont et al. 1983 to Serratia quinivorans corrig., sp. nov,” International Journal of Systematic and Evolutionary Microbiology, Vol. 52, No. 6, pp. 2281-2289. doi:10.1099/ijs.0.02263-0
E. Blickstad and G. Molin, “Growth and End-Product Formation in Fermenter Cultures of Brochothrix thermosphacta ATCC 11509T and Two Psychrotrophic Lactobacillus spp. in Different Gaseous Atmospheres,” Journal of Applied Bacteriology, Vol. 57, No. 2, 1984, pp. 213220. doi:10.1111/j.1365-2672.1984.tb01385.x
B. Bhadra, P. Roy and R. Chakraborty, “Serratia ureilytica sp. nov., a Novel Urea-Utilizing Species,” International Journal of Systematic and Evolutionary Microbiology, Vol. 55, No. 5, 2005, pp. 2155-2158. doi:10.1099/ijs.0.63674-0
R. A. Holley, T. Y. Guan, M. Peirson and C. K. Yost, “Carnobacterium Viridans sp. nov., an Alkaliphilic, Facultative Anaerobe Isolated from Refrigerated, VacuumPacked Bologna Sausage,” International Journal of Systematic and Evolutionary Microbiology, Vol. 52, No. 5, 2002, pp. 1881-1885. doi:10.1099/ijs.0.02216-0
E. P. Ivanova, T. Sawabe, N. M. Gorshkova, V. I. Svetashev, V. V. Mikhailov, D. V. Nicolau and R. Christen, “Shewanella japonica sp. nov,” International Journal of Systematic and Evolutionary Microbiology, Vol. 51, No. 3, 2001, pp. 1027-1033. doi:10.1099/00207713-51-3-1027
S. Todorov and B. Franco, “Lactobacillus Plantarum: Characterization of the Species and Application in Food Production,” Food Reviews International, Vol. 26, No. 3, 2010, pp. 205-229. doi:10.1080/87559129.2010.484113
X. Corbrella, A. Montero, M. Pujol, A. Dominguez, A. Ayats, M. J. Argerich, F. Garrugosa, J. Ariza and F. Gudio, “Emergence and Rapid Spread of Carbapenem Resistance during a Large and Sustained Hospital Outbreak of Multiresistant Acinetobacter baumannii,” Journal of Clinical Microbiology, Vol. 38, No. 11, 2000, pp. 4086-4095.
S. F. Snieszko, P. J. Griffin and S. B. Freddle, “A New Bacterium (Hemophilus Piscum N. Sp.) from Ulcer Disease of Trout,” Journal of Bacteriology, Vol. 59, 1950, pp. 699-710.
L. Toffin, A. Bidault, P. Pignet, B. J. Tindall, A. Slobodkin, C. Kato and D. Prieur, “Shewanella profunda sp. nov., Isolated from Deep Marine Sediment of the Nankai Trough,” International Journal of Systematic and Evolutionary Microbiology, Vol. 54, No. 6, 2004, pp. 19431949. doi:10.1099/ijs.0.03007-0
C. G. Lobb, S. H. Ghaffari, J. R. Hayman and D. T. Thompson, “Plasmid and Serological Differences between Edwardsiella ictaluri Strains,” Applied and Environmental Microbiology, Vol. 59, No. 9, 1993, pp. 2930-2836.
M. Satomi, B. Kimura, T. Hamada, S. Harayama and T. Fuji, “Phylogenetic Study of the Genus Oceanospirillum Based on 16S rRNA and gyrB Genes: Emended Description of the Genus Oceanospirillum, Description of Pseudospirillum Gen. nov., Oceanobacter Gen. nov. and Terasakiella Gen. nov. and transfer of Oceanospirillum jannaschii and Pseudomonas stanieri to Marinobacterium as Marinobacterium jannaschii Comb. nov. and Marinobacterium stanieri comb. nov,” International Journal of Systematic and Evolutionary Microbi
M. Satomi, B. F. Vogel, L. Gram and K. Venkateswaran, “Shewanella hafniensis sp. nov. and Shewanella morhuae sp. nov. Isolated from Marine Fish of the Baltic Sea,” International Journal of Systematic and Evolutionary Microbiology, Vol. 56, No. 1, 2006, 243-249.
