Microbial Interactions within the Cheese Ecosystem and Their Application to Improve Quality and Safety
Abstract
:1. General Introduction
2. Cheese Starters and Adjunct Cultures
3. Cheese Microbiology
4. The Cheese Microbiota
5. Microbial Interactions in Cheese
5.1. Competition
5.2. Amensalism
5.3. Commensalism
5.4. Mutualism
6. Dynamics of Microbial Communities in Cheese
7. Microbiota-Based Starters
8. Conclusions and Prospects
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Microbial Group/Species | Cheese | Type of Starter | Main Role/s |
---|---|---|---|
Lactic acid bacteria | |||
Lc. lactis subsp. lactis Lc. lactis subsp. cremoris | Most cheeses | Primary | Acidification, flavor development |
S. thermophilus Lb. delbrueckii subsp. lactis | Italian and Swiss types | Primary | Acidification, flavor development |
Leuc. mesenteroides subsp. cremoris Leuc. lactis | Soft and semi-hard | Secondary/adjunct | Flavor development, CO2 production |
Lb. helveticus | Semi-hard, hard | Secondary/adjunct | Flavor development, health benefits |
Lb. casei/Lb. paracasei | Artisanal | Secondary/adjunct | Flavor development |
Lb. plantarum | Artisanal | Secondary/adjunct | Flavor development |
Propionibacteria | |||
Propionibacterium freudenreichii | Swiss-type | Secondary/ripening | Hole formation, flavor development |
Other bacteria | |||
Brevibacterium linens | Smear-ripened | Secondary/ripening | Color, flavor development |
Corynebacterium casei | Smear-ripened | Secondary/ripening | Flavor development |
Fungi | |||
P. camemberti | White moldy | Secondary/ripening | Aspect, texture, and flavor development |
P. roqueforti | Blue-veined | Secondary/ripening | |
G. candidum | Smear-ripened | Secondary/ripening |
Cheese/Type, Country (Milk Type) | Technique | Microbial Target | No. of Specimens | Main Families/Genera/Species (Relative Abundance); Sampling Point | Reference |
---|---|---|---|---|---|
Culturing | |||||
Bryndza/soft Feta-type, Slovakia (Sheep) | Culturing | Fungi | 5 species | Geotrichum candidum > Kluyveromyces marxianus > Pichia fermentans > Candida inconspicua > Trichosporon cutaneum | Laurencík et al. [106] |
Cabrales/blue-veined, Spain (Cow, sheep, and goat) | Culturing | LAB | 15 species | Lc. lactis subsp. lactis > Lb. plantarum > Leuc. mesenteroides > Leuc. citreum > Enterococcus > Lb. paracasei | Flórez et al. [107] |
Gubbeen/smear-ripened, Ireland (Cow) | Culturing | Corynebacteria | 39 species | Corynebacterium casei (50.2%) > Corynebacterium mooreparkense (26%) > Microbacterium gubbeenense (12.8%); cheese rind | Brennan et al. [48] |
May bryndza/soft, Slovakia (Sheep) | Culturing | Bacteria Fungi | 5 species 17 species | Lc. lactis subsp. cremoris > Lc. lactis subsp. lactis > Mannheimia glucosida G. candidum > Penicillium > Beauveria brongniartii > Alternaria alternata | Pangallo et al. [108] |
Rinds of 33 cheeses/smear-ripened, various countries (Cow, sheep, or goat) | Culturing, sequencing | Microbes | 104 bacterial genera, 39 fungal genera | Staphylococcus (78%) > Brevibacterium (75%) > Corynebacterium (75%) > Arthrobacter (66%) > Lactococcus (50%) > Enterococcus (41%) > Brachybacterium (38%) > Microbacterium (38%) > Psychrobacter (33%) > Halomonas (31%) > Lactobacillus (25%) > Streptococcus (22%) > Marinilactibacillus (22%) > Pseudoalteromonas (22%) > Agrococcus (19%) > Micrococcus (19%) > Vibrio (19%) > Vagococcus (16%) > Facklamia (16%) Debaryomyces (86%) > Yarrowia (57%) > Candida (54%) > Geotrichum (49%) > Kluyveromyces (32%) > Pichia (22%) > Penicillium (19%) > Scopulariopsis (8%) > Fusarium (8%) | Irlinger et al. [12] |
