Food spoilage--interactions between food spoilage bacteria.

Food spoilage is a complex process and excessive amounts of foods are lost due to microbial spoilage even with modern day preservation techniques. Despite the heterogeneity in raw materials and processing conditions, the microflora that develops during storage and in spoiling foods can be predicted based on knowledge of the origin of the food, the substrate base and a few central preservation parameters such as temperature, atmosphere, a(w) and pH. Based on such knowledge, more detailed sensory, chemical and microbiological analysis can be carried out on the individual products to determine the actual specific spoilage organism. Whilst the chemical and physical parameters are the main determining factors for selection of spoilage microorganisms, a level of refinement may be found in some products in which the interactive behavior of microorganisms may contribute to their growth and/or spoilage activity. This review gives three such examples. We describe the competitive advantage of Pseudomonas spp. due to the production of iron-chelating siderophores, the generation of substrates for spoilage reactions by one organism from another microorganism (so-called metabiosis) and the up-regulation of phenotypes potentially involved in spoilage through cell-to-cell communication. In particular, we report for the first time the widespread occurrence of N-acyl homoserine lactones (AHL) in stored and spoiling fresh foods and we discuss the potential implications for spoilage and food preservation.

[1]  Cindra A. Widrig,et al.  Analogs of the autoinducer of bioluminescence inVibrio fischer , 1986, Archives of Microbiology.

[2]  P. Vandamme,et al.  Lactobacillus alimentarius: a specific spoilage organism in marinated herring. , 2001, International journal of food microbiology.

[3]  K. Rinehart,et al.  Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Borch,et al.  Bacterial spoilage of meat and cured meat products. , 1996, International journal of food microbiology.

[5]  P. Dalgaard,et al.  Application of an iterative approach for development of a microbial model predicting the shelf-life of packed fish. , 1997, International journal of food microbiology.

[6]  P. Delaquis,et al.  Shelf-life of coleslaw made from cabbage treated with gaseous acetic acid , 1997 .

[7]  R H Dainty,et al.  Bacterial sources of putrescine and cadaverine in chill stored vacuum-packaged beef. , 1986, The Journal of applied bacteriology.

[8]  H. Korkeala,et al.  The spoilage flora of vacuum-packaged, sodium nitrite or potassium nitrate treated, cold-smoked rainbow trout stored at 4°C or 8°C , 1998 .

[9]  J. Pitt,et al.  Fungi and Food Spoilage , 1987 .

[10]  P Dalgaard,et al.  Predictive modelling of the growth and survival of Listeria in fishery products. , 2000, International journal of food microbiology.

[11]  Steven C. Ricke,et al.  Eggs and Egg Products , 2001 .

[12]  J H Lamb,et al.  Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. , 1997, Microbiology.

[13]  E. Greenberg,et al.  Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators , 1994, Journal of bacteriology.

[14]  J. M. Shewan,et al.  Precursors of the volatile sulphides in spoiling north sea cod (Gadus morhua) , 1975 .

[15]  L. Gram Siderophore-Mediated Iron Sequestering by Shewanella putrefaciens , 1994, Applied and environmental microbiology.

[16]  L. Eberl,et al.  N-acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. , 1999, Systematic and applied microbiology.

[17]  P Dalgaard,et al.  Qualitative and quantitative characterization of spoilage bacteria from packed fish. , 1995, International journal of food microbiology.

[18]  Leo Eberl,et al.  Surface Motility of Serratia liquefaciens MG1 , 1999, Journal of bacteriology.

[19]  J. H. Crosa Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria , 1997, Microbiology and molecular biology reviews : MMBR.

[20]  J. Frisvad,et al.  Moulds in food spoilage. , 1996, International journal of food microbiology.

[21]  B. Lund Ecosystems in vegetable foods. , 1992, Society for Applied Bacteriology symposium series.

[22]  H. Huss,et al.  Microbiological quality and shelf life prediction of chilled fish. , 1988, International journal of food microbiology.