S. Khashe and M. Janda, “Biochemical and Pathogenic Properties of Shewanella alga and Shewanella putrefaciens,” Journal of Clinical Microbiology, Vol. 36, No. 3, 1998, pp. 783-787.
Z. A. Zakaria, Z. Zakaria, S. Surif and W. A. Ahmad, “Hexavalent Chromium Reduction by 446 Acinetobacter haemolyticus Isolated from Heavy-Metal Contaminated Wastewater,” Journal of Hazardous Materials, Vol. 146, No. 1-2, 2007, pp. 30-38. doi:10.1016/j.jhazmat.2006.11.052
M. D. Collins, D. Jones, J. A. E. Farrow, R. Kilpper-Balz and K. H. Schleifer, “Enterococcus avium nom. rev., comb. nov.; E. casseliflavus nom. rev., comb. nov.; E. durans nom. rev., comb. nov.; E. gallinarum comb. nov.; and E. malodoratus sp. nov,” International Journal of Systematic Bacteriology, Vol. 34, No. 2, 1984, pp. 220223. doi:10.1099/00207713-34-2-220
S. Mannerova, R. Pantucek, J. Doskar, P. Svec, C. Snauwaert, M. Vancanneyt, J. Swings and I. Sedlacek, “Macrococcus brunensis sp. nov., Macrococcus hajekii sp. nov. and Macrococcus lamae sp. nov., from the Skin of Llamas,” International Journal of Systematic and Evolutionary Microbiology, Vol. 53, No. 5, 2003, pp. 1647-1654. doi:10.1099/ijs.0.02683-0
J. J. Leisner, B. G. Laursen, H. Prévost, D. Drider, P. Dalgaard, “Carnobacterium: Positive and Negative Effects in the Environment and in Foods,” FEMS Microbiology Reviews, Vol. 31, No. 5, 2007, pp. 592-613. doi:10.1111/j.1574-6976.2007.00080.x
L. Tvrzova, P. Schumann, C. Sproer, I. Sedlacek, Z. Pacova, O. Sedo, Z. Zdrahal, M. Steffen and E. Lang, “Pseudomonas moraviensis sp. nov. and Pseudomonas vranovensis sp. nov., Soil Bacteria Isolated on Nitroaromatic Compounds, and Emended Description of Pseudomonas asplenii,” International Journal of Systematic and Evolutionary Microbiology, Vol. 56, No. 11, 2006, pp. 26572663. doi:10.1099/ijs.0.63988-0
Y. Uh, J. S. Son, K. J. Yoon and S. K. Hoog, “Penicillin-Resistant Aerococcus viridans Bacteremia Associated with Granulocytopenia,” Journal of Korean Medical Science, Vol. 17, No. 1, 2002, 113-115.
M. Elomari, L. Corler, B. Hoste, M. Gills, D. Izard and H. Leclerc, “DNA Relatedness among Pseudomonas Strains Isolated from Natural Mineral Waters and Proposal of Pseudornonas veronii sp. nov,” International Journal of Systematic Bacteriology, Vol. 46, No. 4, 1996, pp. 11381144. doi:10.1099/00207713-46-4-1138
S. A. Tailor, E. M. Bailey and M. J. Rybak, “Enterococcus, an Emerging Pathogen,” Annals of Pharmacotherapy, Vol. 27, No. 10, 1993, pp. 1231-1242.
