Potential of indigenous lactobacilli as starter culture in dairy products

Abstract

Traditional production of fermented dairy products involves lactic acid
bacteria that are normally present in the milk and production environment.
These lactic acid bacteria represent the niche microbiota of the geographical
area and they are responsible for local types of fermented products. In order
to standardize indigenous products, the basic requirement is the application
of the determined indigenous lactic acid bacteria as starter cultures
affecting their specific characteristics by performing fermentation and
influencing the ripening process. In the process of cheese fermentation
usually participate bacteria of the genus Lactococcus and homofermentative
lactobacilli. However, the process ripening is influenced mainly by the
so-called nonstarter lactic acid bacteria - lactobacilli and secondary
microflora. Lactobacilli during ripening of cheese continue to breakdown the
rest of lactose, but they are primarily important in the process of protein
breakdown. During metabolism of sugars and amino acids, lactobacilli produce
aromatic compounds which have a positive effect on the flavor of the product.
Some species of lactobacilli are available as probiotics. Some lactobacilli
produce bacteriocins, which prevent the growth of pathogens, as well as many
spoilage microorganisms. Indigenous lactobacilli have application especially
in the production of typical local dairy products that are well accepted by
the local population. Besides that, the use of indigenous lactic acid
bacteria as starter cultures allows the production of cheese with designated
geographical origin that could be placed on the international market.
Consequently, indigenous lactic acid bacteria are a challenge for further
research and possible their practical application in the dairy industry.

Full text

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POTENTIAL OF INDIGENOUS LACTOBACILLI AS STARTER CULTURE
IN DAIRY PRODUCTS
Mirjana Bojanić Rašović*

University of Montenegro, Biotechnical Faculty, Mihaila Lalića 1, 20000 Podgorica, Montenegro
Traditional production of fermented dairy products involves lactic acid bacteria that
are normally present in the milk and production environment. These lactic acid bacteria
represent the niche microbiota of the geographical area and they are responsible for
local types of fermented products. In order to standardize indigenous products, the basic
requirement is the application of the determined indigenous lactic acid bacteria as
starter cultures affecting their specific characteristics by performing fermentation and
influencing the ripening process. In the process of cheese fermentation usually partici-
pate bacteria of the genus Lactococcus and homofermentative lactobacilli. However, the
process ripening is influenced mainly by the so-called nonstarter lactic acid bacteria –
lactobacilli and secondary microflora. Lactobacilli during ripening of cheese continue to
breakdown the rest of lactose, but they are primarily important in the process of protein
breakdown. During metabolism of sugars and amino acids, lactobacilli produce aromatic
compounds which have a positive effect on the flavor of the product. Some species of
lactobacilli are available as probiotics. Some lactobacilli produce bacteriocins, which
prevent the growth of pathogens, as well as many spoilage microorganisms. Indigenous
lactobacilli have application especially in the production of typical local dairy products
that are well accepted by the local population. Besides that, the use of indigenous lactic
acid bacteria as starter cultures allows the production of cheese with designated geogra-
phical origin that could be placed on the international market. Consequently, indigenous
lactic acid bacteria are a challenge for further research and possible their practical
application in the dairy industry.
KEY WORDS: lactic acid bacteria, autochtonous cheese, lactobacillus, cheese ripening
INTRODUCTION
Indigenous foods are an important feature of the culture and habits of a nation and
thus the most important wealth of each country. The indigenous cheeses have a versatile
taste, aroma and consistency when compared to industrially produced cheeses, where
technologies are strictly defined and production conditions are controlled. During the pro-
duction of indigenous cheeses the milk is neither pasteurized nor starter cultures are

* Corresponding author: Mirjana Bojanić Rašović, University of Montenegro, Biotechnical Faculty, Mihaila
Lalića 1, 20000 Podgorica, Montenegro, e-mail: bojanic.m@t-com.me

