The Complex Microbiota of Raw Milk

Quigley, Lisa; O'Sullivan, Orla; Stanton, Catherine; Beresford, Tom P.; Ross, R. Paul; Fitzgerald, Gerald F.; Cotter, Paul D.

doi:10.1111/1574-6976.12030

Cited by 919Milk Quality and Mastitis in Dairy CowsProbiotics and Fermented FoodsAnimal Diversity and Health Studies

The Complex Microbiota of Raw Milk

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Quigley, Lisa, O'Sullivan, Orla, Stanton, Catherine, Beresford, Tom P., Ross, R. Paul, Fitzgerald, Gerald F., Cotter, Paul D.·2013·FEMS Microbiology Reviews

DOI 10.1111/1574-6976.12030

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Abstract

Here, we review what is known about the microorganisms present in raw milk, including milk from cows, sheep, goats and humans. Milk, due to its high nutritional content, can support a rich microbiota. These microorganisms enter milk from a variety of sources and, once in milk, can play a number of roles, such as facilitating dairy fermentations (e.g. Lactococcus, Lactobacillus, Streptococcus, Propionibacterium and fungal populations), causing spoilage (e.g. Pseudomonas, Clostridium, Bacillus and other spore-forming or thermoduric microorganisms), promoting health (e.g. lactobacilli and bifidobacteria) or causing disease (e.g. Listeria, Salmonella, Escherichia coli, Campylobacter and mycotoxin-producing fungi). There is also concern that the presence of antibiotic residues in milk leads to the development of resistance, particularly among pathogenic bacteria. Here, we comprehensively review these topics, while comparing the approaches, both culture-dependent and culture-independent, which can be taken to investigate the microbial composition of milk.

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Environmental factors are crucial in shaping the composition of milk microbiota.
“Environmental factors are crucial in shaping the composition of milk microbiota [38,55,60,61,62,63].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [60]
The indigenous microbiota of raw milk is diverse and heterogeneous and has a significant impact on the overall microbiota of cheese.
“The indigenous microbiota of raw milk is usually quite diverse and heterogeneous and has a significant impact on the overall microbiota of cheese [24].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [24]
Bacteriophages targeting key starter or adjunct cultures are associated with changes in fermentation resulting in slow acidification and undesirable organoleptic characteristics of cheese.
“Phages targeting key starter or adjunct cultures have been associated with changes in fermentation resulting in slow acidification and undesirable organoleptic characteristics of the cheese [24].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [24]