C. Michel, P. Nougayrede, A. Eldar, E. Sochon and P. De Kinkelin, “Vagococcus salmoninarum, a Bacterium of Pathological Significance in Rainbow Trout Oncorhynch usmykiss Farming,” Diseases of Aquatic Organisms, Vol. 30, No. 3, 1997, pp. 199-208. doi:10.3354/dao030199
I. Romano, L. Lama, B. Nicolaus, A. Poli, A. Gambacorta and A. Giordano, “Oceanobacillus oncorhynchi subsp. incaldanensis subsp. nov., an Alkalitolerant Halophile Isolated from an Algal mat Collected from a Sulfurous Spring in Campania (Italy), and Emended Description of Oceanobacillus oncorhynchi,” International Journal of Systematic and Evolutionary Microbiology, Vol. 56, No. 4, 2006, pp. 805-810. doi:10.1099/ijs.0.63575-0
J. Law-Brown and P. R. Meyers, “Enterococcus phoeniculicola sp. nov., a Novel Member of the Enterococci Isolated from the Uropygial Gland of the Red-Billed Woodhoopoe, Phoeniculus purpureus,” International Journal of Systematic and Evolutionary Microbiology, Vol. 53, No. 3, 2003, pp. 683-685. doi:10.1099/ijs.0.02334-0
C. R. Jackson, E. E. Roden and P. F. Churchill, “Changes in Bacterial Species Composition in Enrichment Cultures with Various Dilutions of Inoculum as Monitored by Denaturing Gradient Gel Electrophoresis,” Applied and Environmental Microbiology, Vol. 64, No. 12, 2008, 50465048.
T. Chua and A. A. Bhagwat, “A Rapid and Simple DNA Extraction Procedure to Detect Salmonella spp. and Listeria monocytogenes from Fresh Produce Using Realtime PCR,” Food Analytical Methods, Vol. 2, No. 2, 2009, 96-101. doi:10.1007/s12161-008-9032-5
J. Lee and A. Deininger, “Detection of E. coli in Beach Water within 1 Hour Using Immunomagnetic Separation and ATP Bioluminescence,” Luminescence, Vol. 19, No. 1, 2004, pp. 31-36. doi:10.1002/bio.753
J. Emborg, B. G. Laursen, T. Rathjen and P. Dalgaard, “Microbial Spoilage and Formation of Biogenic Amines in Fresh and Thawed Modified Atmosphere-Packed Salmon (Salmo salar) at 2 Deg C,” Journal of Applied Microbiology, Vol. 92, No. 4, 2002, pp. 790-799. doi:10.1046/j.1365-2672.2002.01588.x
C. Pennacchia, D. Ercolini and F. Villani, “Development of a Real-Time PCR Assay for the Specific Detection of Brochothrix thermosphacta in Fresh and Spoiled Raw Meat,” International Journal of Food Microbiology, Vol. 134, No. 3, 2009, pp. 230-236. doi:10.1016/j.ijfoodmicro.2009.07.005
G. Colman, “Aerococcus-Like Organisms Isolated from Human Infections,” Journal of Clinical Pathology, Vol. 20, No. 3, 1967, pp. 294-297. doi:10.1136/jcp.20.3.294
D. Villers, E. Espaze, M. Coste-Burel, F. Giauffret, E. Ninin, F. Nicolas and H. Richet, “Nosocomial Acinetobacter baumanii Infections: Microbiological and Clinical Epidemiology,” Annals of Internal Medicine, Vol. 129, No. 3, 1998, pp. 182-189.
J. P. Hawke, A. C. McWhorter, A. G. Steigerwalt and D. J. Brenner, “Edwardsiella ictaluri sp. Nov., the Causative Agent of Enteric Septicemia of Catfish,” International Journal of Systematic and Evolutionary Microbiology, Vol. 31, 1981, pp. 396-400.
L. Pagani, A. Lang, C. Vedovelli, O. Moling, G. Rimenti, R. Pristera and P. Mian, “Soft Tissue Infection and Bacteremia Caused by Shewanella putrefaciens,” Journal of 390 Clinical Microbiology, Vol. 41, 2003, pp. 2240-2241.
S. Wang, K. Liu, T. Liang, Y. Kuo and C. Wang, “In Vitro Antioxidant Activity of Liquor and Semi-Purified Fractions from Fermented Squid Pen Biowaste by Serratia ureilytica TKU013,” Food Chemestry, Vol. 119, No. 4, 2010, pp. 1380-1385. doi:10.1016/j.foodchem.2009.09.017
L. M. Schmidtke and J. Carson, “Chararacteristics of Vagococcus Salmoninarum Isolated from Diseased Salmonid Fish,” Journal of Applied Bacteriology, Vol. 77, No. 2, 1994, pp. 229-236. doi:10.1111/j.1365-2672.1994.tb03068.x