Available online at www.sciencedirect.

com

ScienceDirect

Novel insights into the microbiology of fermented dairy

foods
Guerrino Macori1,2 and Paul D Cotter1,2

Fermentation is a traditional approach to food preservation fresh substrate [2]. In the last century, and coinciding with
that, in addition to improving food safety, also confers the large scale, commercial production of fermented
enhanced organoleptic, nutritional, and health-promoting foods, came the use of starter and adjunct culture(s).
attributes upon those foods.Dairy products can be fermented More recently, the health benefits of many fermented
by a diverse microbiota. The accompanying microbes can be dairy products have been the subject of intense investi-
studied using a variety of different, including ‘omics’-based, gation. Some examples include specific studies demon-
approaches that can reveal their composition and strating the impact of kefir consumption on bone mineral
functionality. These methods have increasingly been recently density and bone metabolism [3], evidence of a reduced
applied to study fermented dairy foods from the perspective risk of type 2 diabetes associated with yogurt consump-
of genetic diversity, functionality and succession. The insights tion [4,5] and investigations revealing that a fermented
provided by these studies are summarised in this review. milk product containing a variety of microorganisms
affects the activity of brain regions that control emotion
Addresses and sensation [6]. These and other health-promoting
1
Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland features, combined with a view of fermented foods as
2
APC Microbiome Institute, Cork, Ireland ‘natural’ has further increased the popularity of fermen-
ted dairy foods [7] such as yogurts, fermented or cultured
Corresponding author: Cotter, Paul D (paul.cotter@teagasc.ie)
milks, kefir, acidophilus milk, koumiss, curd, buttermilk
and cheeses. These are produced by the fermentation
Current Opinion in Biotechnology 2018, 49:172–178 of different types of milk by specific microorganisms
This review comes from a themed issue on Food biotechnology or complex microbial communities. This review will
describe recent developments relating to the best known
Edited by Maria Marco and Eddy Smid
dairy fermented foods and the microorganisms that con-
tribute to their fermentation.

http://dx.doi.org/10.1016/j.copbio.2017.09.002 Yogurt and cheeses

0958-1669/ã 2017 Elsevier Ltd. All rights reserved. Protosymbiotic cultures of Streptococcus salivarius subsp.
thermophilus (Str. thermophilus) and Lactobacillus delbrueckii
subsp. bulgaricus (Lb. bulgaricus) are typically used to
convert milk into yogurt. The strains involved have been
exposed to a natural selection pressure imposed during
yogurt production that, in the case of Lb. bulgaricus,
Introduction contributed to the genetic evolution of ancestral strains
Fermented foods are generally defined as those foods or with intermediate acetaldehyde-producing capabilities
beverages made through controlled microbial growth and [8]. As was demonstrated in a recent study of lactic acid
enzymatic conversions of major and minor food compo- bacteria isolated from a range of traditional Greek dairy
nents [1]. The fermentation of foods involves the products, such products can also be a valuable source
breaking down of complex constituents into simpler ones, of novel strains with different health-promoting proper-
many of which can possess bioactive properties, through ties [9].
the use of microorganisms. Nutritional and functional
properties are enhanced through the fermentation pro- Cheese is the most popular fermented milk product. Both
cess. These include the improved availability of trace soft and hard cheeses are produced by culturing milk for a
minerals, vitamins and anti-oxidants as well as greater period of time. Certain types of cheeses can be made
safety, shelf-life and sensory attributes. Human cultures simply by straining the moisture out of sour cream or
across the globe have been consuming fermented dairy yogurt, while others require additional steps in the cul-
products for millennia, exploiting the biochemical action turing and fermentation process. Large scale production
of microorganisms naturally present in the raw milk, of cheeses relies on the use of commercial starter culture
microorganisms that are in the surface of containers in (s), and the addition of adjunct cultures. Adjuncts can
which the dairy foods are placed or through a process impart specific flavours [10] or may be probiotic candi-
known as back-slopping, whereby some of the material dates that are being delivered within the cheese [11],
from a previous fermentation is employed to inoculate thereby opening new opportunities for the design of dairy