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Bifidobacteria and Their Role
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Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing
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Characteristics of Shiga toxin-producing Escherichia coli from meat and milk products of different origins and association with food producing animals as main contamination sources
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Basic and incentive payments for goat and sheep milk in relation to quality
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Bacterial Community Dynamics during Production of Registered Designation of Origin Salers Cheese as Evaluated by 16S rRNA Gene Single-Strand Conformation Polymorphism Analysis
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Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and-independent approaches
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Diversity of lactic acid bacteria associated with traditional fermented dairy products in Mongolia.
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High temperature, short time pasteurization temperatures inversely affect bacterial numbers during refrigerated storage of pasteurized fluid milk
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Silage and the safety and quality of dairy foods: A review
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The technological characteristics of Debaryomyces hansenii and Yarrowia lipolytica and their potential as starter cultures for production of Danablu
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Milk Fermented by Propionibacterium freudenreichii Induces Apoptosis of HGT-1 Human Gastric Cancer Cells
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Factors affecting goat meat production and quality
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An Outbreak ofYersinia enterocoliticaO:8 Infections Associated with Pasteurized Milk
Ackers, M., Schoenfeld, S., Markman, J. D., Smith, M., Nicholson, M. A., DeWitt, W. E., Cameron, D. N., Griffin, P. M., & Slutsker, L. (2000) · The Journal of Infectious Diseases · doi:10.1086/315436 · Cited by 145 · see citing works
Complete Sequences of Four Plasmids of Lactococcus lactis subsp. cremoris SK11 Reveal Extensive Adaptation to the Dairy Environment
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Crohn’s disease and the mycobacterioses: A quarter century later. Causation or simple association?
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Environmental Streptococcal Intramammary Infections of the Bovine Mammary Gland
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The fate of indigenous microbiota, starter cultures, Escherichia coli, listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR
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Use of autolytic starter systems to accelerate the ripening of Cheddar cheese
Hannon, J. A., Wilkinson, M. G., Delahunty, C. M., Wallace, J. M., Morrissey, P. A., & Beresford, T. P. (2003) · International Dairy Journal · doi:10.1016/s0958-6946(02)00178-4 · Cited by 141 · cited 2× · see citing works
“Lactobacillus helveticus is also characterised by its ability to grow at relatively high temperatures (55 °C; Kiernan et al., 2000; Hannon et al., 2003) and is the most proteolytic of the LAB frequently used in the manufacture of dairy products.”
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The late blowing in cheese: a new molecular approach based on PCR and DGGE to study the microbial ecology of the alteration process
Cocolin, L., Innocente, N., Biasutti, M., & Comi, G. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(03)00296-4 · Cited by 139 · see citing works
Antihypertensive activity of milk fermented by Enterococcus faecalis strains isolated from raw milk
Muguerza, B., Ramos, M., Sánchez, E., Manso-Silván, M. A., Miguel, M., Aleixandre, A., Delgado, M. A., & Recio, I. (2005) · International Dairy Journal · doi:10.1016/j.idairyj.2005.01.001 · Cited by 139 · see citing works
Antimicrobial activity and antibiotic resistance of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese)
Herreros, M. A., Sandoval, H., González, L., Castro, J. M., Fresno, J. M., & Tornadijo, M. E. (2005) · Food Microbiology · doi:10.1016/j.fm.2004.11.007 · Cited by 139 · see citing works
Staphylococcus epidermidis strains isolated from breast milk of women suffering infectious mastitis: potential virulence traits and resistance to antibiotics
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Use of PCR-Based Methods for Rapid Differentiation of Lactobacillus delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis
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Stability of microbial communities in goat milk during a lactation year: Molecular approaches
Callon, C., Duthoit, F., Delbès, C., Ferrand, M., Lefrileux, Y., CRÉMOUX, R. D., & Montel, M. (2007) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2007.05.004 · Cited by 136 · see citing works
Postgenomic Analysis of Streptococcus thermophilus Cocultivated in Milk with Lactobacillus delbrueckii subsp. bulgaricus : Involvement of Nitrogen, Purine, and Iron Metabolism
Herve‐Jimenez, L., Guillouard, I., Guédon, É., Boudebbouze, S., Pascal Hols, A., Monnet, V., Maguin, E., & Rul, F. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01984-08 · Cited by 136 · see citing works
The antimicrobial activity of donkey milk and its microflora changes during storage
Zhang, X., Zhao, L., Jiang, L., Dong, M.-L., & Ren, F. (2008) · Food Control · doi:10.1016/j.foodcont.2008.01.005 · Cited by 133 · see citing works
Comparison of culture-dependent and -independent methods for bacterial community monitoring during Montasio cheese manufacturing
