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Microbial Ecology of Dairy Products: From Diversity to Functions

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 27152

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Special Issue Editors

Dr. Pascal Bonnarme

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Guest Editor

AgroParisTech INRA, Ctr Biotechnol Agroind, INRA, UMR Genie & Microbiol Proc Alimentaires 782, F-78850 Thiverval Grignon, France
Interests: fermented products; food microbial community design; microbial metabolism; aromatic compounds production
Special Issues, Collections and Topics in MDPI journals

Dr. Christophe Chassard

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Guest Editor

INRA Aurillac, l'Unité de Recherche Fromagères (URF), Centre de recherche Auvergne-Rhônes-Alpes, 20 rue Côte de Reyne, 15000 Aurillac, France
Interests: cheese; food microbiota; functionnality of microbes; microbial ecosystems; health impact
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Microbial ecology of dairy products is an important and growing area of research in food microbiology. There is a need to understand microbial interactions, microbe–matrix interactions, and the origins and diversity of food microbes, as well as their functionality at different scales (e.g., lab, dairy product models, dairy artisanal and industrial products). The emergence of advanced technologies, including next-generation sequencing approaches and related omics approaches, offer new perspectives for research to deeply investigate the food microbiome. Any research related to dairy fermentation, from the production to the biopreservation of dairy products, will be considered in this topic. This includes the phenotypic and genomic characterization of dairy microbes and communities, the development of microbial solutions (starters and other technological microbes) and investigations of complex microbial ecosystems from origin and diversity to function. We want to share knowledge about dairy food technology and safety, targeting most of the large portfolio of dairy products (e.g., milk, raw milk, any foods made from fermented milk, cheese).

Dr. Pascal Bonnarme
Dr. Christophe Chassard
Guest Editors

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Keywords

Fermented dairy products
Food microbiome
Functions of dairy microbes
Microbial diversity and origin
Omics technologies
Dairy technology

Published Papers (10 papers)

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Research

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16 pages, 1970 KiB

Open AccessArticle

Dietary Live Yeast Supplementation Influence on Cow’s Milk, Teat and Bedding Microbiota in a Grass-Diet Dairy System

by Isabelle Verdier-Metz, Céline Delbès, Matthieu Bouchon, Etienne Rifa, Sébastien Theil, Frédérique Chaucheyras-Durand, Eric Chevaux, Lysiane Dunière and Christophe Chassard

Microorganisms 2023, 11(3), 673; https://doi.org/10.3390/microorganisms11030673 - 06 Mar 2023

Cited by 1 | Viewed by 1346

Abstract

The supplementation of animal feed with microbial additives remains questioning for the traditional or quality label raw milk cheeses with regard to microbial transfer to milk. We evaluated the effect of dietary administration of live yeast on performance and microbiota of raw milk, teat skin, and bedding material of dairy cows. Two balanced groups of cows (21 primiparous 114 ± 24 DIM, 18 multiparous 115 ± 33 DIM) received either a concentrate supplemented with Saccharomyces cerevisiae CNCM I-1077 (1 × 10¹⁰ CFU/d) during four months (LY group) or no live yeast (C group). The microbiota in individual milk samples, teat skins, and bedding material were analysed using culture dependent techniques and high-throughput amplicon sequencing. The live yeast supplementation showed a numerical increase on body weight over the experiment and there was a tendency for higher milk yield for LY group. A sequence with 100% identity to that of the live yeast was sporadically found in fungal amplicon datasets of teat skin and bedding material but never detected in milk samples. The bedding material and teat skin from LY group presented a higher abundance of Pichia kudriavzevii reaching 53% (p < 0.05) and 10% (p < 0.05) respectively. A significant proportion of bacterial and fungal ASVs shared between the teat skin and the milk of the corresponding individual was highlighted. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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16 pages, 753 KiB

Open AccessArticle

Prevalence, Virulence Potential, and Growth in Cheese of Bacillus cereus Strains Isolated from Fresh and Short-Ripened Cheeses Sold on the Italian Market

by Erica Tirloni, Cristian Bernardi, Francesco Celandroni, Diletta Mazzantini, Mariacristina Massimino, Simone Stella and Emilia Ghelardi

