EFFECTS OF METABIOTIC BACILLUS SUBTILIS FOR MICROBIOCENOSIS FORMATION IN EARLY-WEANED PIGLETS
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Bulgarian Journal of Veterinary Medicine, 2021 ONLINE FIRST
ISSN 1311-1477; DOI: 10.15547/bjvm.2021-0062
Original article
EFFECTS OF METABIOTIC BACILLUS SUBTILIS FOR
MICROBIOCENOSIS FORMATION IN EARLY-WEANED
PIGLETS
V. POPOV, N. NAUMOV & G. SVAZLYAN
Kursk Federal Agrarian Scientific Center, Kursk, Russian Federation
Summary
Popov, V., N. Naumov & G. Svazlyan, 2021. Effects of metabiotic Bacillus subtilis for mi-
crobiocenosis formation in early-weaned piglets. Bulg. J. Vet. Med. (online first).
This paper discusses the results of research related to cultivation of the probiotic microorganism B.
subtilis on a grain-based nutrient medium of naked oat (Avena nuda) and studies the possibility of
using metabolites as a liquid dietary supplement to correct microbiocenosis gastrointestinal tract dis-
orders in early-weaned piglets. The weight fraction of proteinogenic amino acids in the experimental
probiotic suspensions was determined by means of capillary electrophoresis. The metabolic activity of
Bacillus subtilis DSM-32424 strain was studied on both sprouted as well as non-sprouted naked oat
(Avena nuda) ‘Nemchinovsky’ variety grain-based nutrient medium. It was proved that the maximum
microbial count reached 4.9×107 CFU/cm3 on the 6th day of cultivation on the medium based on
sprouted naked oat. The use of dietary supplement based on Bacillus subtilis DSM-32424 strain in
amount of at least 1×109 CFU/pig had a positive impact in terms of the formation of microbiocenosis
in animals at the time of transferring piglets to plant diet.
Key words: dietary supplement, Enterobacteriaceae, metabiotics, microbiocenosis, nutrient
medium, piglets, probiotics
INTRODUCTION
Probiotics are living microorganisms and microorganisms in nature is manifested,
substances of microbial origin able to among other ways, through their antago-
provide beneficial effects on physiological nism. Antagonism consists in the fact that
functions and biochemical reactions of the bacteria from one species, when develop-
body given the natural process of their ing together with another species, can
administration (Shenderov, 2013; Paja- inhibit its vital activities. This bacterial
rillo et al., 2015; Ardatskaya et al., 2017; property is of practical use in veterinary
Plotnikova, 2018). medicine owing to the use of bacteria as
Published research (Patel & DuPont, probiotics. It is proved that the wide-
2015; Bai et al., 2017; Rusaleyev et al., spread administration of various probiotic
2019) suggest that the interaction between products from living lactobacilli and bifi-Effects of metabiotic Bacillus subtilis for microbiocenosis formation in early-weaned piglets
dobacteria in veterinary and medical prac- sential role of ‘normal microflora’ for the
tice over the past decades has resulted in formation of microbiocenosis of gastroin-
decrease of their therapeutic action, testinal tract in animals (Sánchez et al.,
prompting scientists to seek novel and 2016). Microflora is directly involved in
more effective microorganisms with pro- digestive processes, and produces en-
biotic properties (Rusaleyev et al., 2019). zymes necessary for metabolism of pro-
It is noteworthy that alongside the teins, carbohydrates, lipids and nucleic
search for more effective probiotics, a acids. When autoflora is dying out, the
scientific justification was developed in body system digests and absorbs it as a
support of the administration of metabiot- source of protein (Pritychenko et al.,
ics as an extension of the probiotic con- 2012; Bekhtereva et al., 2014; Uyeno et
cept. Thus, the elaboration of the probi- al., 2015; Roselli et al., 2017).
otic concept through the study and use of Consequently, the production of me-
metabiotics of probiotic microorganisms tabolite-type dietary supplements enriched
in order to develop novel dietary supple- with cell constituents of bacterial produ-
ments and methods for their use in animal cers is a relevant topic in the field of bio-
husbandry was implemented (Popov et al., technology and animal nutrition.
2020a,b). The purpose of this research was to
Metabiotics are a group of medications study the influence of B. subtilis metabo-
that contain active metabolites (products lites on the formation of microbiocenosis
of vital functions) of the probiotic cul- of the gastrointestinal tract in early
tures, among which lysozyme, bacterio- weaned piglets.
