Antifungal Microbial Agents for Food Biopreservation—A Review
Abstract
:1. Introduction
2. Fungal Spoilers
2.1. Quality and Safety Issues
2.2. Isolation and Identification of Fungal Spoilers
2.3. Fungal Spoilers and Food Chains
2.3.1. Fresh or Perishable Foods
2.3.2. Stored and Processed Foods
3. Antifungal Microorganisms in Food
3.1. Screening and Validation Methods
3.1.1. In Vitro Screening
3.1.2. Validation by Challenge-Test in the Food Products
3.2. Antifungal Microorganisms
3.2.1. Lactic Acid Bacteria
3.2.2. Propionibacteria
3.2.3. Bacillus and Other Bacteria
3.2.4. Yeasts
3.2.5. Filamentous Fungi
4. Action Mechanisms of Antifungal Microorganisms
4.1. Action Mechanisms of Antifungal Lactic Acid Bacteria and Propionibacteria in Fermented Foods
4.2. Action Mechanisms of Antifungal Yeasts and Molds in Fermented Foods
4.3. Action Mechanisms of Antifungal Yeasts and Bacillus spp. for Control of Postharvest Diseases
5. Implementation of Biopreservation Methods against Fungal Spoilage
5.1. Optimization and Application Modes
5.2. Constraints
6. Conclusions
Conflicts of Interest
References
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Food Field | Group | Antifungal Microorganisms (Active In Situ/Tested Strains) | In Situ Test | Source of Microorganism | Application Method | Activity Spectrum (Inhibited/Tested) | Reference |
---|---|---|---|---|---|---|---|
bakery | LAB | Lactobacillus brevis ITM18 | yeast-leavened bread | sourdough | CFS as ingredient | Aspergillus niger | [97] |
bakery | LAB | Lactobacillus plantarum HD1 | Korean draft rice wine | kimchi | CFS | Aspergillus fumigatus and Pichia kudriavzevii | [98] |
bakery | LAB | Lactobacillus amylovorus DSM19280 (1/1) | sourdough quinoa bread | cereal isolate | cells in sourdough | environmental molds | [80] |
bakery | LAB | Lactobacillus plantarum CRL778 | wheat bread | homemade wheat dough | SL778: fermentate as ingredient | environmental molds | [99] |
bakery | LAB | Lactobacillus plantarum UFG 121 (only 1 in situ from best 2/88 in vitro) | oat-based product | food | cells in sourdough | Fusarium culmorum (only 1 tested in situ), Penicillium chrysogenum, Penicillium expansum, Penicillium roqueforti, and Aspergillus flavus (5/7 in vitro) | [69] |
bakery | LAB | Lactobacillus amylovorus DSM19280 (1/3) | sourdough wheat bread | cereal isolate | cells as starter | Fusarium culmorum | [83] |
bakery | LAB | Lactobacillus reuteri R29, Lactobacillus brevis R2, Lactobacillus amylovorus DSM19280 | sourdough of quinoa and rice bread | human, pork, and cereal | cells in sourdough | environmental molds | [90] |
bakery | LAB | Lactobacillus bulgaricus CECT 4005, Lactobacillus plantarum CECT 749 (active in situ 2/6), Lactobacillus johnsonii CECT 289, Lactobacillus rhamnosus CECT 288, Lactobacillis ruminis CECT 1324, and Bifidobacterium bifidum CECT 870T (6 active in vitro/16) | loaf bread | not detailed | cells in sourdough | Aspergillus parasiticus (only one tested in situ) and Penicillium expansum | [100] |
bakery | LAB & PAB | Leuconostoc citreum (5 strains), Lactobacillus sakei, Lactobacillus plantarum, Lactobacillus spicheri O15, Lactobacillus reuteri 5529, Lactobacillus brevis Lu35, Propionibacterium acidipropionici and Propionibacterium freudenreichii LSaci68 (by surface-spraying 12 LAB/69) | pound cake and milk bread roll | milk, milk roll sourdough, and others not detailed | whole culture as sourdough ingredient for milk bread roll and sprayed | Cladosporium sphaerospermum and Wallemia sebi on pound cake; and Eurotium repens, Aspergillus niger, and Penicillium corylophilum on milk bread roll | [63] |
dairy | LAB | Lactobacillus harbinensis K.V9.3.1Np, Lactobacillus. rhamnosus K.C8.3.1I, and Lactobacillus paracasei K.C8.3.1Hc1 (3/11) | yogurt | cow and goat milk | cells as adjunct culture | Debaryomyces hansenii, Kluyveromyces lactis, Kluyveromyces marxianus, Penicillium brevicompactum, Rhodotorula mucilaginosa, and Yarrowia lipolytica (6/6) | [78] |