Scamorza Altamurana/pasta filata, Italy (Cow) | Culturing | LAB | 10 species | Lb. delbrueckii > Streptococcus macedonicus > S. thermophilus > Enterococcus durans > Lb. fermentum > Lb. paracasei | Baruzzi et al. [28] |
Culturing and molecular methods | |||||
Casín/kneaded, Spain (Cow) | Culturing DGGE | Bacteria | 14 species | Lc. lactis subsp. lactis > Lactococcus garvieae > Staphylococcus saprophyticus > Klebsiella > Lb. plantarum | Alegría et al. [25] |
Bacteria (V1-V2 16S rDNA) | 14 OTUs | Lc. lactis, Streptococcus parauberis, S. thermophilus, Lc. garvieae, Lb. plantarum, Enterobacter, Corynebacterium variabile, Lb. paracasei, Macrococcus caseolyticus | |||
Castelmagno/semi-hard, Italy (Cow) | Culturing PCR-DGGE | LAB Bacteria (V1 16S rDNA) | 11 species 7 OTUs | Lc. lactis subsp. lactis > Lb. plantarum > Lc. paracasei >Enterococcus faecium >E. durans Lb. plantarum, Lb. kefiranofaciens, Lactobacillus, Lc. lactis, Streptococcus agalactiae, M. caseolyticus | Dolci et al. [44] |
Cueva de la Magahá/hard, Spain (Goat) | Culturing PCR-TTGE | Bacteria Bacteria (V3 16S rDNA) | 10 species 8 species | Lb. paracasei > Lb. plantarum > Lb. brevis > Lactobacillus > Enterococcus Lb. plantarum, Lb. brevis, Lc. Lactis, S. thermophilus, Staphylococcus equorum, Lb. curvatus, Lb. paracasei | Martín-Platero et al. [45] |
Grana Padano/hard, Italy (Cow) | LH-PCR | LAB | 6 species | Lb. rhamnosus > Lb. paracasei > Lb. delbrueckii > Pediococcus acidilactici | Santarelli et al. [22] |
Livarot/smear-ripened, France (Cow) | Culturing Cloning | Bacteria/yeasts Bacteria (V4 16S rDNA) | 8 bacteria, 5 yeasts species 8 species | M. gubbeenense > Leucobacter komagatae > Halomonas; cheese rind Candida catenulata > Candida intermedia > G. candidum > Geotrichum > Yarrowia lipolytica; cheese rindHalomonas > L. komagatae > M. gubbeenense; cheese rind | Mounier et al. [43] |
Nottinghamshire/blue-veined, UK (Cow) | Culturing PCR-DGGE | Bacteria Bacteria (V3, V4-V5, V6-V8 16S rDNA) | 12 species 11 OTUs | Lc. lactis subsp. lactis > E. faecalis > Kokuria > Lactobacillus Lc. lactis, Lb. plantarum, Staph. equorum | Yunita and Dodd [55] |
Ragusano/pasta filata, Italy (Cow) | PCR-DGGE | Bacteria (V6-V8, V1-V3 16S rDNA or rRNA) | 12 species | S. thermophilus, Lb. fermentum, Lb. delbrueckii, Lc. lactis, Leuc. mesenteroides, Lb. casei, Enterococcus hirae > E. faecalis | Randazzo et al. [61] |
Salers/semi-hard, France (Cow) | PCR-SSCP | Bacteria (V2 16S rDNA) | 9 OTUs | E. faecium, Leuconostoc, Enterobacteriaceae, Bacillus thuringiensis, S. thermophilus, Leuc. pseudomesenteroides, Lb. pentosus, Corynebacterium variabilis, Brachybacterium nesterenkovii | Duthoit et al. [66] |
Saint Nectaire/smear-ripened, France (Cow) | Culturing SSCP-PCR | Bacteria Bacteria | 21 species 12 OTUs | Lc. lactis > Staphylococcus fleurettii > E. faecalis > S. thermophilus > Marinilactibacillus psychrotolerans > Chryseobacterium > Klebsiella Lc. lactis, S. thermophilus, Clostridium confusum, Nocardioides dubius, Arthrobacter psychrolactophilus, Enterobacter agglomerans | Delbès et al. [46] |
Molecular methods/high throughput sequencing | |||||
Artisan cheeses/various, Ireland (Cow, goat, or sheep) | Pyrosequencing | Bacteria (V4 16S rDNA) | 5 phyla 21 genera | Lactococcus (50–90%) > Lactobacillus > Leuconostoc > Pseudomonas > Psychrobacter > Staphylococcus > Arthrobacter > Faecalibacterium; common to 62 cheeses | Quigley et al. [76] |