Microorganisms 2023, 11(2), 521; https://doi.org/10.3390/microorganisms11020521 - 18 Feb 2023

Cited by 5 | Viewed by 1845

Abstract

This study investigated B. cereus presence in 122 samples belonging to 34 typologies of fresh or short-ripened cheeses made from cow, sheep, goat, or buffalo pasteurized milk, and sold on the Italian market. B. cereus was isolated at a prevalence of 9.8%, with a marked variability among cheese categories, and at low counts (always below 2.26 Log CFU/g). Twelve isolates were identified by MALDI-TOF analysis and typified by RAPD PCR as belonging to different B. cereus strains. All the strains were tested for the production of hemolysin BL, phosphatidylcholine-specific phospholipase C, proteases, and biofilm formation, and for the presence of chromosomal toxin-encoding genes (sph, plcA, cytK, entFM, bcet, nheA, nheB, nheC). Overall, 92% of strains harbored bcet, 75% the three genes nheA, nheB, and nheC, as well as plcA and sph, 67% entFM, and 33% cytK. All strains showed biofilm-forming ability. A chemical-physical characterization of the cheeses was also performed to show their suitability as substrates for B. cereus growth, showing high heterogeneity in terms of pH, aw, salt content, and concentration of organic acids. Finally, the ability to support spore germination and vegetative cell growth of a selected cheese was investigated in spores-inoculated samples maintained at 10 °C and 15 °C, showing the inhibitory effect of low storage temperatures. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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16 pages, 2053 KiB

Open AccessArticle

An Insight into Goat Cheese: The Tales of Artisanal and Industrial Gidotyri Microbiota

by Aikaterini Nelli, Brigkita Venardou, Ioannis Skoufos, Chrysoula (Chrysa) Voidarou, Ilias Lagkouvardos and Athina Tzora

Microorganisms 2023, 11(1), 123; https://doi.org/10.3390/microorganisms11010123 - 03 Jan 2023

Cited by 3 | Viewed by 2207

Abstract

The purpose of this study was to determine for the first time the microbiota in artisanal-type and industrial-type Gidotyri cheeses and investigate the influence of the cheese-making practices on their composition using culture-independent techniques. The microbiota present in artisanal with commercial starters (Artisanal_CS, n = 15), artisanal with in-house starters (Artisanal_IHS, n = 10) and industrial (Ind., n = 9) Gidotyri cheese samples were analyzed using a targeted metagenomic approach (16S rRNA gene). The Ind. Gidotyri cheese microbiota were less complex, dominated by the Streptococcaceae family (91%) that was more abundant compared to the artisanal Gidotyri cheeses (p < 0.05). Artisanal cheeses were more diverse compositionally with specific bacterial species being prevalent to each subtype. Particularly, Loigolactobacillus coryniformis (OTU 175), Secundilactobacillus malefermentans (OTU 48), and Streptococcus parauberis (OTU 50) were more prevalent in Artisanal_IHS cheeses compared to Artisanal_CS (p ≤ 0.001) and Ind. (p < 0.01) Gidotyri cheeses. Carnobacterium maltaromaticum (OTU 23) and Enterobacter hormaechei subsp. hoffmannii (OTU 268) were more prevalent in Artisanal_CS cheeses compared to Artisanal_IHS cheeses (p < 0.05) and Ind. cheeses (p < 0.05). Hafnia alvei (OTU 13) and Acinetobacter colistiniresistens (OTU 111) tended to be more prevalent in Artisanal_CS compared to the other two cheese groups (p < 0.10). In conclusion, higher microbial diversity was observed in the artisanal-type Gidotyri cheeses, with possible bacterial markers specific to each subtype identified with potential application to traceability of the manufacturing processes’ authenticity and cheese quality. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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21 pages, 3596 KiB

Open AccessArticle

Mining Biosynthetic Gene Clusters in Carnobacterium maltaromaticum by Interference Competition Network and Genome Analysis

by Marco Túlio Pardini Gontijo, Nancy E. Ramia, Alexis Dijamentiuk, Annelore Elfassy, Samir Taha, Cécile Mangavel, Anne-Marie Revol-Junelles and Frédéric Borges