Current Opinion in Biotechnology 2018, 49:172–178 www.sciencedirect.com

 Novel insights into the microbiology of fermented dairy foods Macori and Cotter 173

fermented foods for target populations. The combined as alleviating lactose maldigestion, than on the basis of
probiotic properties of lactic acid and propionic acid flavour [23].
bacteria were employed by Plé and colleagues who devel-
oped a pressed cheese containing Propionibacterium freu- Specific milks (e.g. yak, cow and mares’ milk) are used for
denreichii and Lactobacillus delbrueckii strains previously the production of some fermented dairy drinks. This,
selected for their anti-inflammatory properties [12]. Stud- together with environmental factors, starter and adjunct
ies of the microbiology of cheese have been revolutio- cultures and fermentation parameters (duration, temper-
nised recently through in-depth functional genomic and ature and storage vessel) shape the microbial diversity of
metagenomic studies, which have demonstrated the naturally fermented milks [24]. In the case of koumiss,
microbial diversity of a vast variety of cheeses. These mare’s milk is fermented in containers made of animal
studies are of great value from an applied perspective and skin or wooden casks. Fermentation occurs naturally at
have further highlighted the fact that microbial commu- ambient temperature after the addition of filtered mare
nities are rich and diverse in cheeses and are critical to the milk into a container containing old koumiss, which
typical organoleptic characteristics of traditional products serves as the starter culture [25]. Shubat or Chal is a
[13,14]. Such analyses can also contribute to the selection traditional fermented camel’s milk that is generated
of new strains as starter cultures for the dairy industry through the action of Lb. helveticus and Str. thermophilus,
[15]. In addition, these investigations have also high- resulting in a beverage with hypotensive effects [26].
lighted that cheese can provide valuable model systems Camel’s milk is also used for the production of Gariss,
for microbial ecology studies [16,17], including the shaping a traditional Sudanese raw fermented dairy product [27].
of microbial communities through horizontal gene
transfer [18]. Buttermilk was originally produced as a by-product of
butter making and contains protein, phospholipids, fat,
Fermented milks lactose, and minerals. Lactococcus lactis subsp. cremoris
Fermented milk is produced through the coagulation of (Lc. lactis subsp. cremoris) or Lc. lactis subsp. lactis biovar.
milk, without the elimination of serum, by bacterial diacetylactis (Lc. lactis diacetylactis) (Table 1) are typically
cultures that generally remain present until consumption. responsible for this fermentation and the production
There are three categories of fermented milks: Thermo- process includes a heat treatment of the milk to 95  C
philic sour-milks (e.g. Matzoon), where the fermentation followed by a cooling phase to 20–25  C before the
is conducted at 42–45  C with lactic acid production; addition of the starter culture. Starter is added at 1–2%
Mesophilic sour-milks (e.g. Cultured buttermilk, Viili, and the fermentation is allowed to proceed for 16–20 h
Ymer, Skyr), where the fermentation is conducted at [6]. The milk fat globule membranes (MFGMs) found in
20–30  C with lactic acid production; and acid and alco- buttermilk is rich in unique bioactive proteins [28] and is
holic milks (i.e. Kefir, Gioddu), where the fermentation is the major protein-containing constituent of this fermen-
conducted at 15–25  C with the production of some ted product. Other buttermilk-based fermentations are
alcohol in addition to lactic acid and carbon dioxide combined with plants and fruits, as in the case of Oma-
(Table 1). shikwa, a Namibian artisanal product made from tree
roots (Boscia albitrunca) added to the fermented butter-
Many drinkable fermented milk products are produced milk. This product is dominated by Lb. fermentum and
by the addition of water to yoghurt or by the addition of Kluyveromyces marxianus [27].
cultures of Str. thermophilus and Lb. bulgaricus to standard-
ized milk for fermentation at room temperature. How- Starter cultures, adjuncts and complex
ever, efforts continue to commercialise other such fer- fermenting communities
mented milks. Indeed the traditional Turkish fermented- In addition to producing acid for preservation purposes,
milk drink, Ayran, and a spontaneously fermented starter cultures, which include a variety of bacteria, yeasts
yoghurt-like product made in Ghana and other parts of and moulds, allow for a more controlled and predictable
West Africa, Nunu, have recently been studied in order to fermentation in terms of sensory-related features, appear-
improve quality and shelf-life stability to, ultimately, ance and other physical and chemical characteristics.
facilitate commercialisation [19,20]. In the case of Ayran, Starter cultures consist of one or more (referred to as a
in addition to Str. thermophilus and Lb. bulgaricus, this co-culture or mixed culture) fermenting species [29].
fermented milk contains Lb. helveticus, Lb. fermentum and Undefined starter cultures also continue to be relevant
Lb. paracasei. These additional cultures allow fast acidifi- in traditional dairy foods fermentation and consist of
cation and extensive proteolysis [21]. Acidophilus milk is complex uncharacterized microbial community, which
a traditional milk fermented with Lb. acidophilus in pas- can be revealed with high-throughput DNA sequencing
teurised-standardized milk [22]. The milk is inoculated technologies and predictive metabolic modelling [30].
and incubated at 37  C for 18–20 h and, because of its During the growth of dairy starter bacteria, which are
strong acid taste, its consumption is more typically asso- typically Lactic Acid Bacteria (LAB), in milk, the initial
ciated with a desire to address health-related issues, such metabolism of lactose results in the formation of glucose

www.sciencedirect.com Current Opinion in Biotechnology 2018, 49:172–178

174 Food biotechnology

Table 1

Traditional fermented dairy products along with the particular associated microorganisms