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applied (Table 1, Figure 1,) (1). This way of production involves lactic acid bacteria
(LAB) that are normally present in the production environment, as well as in milk. The
study of the technological and probiotic properties of autochthonous lactic bacteria is the
first step towards their practical application in obtaining indigenous dairy products. The
diversity of lactic acid bacteria in traditional dairy products and production environment
represents a great potential in biotechnology (2, 3). In order to standardize indigenous
products, the basic requirement is to employ the determined indigenous LAB as starter
cultures which affect their specific characteristics by performing fermentation and influ-
ence the ripening process (4-8).
Diversity of lactobacilli in indigenous dairy products
In artisanal cheeses, the microbiota is quite heterogeneous. Its composition changes
during the cheese ripening. The dominant species in fresh cheese are Lactobacillus pa-
racasei, Lb. plantarum and Lb. brevis, but only Lb. paracasei dominates in the ripened
cheese (9, 10). Lb. paracasei ssp. paracasei represents a dominant strain in the micro-
flora of traditionally homemade Bukuljac cheese (11). Mesophilic lactobacilli are the do-
minant organisms in mature Cheddar cheese (12). Strains Lb. paracasei ssp. paracasei,
Lb. plantarum, Lb. brevis, Lactococcus lactis ssp. lactis, Enterococcus faecium and
Enterococcus faecalis were the main groups present in the Zlatar cheese during ripening
(13, 5, 14). In this cheese are also isolated Lb. casei and Lb. parabuchneri (15). In Irish
Cheddar cheese the main nonstarter lactic acid bacteria (NSLAB) are Lb. paracasei, Lb.
plantarum, Lb. curvatus and Lb. brevis. In fermented yak milk are present Lb. fermentum,
Lb. helveticus and Lb. curvatus, showing that lactobacilli could play an important role in
the fermentation of yak milk. Lb. paracasei, Lb. brevis and Lb. plantarum are dominant
NSLAB of Spanish artisanal goat cheese (16). Lb. paracasei, Lb. plantarum, Lb. pen-
tosus, Lb. rhamnosus and Lb. curvatus are isolated from Pecorino Siciliano cheese du-
ring ripening (17). All of these LAB also were frequently found in the various traditional
fermented products in many countries of Balkan, Europe and in the world (1, 18-29).
Importance of indigenous lactobacilli in dairy industry
Lactobacilli have a great industrial significance, since they are widely used as starter
cultures for a variety of fermented products (30, 31). They are present in raw milk and
dairy products such as cheeses, yoghurts and fermented milks (32). Strains of lactobacilli
from non-dairy foods can also be a potential source of novel starter and adjunct culture
for cheese making (33). Lactobacilli during ripening of cheese continue breakdown of
rest lactose, but are primarily important in the process of protein breakdown. Proteins are
readily degradate by lactobacilli, because they previously breakdown by peptidases and
proteinases and enzymes released upon autolysis lactococci (10). Some species of lacto-
bacilli are traditionally used in the production of various fermented milk, meat and other
products. Lb. helveticus and Lb. delbrueckii subsp. bulgaricus are used in the production
of cheeses such as Parmesan, Mozzarella, Provolone and Swiss cheeses. In addition to