[23]  M. Doyle,et al.  Identification of Pseudomonas fluorescens Strains Isolated from Raw Pork and Chicken That Produce Siderophores Antagonistic towards Foodborne Pathogens. , 1995, Journal of food protection.

[24]  J. Costerton,et al.  The involvement of cell-to-cell signals in the development of a bacterial biofilm. , 1998, Science.

[25]  J. Samelis,et al.  The spoilage microflora of cured, cooked turkey breasts prepared commercially with or without smoking. , 2000, International journal of food microbiology.

[26]  G Molin,et al.  Classification of the spoilage flora of raw and pasteurized bovine milk, with special reference to Pseudomonas and Bacillus. , 1993, The Journal of applied bacteriology.

[27]  P. Murphy,et al.  Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones , 1993, Nature.

[28]  Bongjoon Kim,et al.  Isolation of Dextran-producing Leuconostoc lactis from Kimchi , 2001 .

[29]  H. Ramaswamy,et al.  Enhanced destruction of spoilage microorganisms in apple juice during continuous flow microwave heating , 1998 .

[30]  J. M. Shewan,et al.  Roles played by bacterial and autolytic enzymes in the production of volatile sulphides in spoiling North Sea cod (Gadus morhua) , 1976 .

[31]  H. Lappin-Scott,et al.  The use of an automated growth analyser to measure recovery times of single heat‐injured Salmonella cells , 1997, Journal of applied microbiology.

[32]  I. Walls,et al.  Spoilage of fruit juices by Alicyclobacillus acidoterrestris : Alicyclobacillus in the food industry , 2000 .

[33]  S. Ahrné,et al.  Contamination routes of Gram-negative spoilage bacteria in the production of pasteurised milk, evaluated by randomly amplified polymorphic DNA (RAPD) , 2000 .

[34]  S. Kjelleberg,et al.  Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. , 1999, Microbiology.

[35]  L. Gram,et al.  The bacteriology of fresh and spoiling Lake Victorian Nile perch (Lates niloticus). , 1990, International journal of food microbiology.

[36]  S. Molin,et al.  The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. , 2001, Microbiology.

[37]  Michiel Kleerebezem,et al.  Quorum sensing by peptide pheromones and two‐component signal‐transduction systems in Gram‐positive bacteria , 1997, Molecular microbiology.

[38]  Lian-Hui Zhang,et al.  AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora , 2000 .

[39]  N. A. Whitehead,et al.  Quorum-sensing in Gram-negative bacteria. , 2001, FEMS microbiology reviews.

[40]  J. Neilands,et al.  Siderophores in microbially processed cheese. , 1979, Journal of agricultural and food chemistry.

[41]  K. Omori,et al.  N-Acyl-l-Homoserine Lactone-Mediated Regulation of the Lip Secretion System inSerratia liquefaciens MG1 , 2001, Journal of bacteriology.

[42]  D. Pritchard,et al.  Quorum sensing: a novel target for anti-infective therapy. , 1998, The Journal of antimicrobial chemotherapy.

[43]  P. Dalgaard,et al.  Multiple compound quality index for cold-smoked salmon (Salmo salar) developed by multivariate regression of biogenic amines and pH. , 2000, Journal of agricultural and food chemistry.

[44]  L. Raaska,et al.  Antimicrobial activity of Pseudomonas spp. against food poisoning bacteria and moulds , 1996, Letters in applied microbiology.

[45]  B M Mackey,et al.  The relationship between the phenotypic properties of bacteria from chill-stored meat and spoilage processes. , 1992, Society for Applied Bacteriology symposium series.

[46]  B. Lee,et al.  Evaluation of Methods for Detecting the Production of H2S, Volatile Sulfides, and Greening by Lactobacilli , 1984 .

[47]  L. Gram,et al.  Spoilage and shelf-life of cod fillets packed in vacuum or modified atmospheres. , 1993, International journal of food microbiology.

[48]  M. Pirhonen,et al.  Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR(Ecc). , 2000, Molecular plant-microbe interactions : MPMI.