Product Name Origin of milk (principal kind Type of starter Some associated
or mostly utilized) microorganisms involved in
fermentation
Cheese Any variety of Any kind of milk (buffalo, Traditional and commercial Various including Lactococcus
cheeses camel, cow, goats, mare, lactis (Lc. lactis), Lactococcus
sheep) spp., Lactobacillus spp.,
Streptococcus spp.
Fermented milk Ayran Cow Traditional and commercial Lactobacillus delbrueckii
Thermophilic sour-milks subsp. bulgaricus (Lb.
bulgaricus) and Streptococcus
salivarius subsp. thermophiles
(Str. thermophilus)
Matzoon Cow Back-slopping (culture from Lb. bulgaricus and
previous productions) Str. thermophilus
Fermented milk Cultured buttermilk Boiled cows or goats milk Traditional and commercial Lc. lactis subsp. cremoris
Mesophilic sour-milks Lc. lactis subsp. lactis biovar.
diacetylactis (Lc. diacetylactis)
Nunu Traditional and commercial Lb. fermentum, Lb. plantarum,
Lb. helveticus, Leuconostoc
mesenteroides (Leuc.
mesenteroides)
Skyr Skimmed sheep and cow Traditional Str. thermophilus and Lb.
milk bulgaricus
Viili Cow Back-slopping (culture from Lc. lactis subsp. cremoris,
previous productions) Lc. diacetylactis, Leuc.
mesenteroides subsp.
cremoris Geotrichum
candidum Kluveromyces
marxianus, Pichia fermentans
Ymer Skimmed cow milk Traditional Lc. lactis
Gioddu Cow, goat, sheep and mixed Back-slopping (culture from Str. thermophilus, Lb.
milks previous productions, called bulgaricus
‘madrighe’) Lc. casei subsp. casei,
Leuc. mesenteroides subsp.
mesenteroides
Fermented milk Kefir Any kind of milk (buffalo, Back-slopping (‘grains’) Lb. acidophilus,
Acid and alcoholic milks camel, cow, goats, sheep) Bifidobacterium bifidum Str.
and mixed milks thermophilus, Lb. bulgaricus
Lb. helveticus, Lb.
kefiranofaciens, Lc. lactis,
Leuconostoc spp
K. marxianus, Micrococci,
K. lactis Saccharomyces kefir,
S. cerevisiae, Torula kefir
Yogurt Traditional yogurt Cow Traditional and commercial Str. thermophilus and Lb.
bulgaricus
Lb. helveticus, Lb. fermentum
and Lb. paracasei
Acidophilus milk Acidophilus milk Cow Traditional Lb. acidophilus
Koumiss Mare Back-slopping (container of Enterococcus faecalis,
previous productions) E.faecium
Shubat or Chal Camel Traditional Lb. paracasei, Lb. helveticus
and Str. thermophilus
Gariss Camel Back-slopping (container of K. marxianus,
previous productions) Candida kefyr
Pichia kudriavzevii
Str. infantarius subsp.
infantarius, Lb. fermentum

Lc., Lactococcus; Str., Streptococcus; Lb., Lactobacillus; Leuc., Leuconostoc; K., Kluveromyces; E., Enterococcus.

Current Opinion in Biotechnology 2018, 49:172–178 www.sciencedirect.com

 Novel insights into the microbiology of fermented dairy foods Macori and Cotter 175

Figure 1

(a) (b)
Homofermentative LAB Fermented milks
Lb. acidophilus, Acid and Mesophilic Thermophilic
Lb. delbrueckii, Lb. helveticus, Lb. salivarius, Homolactic alcoholic milks sour-milks sour-milks
Lb. gasseri fermentation Lactic acid
OH OH OH
Other: O HO OH
O
Lc. lactis subsp. lactis biovar diacetylactis HO O

Enterococcus,
Lactose OH
OH

Streptococcus and Pediococcus spp.