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protective roles achieved by lowering the pH, the used lactobacilli positively influence
the taste and other organoleptic properties of the final product. Lactobacilli during meta-
bolism of sugars and amino acids produce aromatic compounds such as diacetyl, acetate,
benzaldehyde, cresol, skatole and various amines, carbonyl, and sulfur compounds,
which have a positive effect on the flavor of the product (34). Also, very important is the
activity of extracellular proteinases through the production or removal of various peptides
that directly influence the taste and texture of the product (35). The action of proteinases
may produce bioactive peptides with different favorable characteristics (e.g., anti-hyper-
tensive, anti-microbial, antioxidant peptides) (36). Lactobacilli significantly influence the
final characteristics of the product because of tolerance to low pH (a pH lower limit of
3.6 to 4), and that the frequently dominant bacteria in food in the last stages of fermenta-
tion (37). The Lactobacillus genus has widespread use as probiotics and is generally re-
cognized as safe organisms (GRAS) (38). Lb. brevis, Lb. buchneri, Lb. casei, Lb. kefiri,
Lb. paraplantarum, Lb. plantarum have QPS (qualified presumption of safety) status of
EFSA (39, 40). Their favorable activity is indicated in the treatment of various types of
diarrhea, inflammatory bowel disease and syndrome, lactose intolerance, different and
even allergic and cardiovascular diseases, and some cancers (41). Lb. plantarum, Lb. bre-
vis, Lb. casei and Lb. parabuchneri isolated from Brazilian ovine cheese show probiotic
potential, resistance to gastric juices and bile salts and inhibition of food pathogens Liste-
ria monocytogenes, Staphylococcus aureus, Bacillus cereus, Escherichia coli and Salmo-
nella typhimurium (42). Lactobacilli possess inhibitory activity towards the multiplication
of enteropathogens, also spoilage causing bacteria, because they produce antimicrobial
substances (43, 44). Antimicrobial capability of lactobacilli has also been reported (45,
46, 47). They also showed antagonistic activity against Helicobacter pylori (48). Lacto-
bacilli from Zlatar cheese showed good proteolytic activity, as production of bacteriocin-
like substance (13). Technological and flavor formation abilities of the wild strains (Lb.
casei, Lb. plantarum) can be used as starters (24). The lactobacilli community is impor-
tant in the production of Mozzarella cheese (26).
The role of Lb. bulgaricus, together with S. thermophilus is in the milk acidification,
synthesis of aromatic compounds, development of texture and viscosity of dairy products.
Aroma formation is based mainly on the production of acetaldehyde, acetoin and diace-
tyl, exopolysaccharides, bacteriocins, proteinases and peptidases. Bacteriocin "bulgari-
can" created by Lb. bulgaricus operates on Bacillus, Streptococcus, Staphylococcus, Sar-
cina, Pseudomonas, Serratia and Escherichia (49).
Lb. acidophilus stabilizes the microflora of the gastrointestinal tract of humans and
animals. Fermented milk, combining Lb. acidophilus and Lb casei, is available in the pre-
vention of antibiotic-associated diarrhea (50).
Lb. helveticus is found predominantly in the fermented of dairy products and mainly
used for the manufacture of cheeses such as Grana and Provolone. Some interesting cha-
racteristics of this microorganism are its ability to produce high quantities of lactic acid in
milk, its acid tolerance, and the capacity to express a complex proteolytic enzyme system.
This enzyme system, which comprises proteinases, endo peptidases and exopeptidases,
makes an important contribution to the decrease of ripening time, the acceleration of fla-
vor development and the reduction of bitterness (51). Lb. helveticus is obligately homo-

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fermentative LAB. Consumption of cheese containing a Lb. helveticus - exhibits im-
munoregulatory actions, including an increase in the regulatory T cell population and
reduction in proinflammatory cytokine production in mice (52).
Lb. plantarum is a ubiquitous microorganism that is able to colonize several eco-
logical niches, including vegetables, meat, dairy substrates, and the gastro-intestinal tract
(53). It has metabolic capacity and industrial applications (54, 55). Lb. plantarum showed
activity against Salmonella spp. and Pseudomonas aeruginosa. It is resistant to nisin-
additive for fermented dairy products (56). It has a strong inhibitory activity against
Salmonella typhi, E. coli, S. aureus, E. faecalis and Citrobacter spp. (57). Lb. plantarum,
Lb. pentosus, Lb. paraplantarum and Lc. lactis showed bacteriophage resistance on 41
phages from the Chr. Hansen phage collection, as well as good acidification speed and
EPS production (58).
Lb. paraplantarum survives simulated passage through the gastrointestinal tract when
resuspended in the milk (40). It produces bacteriocins that inhibited the growth of Liste-
ria monocytogenes, Listeria innocua and several lactic acid bacteria. It was also observed
that Lb. paraplantarum tolerated exposure to the pH 3.5 and 0.3% bile salts for up to
180 min (59). It is facultative heterofermentative LAB, probiotic starter isolated from
fermented sausage, and it is a great producer of bacteriocins (60). Lb. plantarum and Lb.
paracasei are resistant to acid and bile salts, and they can be used as potentially probiotic
bacteria (61). Lb. plantarum, Lb. paracasei ssp. paracasei isolated from Suero costeño,
can fermente sugars D-Lactose, D-Glucose and D-Galactose. Also, they use other carbo-
hydrates, and it is possible to use these strains as starter cultures for other fermentations
(62). Lb. plantarum and Lb. paracasei isolated from Istrian cheese have a strong aci-
dification ability, as well as proteolitic and antimicrobial activity (63). Lb. plantarum and
Lb. brevis isolated from Brasilian food could be used as probiotic, due to the tolerance to
low pH and bile salts. They exhibited antagonistic activity towards the pathogens L. mo-
nocytogenes and S. aureus, and adhere to the human intestinal epithelial cell line (Caco-
2) (64). Antifungal activity of phenyllactic acid and 4-hydroxyl-phenyl-lactic acid isola-
ted from Lb. plantarum was found (65), as well as the antifungal activity of Lb. brevis on
carcinogenic, toxigenic and allergenic fungi of genera Aspergillus, Fusarium, Penicillium
and Trichoderma (66).
Lb. paracasei ssp. paracasei produces bacteriocins, exhibits auto- and co-aggrega-
tion, and possesses surface polysaccharides and proteins that interact with collagen or si-
milar molecules of eukaryotic cells. The probiotic potential of lactobacillus depends on
the surface characteristics of bacterial cells (40). Lb. paracasei ssp. paracasei formed
coaggregate with L. innocua, E. coli or with Salmonella enterica ser. typhimurium (67).
Lb. paracasei ssp. paracasei isolated from Bukuljac cheese showed a high proteolytic
activity and hydrolyzed alpha(s1)- and beta-caseins. This species produces diacetyl, and
exhibited antimicrobial activity (11). Lb. paracasei ssp. paracasei produce bacteriocin,
exhibited antimicrobial activity against S. aureus and B. cereus and grew well in simula-
ted gastrointestinal conditions (68). It is effective in the regulation of blood cholesterol
and pressure, prevention of gastric mucosal lesion, immunomodulation and alleviation of
allergies, anti-osteoporosis, and inhibition the fat tissue accumulation (69). Also, it pos-
sess strong antagonistic properties against Salmonella enterica ssp. enterica. It is sensi-