Microorganisms 2022, 10(9), 1794; https://doi.org/10.3390/microorganisms10091794 - 06 Sep 2022

Cited by 4 | Viewed by 2207

Abstract

Carnobacterium maltaromaticum is a non-starter lactic acid bacterium (LAB) of interest in the dairy industry for biopreservation. This study investigated the interference competition network and the specialized metabolites biosynthetic gene clusters (BGCs) content in this LAB in order to explore the relationship between the antimicrobial properties and the genome content. Network analysis revealed that the potency of inhibition tended to increase when the inhibition spectrum broadened, but also that several strains exhibited a high potency and narrow spectrum of inhibition. The C. maltaromaticum strains with potent anti-L. monocytogenes were characterized by high potency and a wide intraspecific spectrum. Genome mining of 29 strains revealed the presence of 12 bacteriocin BGCs: four of class I and eight of class II, among which seven belong to class IIa and one to class IIc. Overall, eight bacteriocins and one nonribosomal peptide synthetase and polyketide synthase (NRPS-PKS) BGCs were newly described. The comparison of the antimicrobial properties resulting from the analysis of the network and the BGC genome content allowed us to delineate candidate BGCs responsible for anti-L. monocytogenes and anti-C. maltaromaticum activity. However, it also highlighted that genome analysis is not suitable in the current state of the databases for the prediction of genes involved in the antimicrobial activity of strains with a narrow anti-C. maltaromaticum activity. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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24 pages, 2961 KiB

Open AccessArticle

Dynamics of Starter and Non-Starter Lactic Acid Bacteria Populations in Long-Ripened Cheddar Cheese Using Propidium Monoazide (PMA) Treatment

by Zoha Barzideh, Myra Siddiqi, Hassan Mahmoud Mohamed and Gisèle LaPointe

Microorganisms 2022, 10(8), 1669; https://doi.org/10.3390/microorganisms10081669 - 19 Aug 2022

Cited by 8 | Viewed by 1819

Abstract

The microbial community of industrially produced Canadian Cheddar cheese was examined from curd to ripened cheese at 30–32 months using a combination of viable plate counts of SLAB (GM17) and NSLAB (MRSv), qPCR and 16S rRNA gene amplicon sequencing. Cell treatment with propidium monoazide excluded DNA of permeable cells from amplification. The proportion of permeable cells of both Lactococcus spp. and Lacticaseibacillus spp. was highest at 3–6 months. While most remaining Lacticaseibacillus spp. cells were intact during later ripening stages, a consistent population of permeable Lactococcus spp. cells was maintained over the 32-month period. While Lactococcus sequence variants were significant biomarkers for viable cheese curd communities at 0–1 m, Lacticaseibacillus was identified as a distinctive biomarker for cheeses from 7 to 20 months. From 24 to 32 months, Lacticaseibacillus was replaced in significance by four genera (Pediococcus and Latilactobacillus at 24 m and at 30–32 m, Secundilactobacillus and Paucilactobacillus). These results underscore the importance of monitoring potential defects in cheeses aged over 24 months, which could be diagnosed early through microbial DNA profiling to minimize potential waste of product. Future perspectives include correlating volatile flavor compounds with microbial community composition as well as the investigation of intra-species diversity. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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15 pages, 2887 KiB

Open AccessArticle

Analysis of Microbiota Persistence in Quebec’s Terroir Cheese Using a Metabarcoding Approach

by Annick Raymond-Fleury, Marie-Hélène Lessard, Julien Chamberland, Yves Pouliot, Eric Dugat-Bony, Sylvie L. Turgeon, Daniel St-Gelais and Steve Labrie

Microorganisms 2022, 10(7), 1381; https://doi.org/10.3390/microorganisms10071381 - 09 Jul 2022