Cultured buttermilk,
Facultatively heterofermentative LAB kefir, Gioddu
Viili, Ymer, Skyr
Matzoon
Lb. casei, Lb. curvatus,
Lb. plantarum, Lb. sakei Acidophilus milk Cultured
Cheeses
and yogurt buttermilk
Other: Lactosse -> Glucose + Galactose
Pediococcus pentosaceus, P. acidilactici,
P. claussenii

Obligately heterofermentative LAB: Heterolactic Lactic acid, CO2

Lb. brevis, Lb. buchneri, fermentation Ethanol
Lb. fermentum, Lb. reuteri
Other:
Leuconostoc, Oenococcus, Weissella

Current Opinion in Biotechnology

Overview of types of fermented dairy products and biochemical fermentation involved. (a) Among the genera involved in dairy fermentations,
Lactobacillus are most heterogeneous in terms of the type of fermentation that are carried out. These and other microbes, including a variety of
LAB, determine the flavours, textures and other features of fermented foods. Homolactic fermentations result in the production of lactic acid as
the primary by-product from glucose fermentation. Heterolactic fermentations result in the production of carbon dioxide and other by-products. (b)
In the right side of the figure are reported examples of fermented dairy products.

and galactose. The next step of the metabolic process continue to be investigated in ever greater depth, includ-
varies according to the species present and results in ing through molecular analysis of indigenous fungal iso-
different final products depending on whether a homo- lates from cheeses that could be harnessed to improve
lactic or heterolactic fermentation occurs (Figure 1). sensory qualities of such cheeses in a controlled way [35].
Adjunct cultures are used to provide or enhance the As for bacteria, individual fungal strains have been the
characteristic flavours and textures of dairy fermented focus of increasingly in-depth investigations. Indeed, the
products. These may be homofermentative, and include diversity of isolates of Penicillum roqueforti strains, impor-
other Streptococcus spp., Enterococcus, Pediococcus and Aero- tant due to their production of a wide range of flavour
coccus genera. Alternatively, they may be heterofermen- compounds to influence the flavour profiles of blue-
tative that is ferment glucose with lactic acid, ethanol/ cheese varieties has recently been highlighted [36].
acetic acid and carbon dioxide as end products. Repre-
sentative heterofermenters include Leuconostoc spp., Fermented dairy products can be produced by the action
Lb. brevis, Lb. fermentum, and Lb. reuteri. Other Lactobacil- of complex fermenting microbial communities. These
lus species are considered ‘facultatively’ heterofermenta- cultures can come from the reuse of a fraction of the
tive, meaning they will produce carbon dioxide and other previous production, can be liquid or solid (grains) and are
by-products only under certain conditions or from specific often comprised of a specific and complex mixture of
substrates [31,32]. Genomics has continued to provide bacteria and yeasts that live in a symbiotic association
insights into these and other species involved in fermen- [37]. An example of the latter is kefir, a beverage with
tation. One recent genomics-based investigation has reported health benefits containing, in some instances,
revealed considerable variability among the genomes over 50 species of lactic acid bacteria and yeast. Studies
of Leuconostoc cultures commonly used by the dairy indus- with animal models have suggested that the consumption
try [33]. of kefir can modulate the gut microbiota, with associated
beneficial health impacts including anti-allergenic and
Many fermented dairy foods are produced by the com- anti-carcinogenic effects and the prevention of patholo-
bined actions of LAB and fungi. Saccharomyces, Kluyver- gies like obesity [38,39,40]. In contrast to the solid kefir
omyces, Zygosaccharomyces, Aspergillus, Geotrichum, Penicil- ‘grains’, koumiss is, as noted above, a mare’s milk fer-
lium and Rhizopus genera are the fungi used most often in mented drink. It is produced from a liquid starter culture
dairy fermentations and contribute to the texture and that contains an uncharacterized microbial community
appearance of products [34]. These contributions and, due to the high sugar content of the raw mare’s milk,

www.sciencedirect.com Current Opinion in Biotechnology 2018, 49:172–178

176 Food biotechnology

the fermentation yields a higher, though still mild, alcohol Conclusion

content compared to kefir [39]. Several strains of interest The combined use of culture-dependent and culture-
were isolated recently from koumiss, and have been independent approaches have provided novel insights
characterized as potential bacteriocin producing probio- into the complexity and benefits of microbes present in
tics, with immune-modulating properties. These and fermented dairy products. The continued application of
other strains have the potential to provide the basis for these technologies promises to lead to the discovery of
the development of new functional foods or to be beneficial attributes within these microbes that have
employed as therapeutic adjuvants for inflammatory dis- previously been overlooked, improve flavour, safety,
eases [41–43]. and quality and allow the health promoting properties
of these foods to be maximized.
Future studies of the microbiome of
fermented foods Conflict of interest
Traditionally culture-dependent methodologies have No conflict of interest.
been employed to determine the microbial composition
of dairy fermented foods that is, the use of selective and References and recommended reading
differential growth media [44]. Despite ongoing Papers of particular interest, published within the period of review,
improvements to culture-based systems, through cultiva- have been highlighted as:
tion in situ or by using specific growth factors [45], these  of special interest
approaches are limited by the fact that not all microbes  of outstanding interest
are easily cultured in the laboratory [46] and there is no
1. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligne B,
one culture medium that allows the simultaneous growth  Ganzle M, Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R: Health
of all microbes present. Culture-independent techniques benefits of fermented foods: microbiota and beyond. Curr Opin
Biotechnol 2017, 44:94-102.
present the extraordinary alternative to access the genetic This is an impressive review supporting the advantages of fermented
information contained within the vast number of species foods. It is largely focused on their benefits, examining the recent human
in fermented products [47]. These techniques are mostly studies involving fermented foods and the probiotic features of micro-
organisms responsible for fermentation.
based on the analysis of microbial nucleic acid sequences
2. Zannini E, Waters DM, Coffey A, Arendt EK: Production,
and their comparison with sequence data held in data- properties, and industrial food application of lactic acid
bases to provide information regarding the identity of the bacteria-derived exopolysaccharides. Appl Microbiol
microorganisms present and their functional potential. Biotechnol 2016, 100:1121-1135.