Buryatian/soft, Kazakhstan (Cow) | PacBio sequencing | Microbes | 7 phyla, 82 genera, 145 species | Lactococcus (51.46%) > Streptococcus (17.81%) > Pseudomonas (5.48%) > Acetobacter (4.83%) > Klebsiella (3.36%) > Lactobacillus (2.36%) > Acinetobacter (1.84%) > Raoultella (1.63%) | Jin et al. [79] |
Canestrato Pugliese/hard, Italy (Sheep) | Pyrosequencing | Bacteria (V1-V3 16S rDNA) | 28 genera | Lactococcus (87.2%) > Lactobacillus (4.8%; mainly Lb. plantarum and Lb. sakei) > Leuconostoc (3.9%) | De Pasquale et al. [109] |
Cheddar/semi-hard, UK (Cow) | Illumina sequencing | Bacteria (V4 16S rDNA) | 159 OTUs | Streptococcus > Lactococcus > Lactobacillus > Staphylococcus (70%); interior | Afshari et al. [110] |
Gouda-like cheese/semi-hard, USA (Cow) | Illumina sequencing | Bacteria (V4 16S rDNA) | 36 genera | Bacillaceae > Lactococcus > Lactobacillus > Streptococcus > Staphylococcus | Salazar et al. [111] |
Cotija/hard, Mexico (Cow) | Illumina sequencing | Microbes | 31 phyla, 574 genera | Lb. plantarum > Leuc. mesenteroides > Weissella paramesenteroides (>80%) Aerococcus > Enterococcus > Lactococcus > Staphylococcus (<10%) | Escobar-Zepeda et al. [82] |
Grana/hard, Italy (Cow) | RT-PCR-DGGE Pyrosequencing | Bacteria (V1 16S rDNA) Bacteria (V1-V3 16S rDNA) | 16 OTUs 25 genera | Lb. helveticus, Lb. delbrueckii, S. thermophilus, Lb. acidophilus, Lb. rhamnosus, Acetobacter baumanii, Propionibacterium Lb. helveticus > Propionibacterium > Lb. delbrueckiii > Lb. casei > Lb. rhamnosus > S. thermophilus > Staphylococcus > Lb. brevis | Alessandria et al. [95] |
Artisanal cheeses/soft, Kazakhstan (Cow) | PacBio sequencing | Microbes | 14 phyla, 140 genera, 238 species | Lc. lactis (28.93%) > Lb. helveticus (26.43%) > S. thermophilus (12.18%) > Lb. delbrueckii (12.15%) | Li et al. [80] |
Ocosingo/semi-hard, Mexico (Cow) | Pyrosequencing | Bacteria (V1 16S rDNA) | 162 OTUs | S. thermophilus > Lc. lactis > Lb. helveticus > Lb. delbrueckii > Lb. plantarum (70%); interior | Aldrete-Tapia et al. [17] |
Tomme d’Orchies/semi-hard, France (Cow) | Illumina sequencing | Bacteria (V1-V3 16S rDNA) | 10 species core, 21 species surface | Lactococcuss > Streptococcus (66%); interior Lactobacillus > Lactococcus > Corynebacterium > Micrococcales > Psychrobacter (80%); surface | Ceugniez et al. [83] |
Tomme d’Orchies/semi-hard, France (Cow) | Illumina sequencing | Fungi 5.8S-ITS2 | 30 OTUs | Y. lipolytica > G. candidum/Galactomyces geotrichum (99%); interior Y. lipolytica > G. candidum/Galactomyces geotrichum (98%); surface | Ceugniez et al. [112] |
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Mayo, B.; Rodríguez, J.; Vázquez, L.; Flórez, A.B. Microbial Interactions within the Cheese Ecosystem and Their Application to Improve Quality and Safety. Foods 2021, 10, 602. https://doi.org/10.3390/foods10030602
Mayo B, Rodríguez J, Vázquez L, Flórez AB. Microbial Interactions within the Cheese Ecosystem and Their Application to Improve Quality and Safety. Foods. 2021; 10(3):602. https://doi.org/10.3390/foods10030602
Chicago/Turabian StyleMayo, Baltasar, Javier Rodríguez, Lucía Vázquez, and Ana Belén Flórez. 2021. "Microbial Interactions within the Cheese Ecosystem and Their Application to Improve Quality and Safety" Foods 10, no. 3: 602. https://doi.org/10.3390/foods10030602