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tive to antibiotics and did not produce biogenic amine except for tyramine (70). Lb. casei
and Lb. plantarum efficiently hydrolyzed milk protein (71). Most isolates of Lb. casei are
ribose positive (72).
Lb. coryniformis subsp. coryniformis produces proteinaceous antifungal compounds,
with a maximum activity at the pH between 3.0 and 4.5, which then decreased to the pH
6.0, and was lost at higher pH values (73). Some of the strains Lb coryniformis grew at
45
0
C, also in 6.5% NaCl, produce lactate, also diacetyl and acetoin (74). Consumption of
Lb. coryniformis and Lb. fermentum strains enhances the immune response and may have
a clinical benefit in protection from infections (75). Lb. coryniformis is suitable as a star-
ter in food manufacturing processes, and has a role in eliminating food originated car-
cinogens, such as sodium nitrite and ethyl carbamate (76). Lb. coryniformis was an un-
common species found in Churpi cheese. Its isolates can be potentially used for the deve-
lopment of defined strain starter for Churpi cheese (77).
Lb. curvatus, heterofermentative lactobacillus, produces bacteriocin with a strong
antilisterial activity, and antifungal activity against Cladosporium and Fusarium ssp. was
detected. Bacteriocin is heat and pH stable and its mode of action is bacteriostatic (78,
79). Lb. curvatus is able to grow at low temperature (2-4 °C), and this is important for
fermentation of vegetables, meat product, and sake (80). Lb. rhamnosus prevents the
appearance of antibiotic-associated diarrhea (81).
Lb. rhamnosus was originally isolated from human intestinal flora. It can shorten the
duration and ameliorates the symptoms of infantile rotavirus diarrhea, and has some ef-
fect on preventing atopic diseases among infants and to modulate immune responses (82,
83). Lb. rhamnosus and Lb. plantarum strains isolated from artisanal Coalho cheese are
probiotic candidates to be used in fermented dairy products. They have bacteriocino-
genic potential (84).
Lb pentosus creates exopolysaccharides (EPSs) which improve the texture of yogurt
by increasing the viscosity and binding water, and interacting with other milk constitu-
ents, such as proteins and micelles, to strengthen the rigidity of the casein network. EPSs
produced by LAB have beneficial effects on human health as immunomodulators, anti-
tumor prebiotic effects and cholesterol-lowering ability. EPS can positively affect gut
health (85).
Lb. buchneri has a high cholesterol-reducing rate, acid and bile tolerance, and anti-
microbial activity (86).
Lb. sake in combination with Lc. lactis ssp. lactis produced a good quality cheese.
This bacterium plays an inhibitory effect against food-spoiling bacteria and food-borne
pathogens, including L. monocytogenes, a gram-positive and pathogenic bacterium (87).
Lb. fermentum exhibits probiotic characteristics and has the potential to be a candidate as
a probiotic. It produced inhibitory compound including H
2
O
2
, bacteriocin and bio-surfac-
tants, to inhibit the growth of intestinal and urogenital pathogens. It is effective in de-
creasing the intestinal pathogens and increasing the ratio of probiotic bacteria in healthy
humans (88).
Lb. kefiri isolated from a dairy product have a great potential as a probiotic and can
be used also for producing functional foods. Gram positive pathogens, L. monocytogenes,
B. cereus, E. faecalis, S. aureus, showed sensibility to Lb. kefiri strains, as well as to