DNA sequencing coupled with bioinformatics for the 3. Tu M-Y, Chen H-L, Tung Y-T, Kao C-C, Hu F-C, Chen C-M: Short-
Term wffects of kefir-fermented milk consumption on bone
accurate and rapid identification of microorganisms at mineral density and bone metabolism in a randomized clinical
strain level, as well as the provision of an ever greater trial of osteoporotic patients. PLOS ONE 2015, 10:1-17.
insight into their functional potential, is an exciting 4. Dı́az-López A, Bulló M, Martı́nez-González, Corella D, Estruch R,
prospect and, in one recent proof of concept study, whole Fitó M, Gómez-Gracia E, Fiol M, de la Corte FJG, Ros E et al.: Dairy
product consumption and risk of type 2 diabetes in an elderly
metagenome shotgun sequencing was used to detect Spanish Mediterranean population at high cardiovascular risk.
pathogens and virulence factors in the fermented dairy Eur J Nutr 2016, 55:349-360.
food, nunu [48]. It is expected to be just a matter of time 5. Chen M, Sun Q, Giovannucci E, Mozaffarian D, Manson JE,
before metatranscriptomics [49] is also employed exten- Willett WC, Hu FB: Dairy consumption and risk of type
2 diabetes: 3 cohorts of US adults and an updated
sively to study levels of gene expression among microbial meta-analysis. BMC Med 2014, 12:1-14.
populations in fermented dairy products.
6. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B,
Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, Mayer EA:
The information gained through the aforementioned Consumption of fermented milk product with
probiotic modulates brain activity. Gastroenterology 2013,
approaches can in turn be combined with other 144:1394-1401.
‘Omics’-based approaches, such as proteomics and 7. Vijaya KB, Vijayendra SVN, Reddy OVS: Trends in dairy and non-
metabolomics, to provide a detailed insight into the dairy probiotic products – a review. J Food Sci Technol 2015,
microbiology of the food and its relationship with 52:6112-6124.
flavour, aroma and a variety of other characteristics. 8. Liu W, Yu J, Sun Z, Song Y, Wang X, Wang H, Wuren T, Zha M,
These approaches were recently applied to study Menghe B, Heping Z: Relationships between functional genes
in Lactobacillus delbrueckii ssp. bulgaricus isolates and
microbial succession, flavour production, core meta- phenotypic characteristics associated with fermentation time
bolic pathways and microbiome-specific functionality and flavor production in yogurt elucidated using multilocus
sequence typing. J Dairy Sci 2016, 99:89-103.
in fermented dairy products from a variety of location
[50,51,52]. Other promising new approaches include 9. Zoumpopoulou G, Tzouvanou A, Mavrogonatou E, Alexandraki V,
Georgalaki M, Anastasiou R, Papadelli M, Manolopoulou E,
single-cell amplification techniques for analysing the Kazou M, Kletsas D, Papadimitriou K, Tsakalidouet E: Probiotic
microbiota, that in the future will highlight rare species features of lactic acid bacteria isolated from a diverse pool
of traditional Greek dairy products regarding specific strain–
in fermented foods that are of biotechnological interest host interactions. Probiotics Antimicrob Proteins 2017, 1:1-10.
and can be used to monitor changes in dairy food 10. Centeno JA, Garabal JI, Docampo F, Lorenzo JM, Carballo J:
microbiomes [25–39,40,41–43,44,45–50,51,52,53]. Recovering traditional raw-milk tetilla cheese flavour and

Current Opinion in Biotechnology 2018, 49:172–178 www.sciencedirect.com

 Novel insights into the microbiology of fermented dairy foods Macori and Cotter 177

sensory attributes by using Kocuria varians and Yarrowia commercial lactase tablet in alleviating lactose maldigestion.
lipolytica adjunct cultures. Int J Food Microbiol 2017, 251:33-40. Am J Clin Nutr 1989, 49:1233-1237.