dairy | LAB | Lactobacillus casei AST18 (1/1) | yogurt | Chinese dairy products | cells as adjunct culture | Penicillium sp. (1/1) | [88] |
dairy | LAB | Lactobacillus paracasei DCS302 | yogurt | not detailed | cells as adjunct culture | Penicillium sp. nov. DCS 1541, Penicillium solitum (2/8) | [101] |
dairy | LAB | Lactobacillus harbinensis K.V9.3.1Np (1/2) | yogurt | cow milk | cells as adjunct culture | Yarrowia lipolytica (1/1) | [87] |
dairy | LAB | Lactobacillus reuteri INIA P57 | semi-hard ewe milk cheese | pig feces (isolated by Langa 2003) | cells as adjunct culture supplemented with glycerol | Not evaluated | [102] |
dairy | LAB | Lactobacillus amylovorus DSM 19280 (1/1) | cheddar cheese | cereal environment | cells as adjunct culture | Penicillium expansum (1/1) and environmental molds | [89] |
dairy | LAB | 12 strains of Lactobacillus plantarum (12/897) | cottage cheese | fresh herbs, fruits, and vegetables | cells as added to the finished product | Penicillium commune | [103] |
dairy | LAB | L. rhamnosus A238, L. rhamnosus A119 (2/5) The association of L. rhamnosus A238 with B. animalis subsp. lactis A026, and L. rhamnosus A119 with B. animalis subsp. lactis A026 | cottage cheese | not detailed | cells added to the finished product | Penicillium chrysogenum (1/1) | [104] |
malting | LAB | Lactobacillus brevis R2Δ (1/1) | barley malt extract fermentation | porcine isolate | cells as starter | Not evaluated | [105] |
malting | LAB | Lactobacillus brevis R2Δ and Lactobacillus plantarum FST1.7 (2/2) | barley malt extract (wort) fermentation | porcine and barley isolate | cells as starter | Fusarium culmorum | [106] |
malting | LAB | Lactobacillus brevis R2Δ (1/1) | barley in malting process | porcine isolate | cells as starters and CFS | Fusarium culmorum and Fusarium graminearum | [107] |
malting | LAB | Lactobacillus reuteri R29 and Lactobacillus amylovorus DSM19280 | malting process (steeping and germination) | human and cereal isolates | CFS (wort as growth media) as the steeping liquor | Fusarium culmorum | [94] |
fermented vegetables | LAB | Pediococcus spp. A19 (tested in situ) Pediococcus spp. A21, Lactobacillus plantarum B4496, Lactobacillus brevis 207, and Lactobacillus sanfranciscensis BB12 (5/13) | cocoa | fermenting cocoa | cells as starter | Aspergillus carbonarius, Aspergillus niger, and Aspergillus ochraceus | [108] |
fermented vegetables | LAB | Lactobacillus fermentum YML014 | tomato puree | gari, fermented cassava (starchy root) | cells | Penicillium expansum (only one tested in situ), Aspergillus flavus, Aspergillus niger, Candida albicans, and Zygosaccharomyces rouxii (low inhibition of yeasts) | [109] |
fermented vegetables | LAB | Lactobacillus helveticus KLDS 1.8701 (1/4 also L. helveticus) | fermented soybean milk | dairy products | cells as adjunct culture | Penicillium sp. (1/1) | [81] |
grain/seed | LAB | Lactococcus sp. BSN307 | wheat grains | rotten jackfruit, guava, and animals fecal samples | submerged in purified volatile organic compound 2,4-di-tert-butylphenol | A. niger, F. moniliforme, F. graminearum, F. chlamydosporum, and F. oxysporum | [110] |
grain/seed | LAB | Lactobacillus plantarum LR/14 | wheat seeds (Triticum aestivum var. HD 2824) | not detailed | AMP LR14 solution | Aspergillus niger, Rhizopus stolonifer, Mucor racemosus, and Penicillium chrysogenum. | [111] |
grain/seed | LAB | Lactobacillus plantarum YML007 (1/1400) | soybean | kimchi | CFS | Aspergillus niger | [112] |
grain/seed | LAB & Fungi | kefir grains contain a symbiotic consortium of LAB and yeasts (Lactobacillus plantarum, L. kefir, Lactococcus lactis subsp. lactis, Saccharomyces and Acetobacter) | arepa (corn cakes) | kefir grains | CFS | Aspergillus flavus | [113] |