Carraro, L., Maifreni, M., Bartolomeoli, I., Martino, M. E., Novelli, E., Frigo, F., Marino, M., & Cardazzo, B. (2011) · Research in Microbiology · doi:10.1016/j.resmic.2011.01.002 · Cited by 132 · see citing works
Classification of Bacteriocins from Gram-Positive Bacteria
Rea, M. C., Ross, R. P., Cotter, P. D., & Hill, C. (2011) · Springer eBooks · doi:10.1007/978-1-4419-7692-5_3 · Cited by 129 · see citing works
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Diversity and assessment of potential risk factors of Gram-negative isolates associated with French cheeses
Coton, M., Delbès, C., Irlinger, F., Desmasures, N., Flèche‐Matéos, A. L., Stahl, V., Montel, M.-C. M.-C., & Coton, E. (2011) · Food Microbiology · doi:10.1016/j.fm.2011.08.020 · Cited by 129 · see citing works
Molecular analysis of bacterial communities in raw cow milk and the impact of refrigeration on its structure and dynamics
Raats, D., Ofek, M., Minz, D., & Halpern, M. (2010) · Food Microbiology · doi:10.1016/j.fm.2010.10.009 · Cited by 128 · see citing works
FLAVOR DEVELOPMENT AND MICROBIOLOGY OF SWISS CHEESE-A REVIEW
Langsrud, T., & Reinbold, G. W. (1973) · Journal of Milk and Food Technology · doi:10.4315/0022-2747-36.12.593 · Cited by 128 · see citing works
Artisanal and experimental Pecorino Siciliano cheese: Microbial dynamics during manufacture assessed by culturing and PCR–DGGE analyses
Randazzo, C. L., Vaughan, E. E., & Caggia, C. (2006) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2005.11.002 · Cited by 127 · see citing works
Dairy propionibacteria as human probiotics: A review of recent evidence
Cousin, F., Mater, D. D. G., Foligné, B., & Jan, G. (2010) · Dairy Science and Technology · doi:10.1051/dst/2010032 · Cited by 127 · see citing works
Milk and Dairy Products
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Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec
Lavoie, K., Touchette, M., St‐Gelais, D., & Labrie, S. (2011) · Dairy Science and Technology · doi:10.1007/s13594-011-0051-4 · Cited by 126 · see citing works
Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm-dairies
Rosengren, Å., Fabricius, A., Guss, B., Sylvén, S., & Lindqvist, R. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.10.004 · Cited by 126 · see citing works
Genetic diversity in proteolytic enzymes and amino acid metabolism among Lactobacillus helveticus strains
Broadbent, J. R., Cai, H., Larsen, R. L., Hughes, J. E., Welker, D. L., De Carvalho, V. G., Tompkins, T. A., Ardö, Y., Vogensen, F., De Lorentiis, A., et al. (2011) · Journal of Dairy Science · doi:10.3168/jds.2010-4068 · Cited by 124 · cited 1× · see citing works
“These include rapid autolysis of the strains, which results in the release of intracellular enzymes and a reduction in bitterness and increased flavour notes in cheese (Broadbent et al., 2011).”
Background
The Influence of Methods of Collection and Storage on the Bacteriology of Human Milk
West, P. A., Hewitt, J. H., & Murphy, O. M. (1979) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1979.tb00820.x · Cited by 124 · see citing works
Chapter 1 Phage Evolution and Ecology
Abedon, S. T. (2009) · Advances in applied microbiology · doi:10.1016/s0065-2164(08)01001-0 · Cited by 121 · see citing works
Seasonal influence on heat‐resistant proteolytic capacity of Pseudomonas lundensis and Pseudomonas fragi , predominant milk spoilers isolated from Belgian raw milk samples
Marchand, S., Heylen, K., Messens, W., Coudijzer, K., Vos, P. D., Dewettinck, K., Herman, L., Block, J. D., & Heyndrickx, M. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01785.x · Cited by 120 · see citing works
PCR-DGGE fingerprints of microbial succession during a manufacture of traditional water buffalo mozzarella cheese
Ercolini, D., Mauriello, G., Blaiotta, G., Moschetti, G., & Coppola, R. (2004) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2003.02146.x · Cited by 120 · see citing works
Antifungal activity of non-starter lactic acid bacteria isolates from dairy products
Voulgari, K., Hatzikamari, M., Delepoglou, A., Georgakopoulos, P., LITOPOULOU‐TZANETAKI, E., & Tzanetakis, N. (2009) · Food Control · doi:10.1016/j.foodcont.2009.04.007 · Cited by 120 · see citing works
Lactococcus pisciumsp. nov. a newLactococcusspecies from salmonid fish
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Bacteriocins produced by wild Lactococcus lactis strains isolated from traditional, starter-free cheeses made of raw milk
Alegría, Á., Delgado, S., Roces, C., López, B., & Mayo, B. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.07.029 · Cited by 119 · see citing works
Lactic acid bacteria from raw milk as potentially beneficial strains to prevent bovine mastitis
Espeche, M. C., Pellegrino, M., Frola, I. D., Larriestra, A. J., Bogni, C. I., & Nader-Macı́as, M. E. (2012) · Anaerobe · doi:10.1016/j.anaerobe.2012.01.002 · Cited by 119 · see citing works
Environmental bacteria and childhood asthma
Ege, M. J., Mayer, M., Schwaiger, K., Mattes, J., Pershagen, G., van Hage, M., Scheynius, A., Bauer, J., & von Mutius, E. (2012) · Allergy · doi:10.1111/all.12028 · Cited by 118 · see citing works
Milk Contamination and Resistance to Processing Conditions Determine the Fate of Lactococcus lactis Bacteriophages in Dairies
Madera, C., Monjardín, C., & Suárez, J. E. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.12.7365-7371.2004 · Cited by 117 · see citing works
Bifidobacteria in Feces and Environmental Waters
Lamendella, R., Domingo, J. W. S., Kelty, C. A., & Oerther, D. B. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01221-07 · Cited by 117 · see citing works
Adaptation of the brucellae to their intracellular niche
Roop, R. M., Bellaire, B. H., Valderas, M. W., & Cardelli, J. A. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04017.x · Cited by 116 · see citing works
Effect of Pasteurization on Survival of Mycobacterium paratuberculosis in Milk