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Gram negative bacteria (P. aeruginosa, Salmonella enteritidis, Shigella flexneri) (89). Lb.
kefiri is used to control gut inflammatory disorders (90). Secretion products and surface
proteins from Lb. kefiri have a protective action against the invasion of Salmonella ente-
rica serovar enteritidis to Caco-2 cells and also against the cytotoxic effects of clostridial
toxins on Vero cells (91). Lb. kefiri prevents S. enteritidis interaction with epithelial cells
(92).
Table 1. Characteristics of some indigenous cheeses of some countries of the Balkans
Name of cheese Country Raw milk Type of cheese Senzory characteristics
Njeguški cheese Montenegro sheep, cow
and goat
semi–hard to hard,
full-fat sheep cheese
round, low cylinder, compact surface, crust is golden–
yellow, a few ‘cheese eyes’ evenly distributed, round, shiny,
pleasant, slightly sour–milky and moderately taste.
Pljevaljski cheese Montenegro sheep and
cow
white, brined, soft to semi–
hard, fat to full fat sheep
cheese
uniform triangle or rectangle, slices without crust, uniform
shape, very slight porosity, brittle, curd gentle, porcelain–
looking, milky–sour taste, moderately salty with pleasant,
clearly expressed milk
y
–sour smell
Pirotski cheese Serbia sheep soft, full–fat brined cheese
square slice with regular dimensions and shapes (triangular),
surface is smoothly, color is white, shiny and homogeneous
few small-sized cheese eyes and technological cavities filled
with whey solid cheese body, slightly crumbly and soft after
ripening, moderately to strongly salty and sour, clearly
expressed, taste of sheep milk, pleasant taste, typical.
Sjenički cheese Serbia sheep soft, full–fat brined cheese
triangular shaped slices with flat sides, one side is convex,
surface is smooth with markedly white color equal, ivory
white color, few lentil sized cheese eye solid cheese body,
brittle, well linked, not crumbly pleasant – of sheep milk,
typical lactic acid odor, clearly expressed, aromatic,
moderately to strongly salty and slightly piquant.
Livanjski cheese Bo snia and
Herzegovina
cow and
sheep hard, full–fat
golden–yellow, a couple of medium–sized cheese eyes firm,
not too hard, moderately elastic full, moderately salty,
piquant pleasant, typical of sheep cheeses
Travnički/Vlašićki
cheese
Bosnia and
Herzegovina sheep white, full–fat brined
cheese
white, typical of sheep milk cheeses none to few irregular
shaped cheese eyes firm, not too hard, well connected,
porcelain–like breaks, spreadable, easy to cut and crumbly
milky sour taste, clean, moderately salty, typical of sheep
cheeses clearly pronounced, pleasant and without foreign
additives, typical of sheep cheeses.
Dolenjski cheese Slovenia sheep hard, full–fat
upper and peripheral sides are slightly convex; cheese is
evenly grey–beige in color curd is hard, firm, compact but
not crumbly aromatic, clean, full to slightly piquant, typical.
Kraški cheese Slovenia sheep hard, full–fat
upper side o f the cheese is flat, peripheral side is slightly
convex, cheese is grey–beige in color curd is hard, firm and
granular but not crumbly aromatic, intensive.
Istarski cheese Croatia sheep hard sheep cheese
cylindrical, smooth skin, dark yellow to light brown in color
on the section of the cheese a few cheese stitches size 0.5–1
mm are allowed ‘rocky’ structure full flavor, characteristic
of sheep cheeses
Krčki cheese Croatia sheep hard, full–fat
the rind of the cheese is s mooth, cylindrical shape and the
color varies from ligh t yellow to golden the body is compact
and bound with even shell–like surface at braking, but not
crumbly, on the cut surface a handful of tiny cheese eyes can
be seen ‘rocky’ structure depends on the duration of ripening
of cheese, and ranges from moderate to strongly acid ic and
strong, characteristic of hard type sheep cheese.
Paški cheese Croatia sheep h ard, full-fat
Crust is hard and smooth, yellow to light brown, on the sec-
tion with rarely spaced, tiny circular cheese eyes, or without
them, piquant, typical of sheep sheese, with fine “crystals”.