fruit | LAB & other bacteria | Lactobacillus lactis subsp. lactis LABW1, LABW3, LABW4, Burkholderia cenocepacia VBC7 and Pseudomonas poae VBK1 | jackfruit | rotten jackfruit | cells sprayed over the fruit | Rhizopus stolonifer | [114] |
fruit | LAB | Lactobacillus paracasei ŁOCK0921 (1 tested in situ) (1/(9 in vitro/60)) | wild cherries | plant and human | CFS cultivated with xylitol or galactosyl-xylitol directly on wild cherries | Alternaria brassicicola (1 tested in situ), Alternaria alternata, Aspergillus niger, Fusarium lateritium, Geotrichum candidum, and Mucor hiemalis (6/8) | [115] |
fruit | LAB | Lactic acid bacteria strains LCM5, LAB 58, LAB 13, and LAB 43 (4/6) | apple | plants, fermented wheat bran, pickles, and sauerkraut | cells sprayed over the fruit (wounded and non-wounded) | Penicillium expansum | [116] |
fruit/dairy | LAB | Lactobacillus plantarum TK9 | citrus, apples and yogurt | Chinese naturally fermented congee | cells | Penicillium roqueforti, Penicillium citrinum, Penicillium oxalicum, Aspergillus fumigatus, Aspergillus flavus, and Rhizopus nigricans (6/7) | [117] |
grain/seed | Other bacteria | Acetobacter nigricans AZT 54 (0/1) | maize, sorghum and wheat grains | paddy field soil samples | cereals submerged in suspension | Fusarium sporotrichioides, Fusarium graminearum, Fusarium poae, and Fusarium equiseti (4/10 in vitro) | [82] |
grain/seed | Other bacteria | Bacillus cereus | peanut kernels | entomopathogenic nematode | cells and purified cyclo(4-hydroxy-l-Pro-l-Trp) | Aspergillus flavus | [118] |
fruit | Other bacteria | Bacillus subtilis AFB22 [1/(50/200 in vitro)] | pomegranate | pomegranate leaves and fruits | cells and CFS by spraying on wounded fruits | P. varsoniana (only in situ), A. flavus, A. clavatus, B. humicola, F. graminearum, and R. stolonifer (in vitro) | [119] |
fruit | Other bacteria | Bacillus amyloliquefaciens ZJ01 and ZJ02 | jujube fruit | phyllosphere of Chinese jujube | whole culture in created wounds-prevention treatment | Phoma destructiva (2 strains), Alternaria alterna (2 strains), and Fusicoccum spp. (5/5) | [120] |
fruit | Other bacteria | Bacilllus subtilis V26 | tomato fruit | rhizosphere of almond trees | whole culture, endospores, and CFS in created wounds | Botrytis cinerea | [84] |
fruit | Other bacteria | Paenibacillus polymyxa APEC136 and Bacillus subtilis APEC170 | apple | soil from several apple orchards | cells over created wounds | Colletotrichum gloeosporioides, Colletotrichum acutatum, and Botryosphaeria dothidea | [121] |
fruit | Other bacteria | Bacillus amyloliquefaciens BUZ-14 | apple, orange, grape, and cherries | surface of peach fruit from an orchard | cells, endospores and CFS | Botrytis cinerea, Monilinia fructicola, Monilinia laxa, Penicillium digitatum, Penicillium expansum, and Penicillium italicum | [122] |
fruit | Other bacteria | Cryptococcus laurentii | peach fruit | surfaces of apple fruits | cells in created wounds | Penicillium expansum | [123] |
fruit | Other bacteria | Bacillus amyloliquefaciens CPA-8 | cherries | nectarine surface | wounded fruits packaged with in situ produced volatile organic compounds | Monilia fructicola (1/3) | [124] |
fruit | Other bacteria | Paenibacillus pasadenensis R16 | grape berries | leaf of grapevine plant | wounded fruit submerged in cell suspension | Botrytis cinerea | [125] |
fruit | Yeast | Cryptococcus laurentii 2.3803 | strawberries | not detailed | cells sprayed over fruits prior to harvest | Botrytis cinerea | [126] |
fruit | Yeast | Hanseniaspora uvarum | grape berries | strawberries surface | cells in wounds and fruit submerged in salicylic acid or sodium bicarbonate | Botrytis cinerea | [127] |