Gao, A., Mutharia, L. M., Chen, S., Rahn, K., & ODUMERU, J. A. (2002) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(02)74408-1 · Cited by 116 · see citing works
Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae
Richards, V. P., Lang, P., Bitar, P. D. P., Tristan, L., Schukken, Y. H., Zadoks, R. N., & Stanhope, M. J. (2011) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2011.04.019 · Cited by 116 · see citing works
Fungal diversity in cow, goat and ewe milk
Delavenne, E., Mounier, J., Asmani, K., Jany, J., Barbier, G., & Blay, G. L. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.08.029 · Cited by 115 · see citing works
Detection and characterization of a bacteriocin, garviecin L1-5, produced by Lactococcus garvieae isolated from raw cow’s milk
Villani, F., Aponte, M., Blaiotta, G., Mauriello, G., Pepe, O., & Moschetti, G. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01261.x · Cited by 115 · see citing works
The Dairy Leuconostoc: Use in Dairy Products
Vedamuthu, E. R. (1994) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(94)77215-5 · Cited by 114 · cited 2× · see citing works
“Leuconostoc spp. grow poorly in milk due to a lack of sufficient proteolytic activity and thus require the addition, or generation by other microorganisms, of amino acids or peptides to stimulate growth (Vedamuthu, 1994; Hemme & Foucaud-Scheunemann, 2004).”
Background
Lactobacillus fermentum CECT 5716 is safe and well tolerated in infants of 1–6 months of age: A Randomized Controlled Trial
Gil‐Campos, M., Díaz-López, M. Á., Rodriguez-Benítez, M. V., Romero, J., Roncero, I., Linares, M. D., Maldonado, J. A., López‐Huertas, E., Berwind, R., Ritzenthaler, K. L., et al. (2011) · Pharmacological Research · doi:10.1016/j.phrs.2011.11.016 · Cited by 113 · see citing works
Can farm milk consumption prevent allergic diseases?
Braun‐Fahrländer, C., & von Mutius, E. (2010) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2010.03665.x · Cited by 113 · see citing works
Safety assessment of dairy microorganisms: Propionibacterium and Bifidobacterium
Meile, L., Blay, G. L., & Thierry, A. (2007) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2007.08.019 · Cited by 112 · see citing works
Diacetyl production by different strains of Lactococcus lactis subsp. lactis var. diacetylactis and Leuconostoc spp.
Hugenholtz, J., & Starrenburg, M. J. C. (1992) · Applied Microbiology and Biotechnology · doi:10.1007/bf00169412 · Cited by 111 · see citing works
Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis
Ward, P. N., Holden, M. T. G., Leigh, J. A., Lennard, N. J., Bignell, A., Barron, A., Clark, L., Quail, M. A., Woodward, J., Barrell, B. G., et al. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-54 · Cited by 110 · see citing works
Microbiological assessment and evaluation of rehydration instructions on powdered infant formulas, follow-up formulas, and infant foods in Malaysia
Sani, N. A., Hartantyo, S. H. P., & Forsythe, S. J. (2012) · Journal of Dairy Science · doi:10.3168/jds.2012-5409 · Cited by 109 · see citing works
Macedocin, a Food-Grade Lantibiotic Produced by Streptococcus macedonicus ACA-DC 198
Georgalaki, M. D., den Berghe, E. V., Kritikos, D., Devreese, B. V., BEEUMEN, J. V., Kalantzopoulos, G., Vuyst, L. D., & Tsakalidou, E. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.12.5891-5903.2002 · Cited by 108 · see citing works
Culture-independent exploration of the teat apex microbiota of dairy cows reveals a wide bacterial species diversity
Braem, G., Vliegher, S. D., Verbist, B., Heyndrickx, M., Leroy, F., & Vuyst, L. D. (2011) · Veterinary Microbiology · doi:10.1016/j.vetmic.2011.12.031 · Cited by 107 · see citing works
THE USE AND MEANING OF THE TERM ‘PSYCHROPHILIC’
Eddy, B. P. (1960) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1960.tb00195.x · Cited by 106 · see citing works
Aflatoxin M1 in raw and ultra high temperature-treated milk commercialized in Portugal
Martins, M. L., & Martins, H. M. (2000) · Food Additives & Contaminants · doi:10.1080/026520300420457 · Cited by 105 · see citing works
Phenotypic typing, technological properties and safety aspects of Lactococcus garvieae strains from dairy environments
Fortina, M. G., Ricci, G., Foschino, R. C., Picozzi, C., Dolci, P., Zeppa, G., Cocolin, L., & Manachini, P. L. (2007) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.03265.x · Cited by 105 · see citing works
A survey on the microbiological and chemical composition of buffalo milk in China
Han, B., Meng, Y., Li, M., Yang, Y.-X., Ren, F., Zeng, Q., & Nout, M. J. R. (2006) · Food Control · doi:10.1016/j.foodcont.2006.03.011 · Cited by 104 · see citing works
Detection of Airborne Lactococcal Bacteriophages in Cheese Manufacturing Plants
Verreault, D., Gendron, L., Rousseau, G. M., Veillette, M., Massé, D. I., Lindsley, W. G., Moineau, S., & Duchaine, C. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01391-10 · Cited by 103 · see citing works
Streptococcus thermophilus Core Genome: Comparative Genome Hybridization Study of 47 Strains
Rasmussen, T. B., Danielsen, M., Valina, O., Garrigues, C., Johansen, E., & Pedersen, M. B. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00132-08 · Cited by 102 · see citing works
Quantitative and qualitative microbial analysis of raw milk reveals substantial diversity influenced by herd management practices
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Complete Sequencing and Pan-Genomic Analysis of Lactobacillus delbrueckii subsp. bulgaricus Reveal Its Genetic Basis for Industrial Yogurt Production
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Tsakalidou E & Odos I (2012) Microbiota of Goat's Milk and Goat's Milk Cheese. Proceedings of First Asia Dairy Goat Conference, pp. 40-41. University Putra Malaysia and the Food and Agricultural Organisation on the United Nations (FAO), Kuala Lumpur, Malaysia.