11. Pino A, Van Hoorde K, Pitino I, Russo N, Carpino S, Caggia C, 24. Zhong Z, Hou Q, Kwok L, Yu Z, Zheng Y, Sun Z, Menghe B,
 Randazzo CL: Survival of potential probiotic lactobacilli used  Zhang H: Bacterial microbiota compositions of naturally
as adjunct cultures on Pecorino Siciliano cheese ripening and fermented milk are shaped by both geographic origin and
passage through the gastrointestinal tract of healthy sample type. J Dairy Sci 2016, 99:7832-7841.
volunteers. Int J Food Microbiol 2017, 252:42-52. The authors present a novel study comparing the microbiota of a large
In this study, two potentially probiotic strains, Lactobacillus rhamnosus collection of traditional and artisanal products, including 55 yogurts,
(H25) and Lactobacillus paracasei (N24), were added to Pecorino Siciliano 18 yak milks, 6 koumisses, and 6 cheeses. The results suggest a dis-
cheese production. This cheese was used as matrix for the delivery of the tinction between the cheese microbiome and the other sample types,
probiotics that were initially selected for their ability to survive passage characterized by the existence of a much higher proportions of Lacto-
through the gastrointestinal tract and for their antimicrobial activity coccus and Streptococcus. Besides sample type, the study highlighted
against pathogens. the significant impact of geographical origin in determining the microbial
biodiversity.
12. Plé C, Breton J, Richoux R, Nurdin M, Deutsch SM, Falentin H,
Hervé C, Chuat V, Lemée R, Maguin E et al.: Combining selected 25. Gesudu Q, Zheng Y, Xi X, Hou QC, Xu H, Huang W, Zhang H,
immunomodulatory Propionibacterium freudenreichii and Menghe B, Liu W: Investigating bacterial population structure
Lactobacillus delbrueckii strains: reverse engineering and dynamics in traditional koumiss from Inner Mongolia
development of an anti-inflammatory cheese. Mol Nutr Food using single molecule real-time sequencing. J Dairy Sci 2016,
Res 2016, 60:935-948. 99:7852-7863.

13. Jans C, Meile L, Kaindi DWM, Kogi-Makau W, Lamuka P, 26. Yahya MA, Alhaj OA, Al-Khalifah AS: Antihypertensive effect of
Renault P, Kreikemeyer B, Lacroix C, Hattendorf J, Zinsstag J, fermented skim camel (Camelus dromedarius) milk on
Schelling E, Fokou G, Bonfoh B: African fermented dairy spontaneously hypertensive rats. Nutr Hosp 2017, 34:416-421.
products – overview of predominant technologically important
microorganisms focusing on African Streptococcus 27. Jans C, Meile L, Kaindi DWM, Kogi-Makau W, Lamuka P,
infantarius variants and potential future applications for Renault P, Kreikemeyer B, Lacroix C, Hattendorf J, Zinsstag J,
enhanced food safety and security. Int J Food Microbiol 2017, Schelling E, Fokou G, Bonfoh B: African fermented dairy
250:27-36. products – overview of predominant technologically important
microorganisms focusing on African Streptococcus
14. Carafa I, Nardin T, Larcher R, Viola R, Tuohy K, Franciosi E: infantarius variants and potential future applications for
Identification and characterization of wild lactobacilli and enhanced food safety and security. Int J Food Microbiol 2017,
pediococci from spontaneously fermented Mountain Cheese. 250:27-36.
Food Microbiol 2015, 48:123-132.
28. Conway V, Couture P, Gauthier S, Pouliot Y, Lamarche B,
15. Centi V, Matteucci F, Lepidi A, Del Gallo M, Ercole C: Kengne A-P et al.: Effect of buttermilk consumption on blood
Microbiological and biochemical aspects of inland Pecorino pressure in moderately hypercholesterolemic men and
Abruzzese cheese. Heliyon 2017, 3:1-26. women. Nutrition 2014, 30:116-119.

16. Wolfe BE, Button JE, Santarelli M, Dutton RJ: Cheese rind 29. Hill D, Sugrue I, Arendt E, Hill C, Stanton C, Ross RP: Recent
communities provide tractable systems for in situ and in vitro advances in microbial fermentation for dairy and health.
studies of microbial diversity. Cell 2014, 158:422-433. F1000Research 2017, 6:751.
17. Dugat-Bony E, Garnier L, Denonfoux J, Ferreira S, Sarthou AS, 30. Smid EJ, Erkus O, Spus M, Wolkers-Rooijackers JC, Alexeeva S,
Bonnarme P, Irlinger F: Highlighting the microbial diversity Kleerebezem M: Functional implications of the microbial
of 12 French cheese varieties. Int J Food Microbiol 2016, community structure of undefined mesophilic starter cultures.
238:265-273. Microb Cell Fact 2014, 13:1-9.