fruit | Yeast | Wickerhamomyces anomalus BS91, Metschnikowia pulcherrima MPR3, Aureobasidium pullulans PI1, and Saccharomyces cerevisiae BCA62 | grape berries | fermented olive brine and pomegranate | cells in created wounds | Botrytis cinerea | [71] |
fruit | Yeast | Aureobasidium pullulan (25 strains), Cryptococcus magnus (2 strains), Candida sake 2AM3 [(28/33 in situ) (33/55 in vitro)] | grape berries | surface of grape berries | wounded fruits submerged in cells suspension | Aspergillus tubingensis | [70] |
fruit | Yeast | Candida intermedia and Wickerhamomyces anomalus | avocado | fruits, leaves, and the soil of the avocado orchards | cells in created wounds | Colletotrichum gloeosporioides and Colletotrichum acutatum | [128] |
fruit | Yeast | Hanseniaspora uvarum Y3 | orange | surfaces of grapes in vineyard | cells in created wounds | Penicillium digitatum | [85] |
fruit | Yeast | Pichia membranaefaciens | citrus fruits Citrus sinensis | not detailed | cells in created wounds | Colletotrichum gloerosporioides | [129] |
fruit | Yeast | Rhodotorula minuta ACBL-23, Candida azyma ACBL-44, S. cerevisiae ACBL-52, Rhodotorula mucilaginosa ACBL-68, and Aureobasidium pullulans ACBL-77 | ‘Pera’ orange fruits | citrus leaves, flowers, fruits, and citrus-growing soils | cells in created wounds | Geotrichum citri-aurantii | [130] |
fruit | Yeast | Pichia fermentans (2 strains), Wickerhamomyces anomalus, Kazachstania exigua, and Saccharomyces cerevisiae | lemons | surface of leaves and fruits of different citrus and wash-water from lemon shells | wounded fruits submerged cells suspension | Penicillium digitatum and Penicillium italicum | [131] |
fruit | Yeast | Debaryomyces hansenii KI2a, D. hansenii MI1a, and Wickerhamomyces anomalus BS91 | peach and plum fruits | blue-veined Rokpol cheese and fermented olive brine | cells in created wounds | Monilinia fructigena and Monilinia fructicola | [132] |
fruit | Yeast | Candida tropicalis YZ27 | banana | from bitter gourd | cells in created wounds | Colletotrichum musae | [133] |
fruit | Yeast | Yarrowia lipolytica | grape berries | surface of grapes | cells in created wounds | Talaromyces rugulosus | [134] |
meat | Yeast | Debaromyces hansenii FHSCC 253H | dry-cured ham slices | dry-cured meat products | cells over slices (aw controlled) | Penicillium nordicum | [135] |
meat | Yeast | Debaromyces hansenii 253H and 226G G | dry-fermented sausage | dry-cured meat products | cells over slices after fermentation | Penicillium verrucosum | [136] |
meat | Molds | Penicillium nalgoviense | dry-fermented sausages | TEXEL PN1 from Danisco (Niebüll, Germany) | immersion of sausages in cells suspension | Penicillium verrucosum | [137] |
meat | Molds | Penicillium chrysogenum CECT 20922 | dry-cured ham slices | not detailed | cells | Cladosporium cladosporioides, C. herbarum, and C. oxysporum | [138] |
fruit | Molds | Clonostachys rosea | tomato fruit | not detailed | cells sprayed over the fruit | Botrytis cinerea | [139] |
Product Name | Application Field | Properties | Composition | Manufacturer |
---|---|---|---|---|
Holdbac YM-B or YM-C | fermented food and white cheeses | protection against yeasts and molds | Lactobacillus rhamnosus and Propionibacterium freudenreichii subsp. shermanii | DuPont Danisco |
Holdbac YM-XPM | fermented dairy and mild acidic yogurt | protection against yeasts and molds | Lactobacillus plantarum | DuPont Danisco |
Holdbac YM-XPK | all types of cheeses | protection against yeasts and molds | Lactobacillus plantarum | DuPont Danisco |
FreshQ 1 and FreshQ 4 | cottage cheese | protection against yeasts and molds | Lactobacillus rhamnosus and Lactobacillus paracasei | CHR Hansen |
FreshQ 2 | cottage cheese | protection against yeasts and molds | Lactobacillus rhamnosus | CHR Hansen |