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“Phages targeting key starter or adjunct cultures have been associated with changes in fermentation resulting in slow acidification and undesirable organoleptic characteristics of the cheese [24].”
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Invited review: Microbiota of the bovine udder: Contributing factors and potential implications for udder health and mastitis susceptibility
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Authors: Quigley, L., O'Sullivan, O., Stanton, C., Beresford, T. P., Ross, R. P., Fitzgerald, G. F., & Cotter, P. D.
Affiliations: Teagasc - The Irish Agriculture and Food Development Authority (IE)
University College Cork (IE)
Corresponding author: Cotter, Paul D.
ORCID: Stanton, Catherine
Beresford, Tom P.
Ross, R. Paul
Cotter, Paul D.
Venue: FEMS Microbiology Reviews
Publisher: Oxford University Press (OUP)
Published: 2013-09
Volume: 37
Issue: 5
Pages: 664-698
ISSN: 0168-6445 (ISSN-L)
1574-6976
DOI: 10.1111/1574-6976.12030
OpenAlex: W2104638531
Cited by: 919
References: 323
Citations by year: 2026: 58 · 2025: 95 · 2024: 115 · 2023: 88 · 2022: 100 · 2021: 100 · 2020: 82 · 2019: 62 · 2018: 65 · 2017: 57 · 2016: 48 · 2015: 25 · 2014: 22 · 2013: 1
FWCI: 5.57
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Microbiology Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: Teagasc
FP7 Food, Agriculture and Fisheries, Biotechnology
Topics: Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Milk Quality and Mastitis in Dairy Cows
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Agricultural and Biological Sciences › Food Science › Animal Diversity and Health Studies
Keywords: raw milk microbiota, milk spoilage, dairy fermentation, Lactococcus, Lactobacillus, Bifidobacterium, Listeria, Salmonella, antibiotic resistance, antibiotic residues, mycotoxigenic fungi, Pseudomonas, Clostridium, thermoduric bacteria, cow's milk, sheep milk, goat milk, breast milk
MeSH terms: Animals, Humans, Milk, Milk, Human, Food Safety, Food Storage, Microbiota

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