[49]  S. Atkinson,et al.  A hierarchical quorum‐sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping , 1999, Molecular microbiology.

[50]  W. Waites,et al.  Detection of rope spoilage in bread caused by Bacillus species , 1998 .

[51]  S. Kjelleberg,et al.  Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling , 1996, Journal of bacteriology.

[52]  J. M. Shewan,et al.  Psychrophilic spoilage bacteria of fish. , 1968, The Journal of applied bacteriology.

[53]  A. Margolles,et al.  Hop Resistance in the Beer Spoilage Bacterium Lactobacillus brevis Is Mediated by the ATP-Binding Cassette Multidrug Transporter HorA , 2001, Journal of bacteriology.

[54]  S. Molin,et al.  Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon , 1996, Journal of bacteriology.

[55]  W. Segal,et al.  Microbial Decomposition of Methionine and Identity of the Resulting Sulfur Products , 1969, Journal of bacteriology.

[56]  J. A. Ordóñez,et al.  GROWTH/SURVIVAL OF NATURAL FLORA AND LISTERIA MONOCYTOGENES ON REFRIGERATED UNCOOKED PORK AND TURKEY PACKAGED UNDER MODIFIED ATMOSPHERES , 1995 .

[57]  M. Pirhonen,et al.  A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. , 1993, The EMBO journal.

[58]  J W Wimpenny,et al.  Ecological concepts in food microbiology. , 1992, Society for Applied Bacteriology symposium series.

[59]  M. Bailey,et al.  Identification of conserved traits in fluorescent pseudomonads with antifungal activity. , 2000, Environmental microbiology.

[60]  Hutson,et al.  Lactobacillus kunkeei sp. nov. : a spoilage organism associated with grape juice fermentations , 1998, Journal of applied microbiology.

[61]  R H Dainty,et al.  Putrescine and cadaverine formation in vacuum packed beef. , 1985, The Journal of applied bacteriology.

[62]  L. Gram,et al.  Interaction between fish spoilage bacteria Pseudomonas sp. and Shewanella putrefaciens in fish extracts and on fish tissue. , 1996, The Journal of applied bacteriology.

[63]  R. Buchanan,et al.  Microbial Competition: Effect of Culture Conditions on the Suppression of Listeria monocytogenes Scott A by Carnobacterium piscicola †. , 1997, Journal of food protection.

[64]  C. Liao Analysis of pectate lyases produced by soft rot bacteria associated with spoilage of vegetables , 1989, Applied and environmental microbiology.

[65]  S. Molin,et al.  Production of Acylated Homoserine Lactones by Psychrotrophic Members of the Enterobacteriaceae Isolated from Foods , 1999, Applied and Environmental Microbiology.

[66]  A. King,et al.  Relationship between lactic acid concentration and bacterial spoilage in ground beef , 1983, Applied and environmental microbiology.

[67]  A. Lonvaud-Funel,et al.  La biosynthèse d'exopolysaccharide par des souches de Pediococcus damnosus isolées du vin : mise au point d'outils moléculaires de détection , 2001 .

[68]  J. S. Lee,et al.  Identification of the volatile compounds produced in sterile fish muscle (Sebastes melanops) by Pseudomonas fragi. , 1973, Applied microbiology.

[69]  S. Ahrné,et al.  Enterobacteriaceae found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of toxin encoding genes. , 1998, International journal of food microbiology.

[70]  H. Huss,et al.  Comparison of the microflora isolated from spoiled cold-smoked salmon from three smokehouses , 1998 .

[71]  E. Greenberg,et al.  Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. , 1996, Annual review of microbiology.

[72]  M. Gambello,et al.  Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. , 1993, Science.

[73]  J. J. Connell Advances in fish science and technology , 1980 .

[74]  M. Cardinal,et al.  Research of quality indices for cold‐smoked salmon using a stepwise multiple regression of microbiological counts and physico‐chemical parameters , 2001, Journal of applied microbiology.

[75]  A. Fredrickson Behavior of mixed cultures of microorganisms. , 1977, Annual review of microbiology.