FreshQ 5 | cottage cheese | protection against yeasts and molds | Lactobacillus paracasei | CHR Hansen |
Natamax | fruit juices, wine, surface of dry-ripened food, dairy, and bakery products | protection against yeasts and molds | Natamycin produced by Streptomyces natalensis | DuPont Danisco |
MicroGard | sauces, salad dressings, prepared meals, cured meat, pastas, bakery and dairy products, hash brown potatoes | protection against Gram-positive bacteria, Gram-negative bacteria, yeasts, and molds | Fermentate (skim milk or dextrose) of Propionibacterium freudenreichii subsp. shermani | DuPont Danisco |
Hi Shield P | bakery products, salad dressings, and general used in food industry | protection against molds, yeasts (Pichia anomala), and bacteria (Bacillus subtilis); increase sour taste; and reduce salt content (flavor improver and enhancer) | Fermentate (corn) of lactic acid bacteria and yeasts | HI-FOOD S.p.A. |
Inhibit FOG, Inhibit 2800, Inhibit 1900CW, Inhibit 3600 and Inhibit 2100NF | bakery products, cheeses, meats, salad dressings, condiments, dips, spreads, and meats | protection against molds, yeasts, and Gram-negative bacteria | Fermentates (dextrose, wheat, wheat flour, whey, brown rice) of Propionibacterium freudenreichii | Mezzoni Foods |
Biosafe 10LP | cherries, pome fruits, citrus, and potatoes | protection against Penicillium expansum, Botrytis cinerea, Mucor piriformis, Fusarium sambucinum, Helminthosporium solani, and Rhizopus stolonifer | Pseudomonas syringae | Nu Farm Inc. USA |
Aspire | citrus and pome fruit | protection against molds (P. expansum and Botrytis cinerea) | Candida oleophila | Ecogen Inc. USA |
Befresh | fresh fermented milk products | control the growth of yeast and molds | Lactobacillus paracasei and Propionibacterium freudenreichii subsp. shermanii, | Handary |
Candifruit | pome fruit | protection against Botrytis cinerea, Penicillium expansum, and Rhizopus stolonifer | Candida sake | Sipcam-Inaagri, SA (Valencia, Spain) |
Boni-Protect | pome fruit | protection against Botrytis cinerea, Monilinia fructigena, Penicillium expansum, and Pezicula malicortici | Aureobasidium pullulan | BioFerm GMbH, Germany |
Shemer | citrus fruit, stone fruits, and berries | protection against Aspergillus niger, Botrytis cinerea, Penicillium expansum, Penicillium digitatum, Penicilllium italicum, and Rhizopus stolonifer | Metschnikowia fructicola | Bayer Cropscience, Israel |
Pantovital | citrus and pome fruit | protection against Botrytis cinerea, Penicillium expansum, Penicillium digitatum, Penicillium italicum, and Rhizopus stolonifer | Pantoea agglomerans | BioDURCAL S.L. |
YieldPlus | citrus, apple, and pear fruit | not detailed | Cryptococcus albidus | Anchor Bio-Technologies, Cape Town, South Africa |
Nexy | pome fruit | protection against Botrytis cinerea and Penicillium expansum | Candida oleophila | BioNext sprl, France |
Serenade | grapes, legumes, pome fruits, and peanuts | protection against fungi causing powdery mildew, late blight brown rot, fireblight | Bacillus subtilis | Agra Quees Inc. |
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Leyva Salas, M.; Mounier, J.; Valence, F.; Coton, M.; Thierry, A.; Coton, E. Antifungal Microbial Agents for Food Biopreservation—A Review. Microorganisms 2017, 5, 37. https://doi.org/10.3390/microorganisms5030037
Leyva Salas M, Mounier J, Valence F, Coton M, Thierry A, Coton E. Antifungal Microbial Agents for Food Biopreservation—A Review. Microorganisms. 2017; 5(3):37. https://doi.org/10.3390/microorganisms5030037
Chicago/Turabian StyleLeyva Salas, Marcia, Jérôme Mounier, Florence Valence, Monika Coton, Anne Thierry, and Emmanuel Coton. 2017. "Antifungal Microbial Agents for Food Biopreservation—A Review" Microorganisms 5, no. 3: 37. https://doi.org/10.3390/microorganisms5030037