Cited by 2 | Viewed by 2059

Abstract

Environmental short amplicon sequencing, or metabarcoding, is commonly used to characterize the bacterial and fungal microbiota of cheese. Comparisons between different metabarcoding studies are complicated by the use of different gene markers. Here, we systematically compare different metabarcoding molecular targets using V3–V4 and V6–V8 regions of the bacterial 16S rDNA and fungal ITS1 and ITS2 regions. Taxonomic profiles varied depending on the molecular markers used. Based on data quality and detection capacity of the markers toward microorganisms usually associated with the dairy environment, the ribosomal regions V3–V4 and ITS2 were selected and further used to evaluate variability in the microbial ecosystem of terroir cheeses from the province of Quebec in Canada. Both fungal and bacterial ecosystem profiles were described for 32 different ready-to-eat bloomy-, washed- and natural-rind specialty cheese varieties. Among them, 15 were studied over two different production years. Using the Bray–Curtis dissimilarity index as an indicator of microbial shifts, we found that most variations could be explained by either a voluntary change in starter or ripening culture composition, or by changes in the cheesemaking technology. Overall, our results suggest the persistence of the microbiota between the two years studied—these data aid understanding of cheese microbiota composition and persistence during cheese ripening. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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15 pages, 3249 KiB

Open AccessArticle

Integration of Multiomic Data to Characterize the Influence of Milk Fat Composition on Cantal-Type Cheese Microbiota

by Marie Frétin, Amaury Gérard, Anne Ferlay, Bruno Martin, Solange Buchin, Sébastien Theil, Etienne Rifa, Valentin Loux, Olivier Rué, Christophe Chassard and Céline Delbès

Microorganisms 2022, 10(2), 334; https://doi.org/10.3390/microorganisms10020334 - 01 Feb 2022

Viewed by 2431

Abstract

A previous study identified differences in rind aspects between Cantal-type cheeses manufactured from the same skimmed milk, supplemented with cream derived either from pasture-raised cows (P) or from cows fed with maize silage (M). Using an integrated analysis of multiomic data, the present study aimed at investigating potential correlations between cream origin and metagenomic, lipidomic and volatolomic profiles of these Cantal cheeses. Fungal and bacterial communities of cheese cores and rinds were characterized using DNA metabarcoding at different ripening times. Lipidome and volatolome were obtained from the previous study at the end of ripening. Rind microbial communities, especially fungal communities, were influenced by cream origin. Among bacteria, Brachybacterium were more abundant in P-derived cheeses than in M-derived cheeses after 90 and 150 days of ripening. Sporendonema casei, a yeast added as a ripening starter during Cantal manufacture, which contributes to rind typical aspect, had a lower relative abundance in P-derived cheeses after 150 days of ripening. Relative abundance of this fungus was highly negatively correlated with concentrations of C18 polyunsaturated fatty acids and to concentrations of particular volatile organic compounds, including 1-pentanol and 3-methyl-2-pentanol. Overall, these results evidenced original interactions between milk fat composition and the development of fungal communities in cheeses. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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18 pages, 4222 KiB

Open AccessArticle

Characterization of Bacterial Microbiota of P.D.O. Feta Cheese by 16S Metagenomic Analysis

by Panagiotis Papadakis, Spyros Konteles, Anthimia Batrinou, Sotiris Ouzounis, Theofania Tsironi, Panagiotis Halvatsiotis, Efstathia Tsakali, Jan F. M. Van Impe, Despina Vougiouklaki, Irini F. Strati and Dimitra Houhoula

Microorganisms 2021, 9(11), 2377; https://doi.org/10.3390/microorganisms9112377 - 17 Nov 2021