18. Bonham KS, Wolfe BE, Dutton RJ: Extensive horizontal gene 31. Hutkins RW: Starter cultures. In Microbiology and Technology of
transfer in cheese-associated bacteria. Elife 2017, 6:1-31. Fermented Foods. Edited by Hutkins RW. Blackwell Publishing;
2007:67-106.
19. Altay F, Karbancioglu-Güler F, Daskaya-Dikmen C, Heperkan D:
A review on traditional Turkish fermented non-alcoholic 32. Cousin FJ, Louesdon S, Maillard MB, Parayre S, Falentin H,
beverages: microbiota, fermentation process and quality Deutsch SM, Boudry G, Jan G: The first dairy product
characteristics. Int J Food Microbiol 2013, 167:44-56. exclusively fermented by Propionibacterium freudenreichii: a
new vector to study probiotic potentialities in vivo. Food
20. Walsh AM, Crispie F, Kilcawley K, O’Sullivan O, O’Sullivan MG, Microbiol 2012, 32:135-146.
 Claesson MJ, Cotter PD: Microbial succession and flavor
production in the fermented dairy beverage kefir. mSystems 33. Frantzen CA, Kot W, Pedersen TB, Ardö YM, Broadbent JR,
2016:1. Vogensen FK, Holo H: Genomic characterization of dairy
In this paper, the authors investigate the changes in the microbial associated Leuconostoc species and diversity of
population of kefir over the course of 24-h. This data is combined with Leuconostocs in undefined mixed mesophilic starter cultures.
volatile-compound profiling and sensory analysis to reveal a number of Front Microbiol 2017, 8:1-14.
correlations before being used to alter flavour in a targeted way. Micro-
biome analysis also highlights genes that likely contribute to kefir’s 34. Guzzon R, Carafa I, Tuohy K, Cervantes G, Vernetti L, Barmaz A,
health-associated attributes. Larcher R, Franciosi E: Exploring the microbiota of the red-
brown defect in smear-ripened cheese by 454-
21. Baruzzi F, Quintieri L, Caputo L, Cocconcelli P, Borcakli M, pyrosequencing and its prevention using different cleaning
 Owczarek L, Jasinska UT, Ska?pska S, Morea M: Improvement of systems. Food Microbiol 2017, 62:160-168.
Ayran quality by the selection of autochthonous microbial
cultures. Food Microbiol 2016, 60:92-103. 35. Atanassova MR, Fernández-Otero C, Rodrı́guez-Alonso P,
This work describes the isolation of technologically useful LAB strains Fernández-No IC, Garabal JI, Centeno JA: Characterization of
from traditional Ayran samples. These isolates contribute to the overall yeasts isolated from artisanal short-ripened cows’
sensory quality, preservation of traditional organoleptic characteristics cheeses produced in Galicia (NW Spain). Food Microbiol 2016,
and extension of shelf-life, that thus can potentially be employed for large- 53:172-181.
scale industrial production of this food.
36. Gillot G, Jany JL, Poirier E, Maillard MB, Debaets S, Thierry A,
22. de Oliveira MN: Fermented milks and yogurt A2 – Batt, Carl A. In Coton E, Coton M: Functional diversity within the Penicillium
Encyclopedia of Food Microbiology, edn 2. Edited by Tortorello roqueforti species. Int J Food Microbiol 2017, 241:141-150.
ML. Academic Press; 2014:908-922.
37. Rosa DD, Dias MMS, Grze skowiak ŁM, Reis SA, Conceição LL,
23. Onwulata CI, Rao DR, Vankineni P: Relative efficiency of yogurt, Peluzio M, do CG: Milk kefir: nutritional, microbiological and
sweet acidophilus milk, hydrolyzed-lactose milk, and a health benefits. Nutr Res Rev 2017, 30:82-96.