[76]  K. Nealson,et al.  Cellular Control of the Synthesis and Activity of the Bacterial Luminescent System , 1970, Journal of bacteriology.

[77]  L. Gram Inhibitory effect against pathogenic and spoilage bacteria of Pseudomonas strains isolated from spoiled and fresh fish , 1993, Applied and environmental microbiology.

[78]  D. Wheeler,et al.  The Pseudomonas aeruginosaQuorum-Sensing Signal MoleculeN-(3-Oxododecanoyl)-l-Homoserine Lactone Has Immunomodulatory Activity , 1998, Infection and Immunity.

[79]  J E JAMESON,et al.  A discussion of the dynamics of salmonella enrichment , 1962, Journal of Hygiene.

[80]  R. Levin,et al.  Detection and incidence of specific species of spoilage bacteria on fish. II. Relative incidence of Pseudomonas putrefaciens and fluorescent pseudomonads on haddock fillets. , 1968, Applied microbiology.

[81]  L. Jespersen,et al.  Specific spoilage organisms in breweries and laboratory media for their detection. , 1996, International journal of food microbiology.

[82]  F. B. Whitfield,et al.  Role of Yersinia intermedia and Pseudomonas putida in the development of a fruity off-flavour in pasteurized milk , 2000, Journal of Dairy Research.

[83]  J. Richard,et al.  Antibacterial activity among Pseudomonas strains of meat origin , 1994 .

[84]  F. Cormier,et al.  Analysis of odor-active volatiles from Pseudomonas fragi grown in milk , 1991 .

[85]  J. Berdagué,et al.  Characterisation of volatile compounds produced by bacteria isolated from the spoilage flora of cold-smoked salmon. , 2001, International journal of food microbiology.

[86]  S. Kjelleberg,et al.  Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. , 2002, Microbiology.

[87]  C. Liao,et al.  Biochemical characterization of pectate lyases produced by fluorescent pseudomonads associated with spoilage of fresh fruits and vegetables , 1997 .

[88]  M. Adams,et al.  Review of the sensitivity of different foodborne pathogens to fermentation , 1997 .

[89]  E. Marth,et al.  Lactic Acid Production by Streptococcus thermophilus and Lactobacillus bulgaricus in Milk Precultured with Psychrotrophic Bacteria. , 1977, Journal of food protection.

[90]  W. C. Frazier,et al.  EFFECT OF PSEUDOMONADS AND ACHROMOBACTERACEAE ON GROWTH OF STAPHYLOCOCCUS AUREUS1,2 , 1966 .

[91]  P. Vanderlinde,et al.  Occurrence, Numbers, and Growth of Listeria monocytogenes on some Vacuum-Packaged Processed Meats. , 1992, Journal of food protection.

[92]  G. Salmond,et al.  N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. , 1992, The Biochemical journal.

[93]  H. Huss,et al.  The effect of biogenic amine production by single bacterial cultures and metabiosis on cold‐smoked salmon , 2000, Journal of applied microbiology.

[94]  E. T. Palva,et al.  Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. , 2001, Molecular plant-microbe interactions : MPMI.

[95]  R. Bell,et al.  Association of psychrotrophic Clostridium spp. with deep tissue spoilage of chilled vacuum-packed lamb. , 1996, International journal of food microbiology.

[96]  Leo Eberl,et al.  Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. , 2002, Microbiology.

[97]  S. Molin,et al.  Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. , 2001, Journal of microbiological methods.

[98]  S. Molin,et al.  Influence of food preservation parameters and associated microbiota on production rate, profile and stability of acylated homoserine lactones from food-derived Enterobacteriaceae. , 2003, International journal of food microbiology.

[99]  van M. Schothorst Microorganisms in Foods 6: Microbial Ecology of Food Commodities. , 1997 .

[100]  S. Kjelleberg,et al.  How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. , 2000, Microbiology.

[101]  L. Gram,et al.  Growth control of Listeria monocytogenes on cold-smoked salmon using a competitive lactic acid bacteria flora. , 1999, Journal of food protection.