Cited by 15 | Viewed by 2771

Abstract

Background: The identification of bacterial species in fermented PDO (protected designation of origin) cheese is important since they contribute significantly to the final organoleptic properties, the ripening process, the shelf life, the safety and the overall quality of cheese. Methods: Ten commercial PDO feta cheeses from two geographic regions of Greece, Epirus and Thessaly, were analyzed by 16S metagenomic analysis. Results: The biodiversity of all the tested feta cheese samples consisted of five phyla, 17 families, 38 genera and 59 bacterial species. The dominant phylum identified was Firmicutes (49% of the species), followed by Proteobacteria (39% of the species), Bacteroidetes (7% of the species), Actinobacteria (4% of the species) and Tenericutes (1% of the species). Streptococcaceae and Lactobacillaceae were the most abundant families, in which starter cultures of lactic acid bacteria (LAB) belonged, but also 21 nonstarter lactic acid bacteria (NSLAB) were identified. Both geographical areas showed a distinctive microbiota fingerprint, which was ultimately overlapped by the application of starter cultures. In the rare biosphere of the feta cheese, Zobellella taiwanensis and Vibrio diazotrophicus, two Gram-negative bacteria which were not previously reported in dairy samples, were identified. Conclusions: The application of high-throughput DNA sequencing may provide a detailed microbial profile of commercial feta cheese produced with pasteurized milk. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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17 pages, 1154 KiB

Open AccessArticle

Lactic Starter Dose Shapes S. aureus and STEC O26:H11 Growth, and Bacterial Community Patterns in Raw Milk Uncooked Pressed Cheeses

by Justine Piqueras, Christophe Chassard, Cécile Callon, Etienne Rifa, Sébastien Theil, Annick Lebecque and Céline Delbès

Microorganisms 2021, 9(5), 1081; https://doi.org/10.3390/microorganisms9051081 - 18 May 2021

Cited by 4 | Viewed by 2904

Abstract

Adding massive amounts of lactic starters to raw milk to manage the sanitary risk in the cheese-making process could be detrimental to microbial diversity. Adjusting the amount of the lactic starter used could be a key to manage these adverse impacts. In uncooked pressed cheeses, we investigated the impacts of varying the doses of a lactic starter (the recommended one, 1×, a 0.1× lower and a 2× higher) on acidification, growth of Staphylococcus aureus SA15 and Shiga-toxin-producing Escherichia coli (STEC) O26:H11 F43368, as well as on the bacterial community patterns. We observed a delayed acidification and an increase in the levels of pathogens with the 0.1× dose. This dose was associated with increased richness and evenness of cheese bacterial community and higher relative abundance of potential opportunistic bacteria or desirable species involved in cheese production. No effect of the increased lactic starter dose was observed. Given that sanitary criteria were paramount to our study, the increase in the pathogen levels observed at the 0.1× dose justified proscribing such a reduction in the tested cheese-making process. Despite this, the effects of adjusting the lactic starter dose on the balance of microbial populations of potential interest for cheese production deserve an in-depth evaluation. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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Review

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19 pages, 2007 KiB

Open AccessReview

Buffalo Milk as a Source of Probiotic Functional Products

by Márcio Vargas-Ramella, Mirian Pateiro, Aristide Maggiolino, Michele Faccia, Daniel Franco, Pasquale De Palo and José M. Lorenzo

Microorganisms 2021, 9(11), 2303; https://doi.org/10.3390/microorganisms9112303 - 05 Nov 2021

Cited by 15 | Viewed by 5657

Abstract

In the past two decades, consumption of food has been accruing due to its health claims which include gastrointestinal health, improved immunity, and well-being. Currently, the dairy industry is the sector where probiotics are most widely used, especially in fermented milk, cheese, yoghurt, butter, and dairy beverages. Although, it is still necessary to face many challenges regarding their stability and functionality in food. Considering the increasing demand for healthy products, it is necessary to develop strategies that aim to increase the consumption of functional foods in order to meet probiotic usefulness criteria and the consumer market. This review aimed to promote the utilization of buffalo milk considering its probiotic effects as a functional food and natural remedy to various ailments, emphasizing the potential of innovation and the importance of milk-based products as health promoters. The intake of probiotics plays an important role in modulating the health of the host, as a result of a balanced intestinal microbiota, reducing the risk of development of various diseases such as cancer, colitis, lactose intolerance, heart diseases, and obesity, among other disorders. However, further studies should be carried out to deepen the knowledge on the relationship between raw buffalo milk, its dairy products microbiota and consumer’s health beneficial effects, as well as to implement a strategy to increase the variety and availability of its products as a functional food in the market. Full article

(This article belongs to the Special Issue Microbial Ecology of Dairy Products: From Diversity to Functions)

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