www.sciencedirect.com Current Opinion in Biotechnology 2018, 49:172–178

178 Food biotechnology

38. Kim D-H, Kim H, Jeong D, Kang I-B, Chon J-W, Kim H-S, 46. Mayo B, Rachid CTCC, Alegrı́a Á, Leite AMO, Peixoto RS,
Song K-Y, Seo K-H: Kefir alleviates obesity and hepatic Delgado S: Impact of next generation sequencing techniques
steatosis in high-fat diet-fed mice by modulation of gut in food microbiology. Curr Genomics 2014, 15:293-309.
microbiota and mycobiota: targeted and untargeted
community analysis with correlation of biomarkers. J Nutr 47. Coughlan LM, Cotter PD, Hill C, Alvarez-ordóñez A, Kelly WJ,
Biochem 2017, 44:35-43. Mora D: Biotechnological applications of functional
metagenomics in the food and pharmaceutical industries.
39. Leite AMO, Leite D, Del Aguila E, Alvares T, Peixoto R, Miguel M, Front Microbiol 2015, 6:1-22.
Silva J, Paschoalin V: Microbiological and chemical
characteristics of Brazilian kefir during fermentation and 48. Walsh AM, Crispie F, Daari K, O’Sullivan O, Martin JC, Arthur CT,
storage processes. J Dairy Sci 2013, 96:4149-4159. Claesson MJ, Scott KP, Cotter PD: Strain-level metagenomic
analysis of the fermented dairy beverage nunu highlights
40. Bourrie BCT, Willing BP, Cotter PD: The microbiota and health potential food safety risks. Appl Environ Microbiol 2017, 83
 promoting characteristics of the fermented beverage kefir. e01144-17.
Front Microbiol 2016, 7:1-17.
49. Creecy JP, Conway T: Quantitative bacterial transcriptomics
A comprehensive review of the effects of kefir and kefir associated strains
with RNA-seq. Curr Opin Microbiol 2015, 23:133-140.
on the host gut and gut microbiome
50. Oki K, Dugersuren J, Demberel S, Watanabe K: Pyrosequencing
41. Yang Y, An H, Zhai Z, Wang G, Li J, Hao Y: Complete genome analysis of the microbial diversity of airag, khoormog and
sequence of Lactobacillus helveticus CAUH18, a potential tarag, traditional fermented dairy products of mongolia. Biosci
probiotic strain originated from koumiss. J Biotechnol 2016, Microbiota Food Health 2014, 33:53-64.
224:18-19.
51. Sun Z, Liu W, Bao Q, Zhang J, Hou Q, Kwok L, Sun T, Zhang H:
42. Yi L, Dang Y, Wu J, Zhang L, Liu X, Liu B, Zhou Y, Lu X, Ge W,  Investigation of bacterial and fungal diversity in tarag using
Johansen HM et al.: Purification and characterization of a novel high-throughput sequencing. J Dairy Sci 2014, 97:6085-6096.
bacteriocin produced by Lactobacillus crustorum MN047 In this study, the authors use high-throughput sequencing to describe the
isolated from koumiss from Xinjiang, China. J Dairy Sci 2016, bacterial and fungal community diversity in 17 tarag samples. It is
99:7002-7015. apparent that microbial diversity across the samples is stratified by
geographic region.
43. Rong J, Zheng H, Liu M, Hu X, Wang T, Zhang X, Jin F, Wang L:
Probiotic and anti-inflammatory attributes of an isolate 52. Jiang Y, Xiong X, Danska J, Parkinson J: Metatranscriptomic
Lactobacillus helveticus NS8 from Mongolian fermented analysis of diverse microbial communities reveals core
koumiss. BMC Microbiol 2015, 15:1-11. metabolic pathways and microbiome-specific functionality.
Microbiome 2016, 4:1-18.
44. Tamang JP, Watanabe K, Holzapfel WH: Review: Diversity of
 microorganisms in global fermented foods and beverages. 53. Yao G, Yu J, Hou Q, Hui W, Liu W, Kwok L-Y, Menghe B, Sun T,
Front Microbiol 2016, 7:1-28.  Zhang H, Zhang W: A perspective study of koumiss microbiome
In this comprehensive review, the authors discuss the microbiology of by metagenomics analysis based on single-cell amplification
fermented foods from around the globe. The paper highlights the diversity technique. Front Microbiol 2017, 8:1-11.
of functional microorganisms that have been associated with fermented In this extensive study, the authors present the use of the single cell
foods and discuss the methods and tools employed to identify micro- genomics technique to analyze the bacterial metagenomes of several
organisms in fermented dairy products. koumiss samples, demonstrating the feasibility of using this strategy to
discover low-abundance taxa. Among the unusual species identified is
45. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Lactobacillus otakiensis, which had never been reported in dairy products
Conlon BP, Mueller A, Hughes DE, Epstein S, Jones M et al.: A new previously, Streptococcus macedonicus, which had not previously been
antibiotic kills pathogens without detectable resistance. reported in koumiss and Ruminicoccus torques, usually found in the gut
Nature 2015, 517:455-459. environment.

Current Opinion in Biotechnology 2018, 49:172–178 www.sciencedirect.com