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Figure 1. Njeguški cheese
CONCLUSION
The diversity of lactic acid bacteria in traditional dairy products and environment re-
presents a great potential for application in dairy industry. The utilization of indigenous
lactic acid bacteria can lead to potential starter cultures with the necessary properties for
typical local products that are well accepted by the local population. Lactobacilli can fer-
ment sugars and decompose proteins. During the metabolism of sugars and amino acids
they also produce aromatic compounds such as diacetyl, acetate, benzaldehyde, cresol,
skatole, and various amines, carbonyl, and sulfur compounds, which have a positive
effect on the flavor of the dairy product. They also produce bacteriocins and have anta-
gonistic activity against pathogen bacteria, and most of them have a probiotic activity. In
addition, the use of indigenous lactic acid bacteria as starter cultures would allow the
production of cheese with designated geographical origin that could be placed on the in-
ternational market. Consequently, they are a challenge for further research and their
possible practical application in the dairy industry.
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ПОТЕНЦИЈАЛ АУТОХТОНИХ ЛАКТОБАЦИЛА КАО СТАРТЕР КУЛТУРA
У МЛЕЧНИМ ПРОИЗВОДИМА
Мирјана Бојанић Рашовић
Универзитет Црне Горе, Биотехнички факултет, Михаила Лалића 1, 20000 Подгорица, Црна Гора
Традиционална производња ферментисаних млечних производа укључује бакте-
рије млечне киселине које су нормално присутне у млеку и производном окруже-
њу. Ове бактерије млечне киселине представљају микробиолошку нишу географ-
ског подручја и одговорне су за локалне врсте ферментисаних производа. У циљу
стандардизације аутохтоних производа, основни захтев је примена одређених ауто-
хтоних бактерија млечне киселине као стартер културa које утичу на њихове спе-
цифичне карактеристике ферментацијом и утицајем на зрење. У процесу фермента-
ције сира најчешће учествују бактерије рода Lactococcus и хомоферментативни
лактобацили. Међутим, на процес зрења највише утичу тзв. нестартер бактерије
млечне киселине - лактобацили и секундарнa микрофлорa. Лактобацили током
зрења сира настављају разградњу остатка лактозе, али су првенствено важни у про-
цесу разградње протеина. Током метаболизма шећера и аминокиселина, лактобаци-
ли производе ароматична једињења која позитивно утичу на укус производа. Неке
врсте лактобацила сe користе као пробиотици. Неки лактобацили производе бакте-
риоцине, који спречавају раст патогена, као и многе микроорганизме кварењa хра-
не. Аутохтони лактобацили би имали примену у производњи типичних локалних
млечних производа који су добро прихваћени од стране локалног становништва.
Осим тога, примена аутохтоних бактерија млечне киселине као стартер култура
омогућило би производњу сирева са географским пореклом који би сe могли пласи-
рати на међународном тржишту. Због тога су аутохтоне бактерије млечнe киселинe
изазов за даље истраживање и могућу њихову практичну примeну у млечној
индустрији.
Кључне речи: бактерије млечне киселине, аутохтони сир, лактобацили, зрење сира
Received: 10 July 2017.
Accepted: 11 September 2017.