cins, catalases, enzymes, organic and
amino acids, polypeptides and other com-
MATERIALS AND METHODS
pounds (Neschilyaev et al., 2016; Sánchez
et al., 2016; Fisinin et al., 2017). In addi- The research studies took place in the
tion to the bioactive action on the host, Laboratory of Agrobiotechnology of Fe-
they greatly amplify antagonistic action of deral State Budgetary Scientific Institu-
the producing probiotic strain, thus creat- tion Kursk Federal Agrarian Scientific
ing favourable conditions for its vital ac- Center (FSBSI Kursk FASC) in Kursk,
tivity and integration into the microbiome the Russian Federation. The grains of na-
community of gastrointestinal tract (Usha- ked oat (Avena nuda) in its ‘Nemchi-
kov et al., 2015; Uyeno et al., 2015; Ma- novsky’ variety served as nutrient medium
gomedaliyev et al., 2020). in order to produce metabolites in the cul-
The clinical performance of dietary ture of Bacillus subtilis DSM-32424
supplements based on probiotic products strain; and were provided by the Depart-
in the formation of microbiocenosis ment of selection and seed farming at
largely depends on biological and chemi- FSBSI Kursk FASC. All experiments
cal composition of gastrointestinal envi- were conducted in compliance with ethi-
ronment, and manifests itself only during cal standards, in accordance with Direc-
the period of administration owing to un- tive 2010/63/EU of the European Parlia-
favourable conditions for assimilation. ment and Council of the European union
Thus, it is necessary to look for ways to as of September 22, 2010 On the protec-
prolong the effect of probiotics’ usage. tion of animals used for scientific pur-
Still, is it compulsory to highlight the es- poses).
2 BJVM, ××, No ×V. Popov, N. Naumov & G. Svazlyan
The nutrient medium used to produce days were formed, with 15 animals in
metabolites of the Bacillus subtilis DSM- each group. Group 1 received EPS based
32424 culture contained sprouted and on sprouted avena; Group 2 received EPS
non-sprouted grains of naked oat (Avena based on whole-grain avena; Group 3 was
nuda), ‘Nemchinovsky’ variety at the ratio control. The experimental dietary supple-
of 100 g of crushed raw material per 3 L ment sample was evaporated in amount of
of water. The substance was gradually at least 1×109 CFU/mL Bacillus subtilis.
heated up at temperature from 25 to 90 °C The analysis of microflora composition in
for 6 hours. Then it was left to cool down faeces took place on the 10th, 25th
naturally. Under control through a pH- (prenursery piglets) and 40th days (early-
meter, pH was adjusted to 7.5 with a 20% weaned piglets) of life by means of a
aqueous solution of NaOH. B. subtilis quantitative cluster analysis of the large
inoculation was done with culture previ- intestine content (Kondrakhina et al.,
ously standardised in laboratory condi- 2004).
tions up to 1×106 CFU/cm3 at a ratio of 4 Sampling was done directly from the
mL per liter of the prepared nutrient me- rectum onto sterile dishes. The initial dilu-
dium. tion was obtained in the following way: 1
Cultivation lasted 14 days in a KBCG g of the weighed faecal matter was well
100/250 thermostat (Premed, Poland) at homogenised with 9 mL sterile buffer
37±1 °C. The number of B. subtilis CFU solution. A number of subsequent dilu-
in the culture fluid was monitored on a tions were produced with a buffer solution
daily basis on a Levenhuk 740T micro- from 103 to 1010 of the initial dilution,
scope (Guangzhou Jinghua Optics & Elec- and then inoculated on the corresponding
tronics Co., Ltd., China), a Levenhuk nutrient media. Incubation of all grains
M1400 PLUS digital camera (Guangzhou was performed at 3738 °C. The assay
Jinghua Optics & Electronics Co., Ltd., content of bifidobacteria was determined
China) and a pH-meter Kelilong pH-013 using the dilutions of 1051010 diluted in
(Kelilong Instruments, China). Blaurock semi-liquid modified hepatic
The weight fraction of proteinogenic medium. The Lactobacillus count was
amino acids in experimental probiotic obtained from dilutions of 105109 in
suspensions (EPS) was determined by thin fat-free milk. Enterococci were
means of capillary electrophoresis accor- marked out on the Alkaline polymyxin
ding the procedure stipulated by GOST R medium for the isolation of enterococci
55569-2013. The calculation of weight from dilutions of 103107. Staphylo-
fraction of crude protein in g/L was car- cocci were detected by inoculation on
ried out in accordance with GOST yolk salt agar (YSA) from dilutions of
32044.1-2012. 104106. Yeast-like fungi of the genus
The scientific and economic analysis Candida were revealed on the Saburo
of experimental probiotic suspension ef- medium containing levomycetin from di-
fect on the formation of microbiocenosis lutions of 103106. Proteus genus mem-
of piglets’ gastrointestinal tract took place bers were detected on slant agar by
on the premises of the Pig Complex Shukevich’s method in dilutions of 101 to
‘Nadezhda’ in Kursk region during rear-
104 (Kislenko, 2005). Spore-forming
ing of weaning piglets up to the age of 75
anaerobes (clostridia) were identified by
days. Three groups of piglets aged 10
inoculation of the suspensions of dilutions
BJVM, ××, No × 3Effects of metabiotic Bacillus subtilis for microbiocenosis formation in early-weaned piglets
102, 105 and 106 into a melted column nism revealed that the maximum count
of Wilson-Blair agar medium. The total reached 4.9×107 CFU/cm3 on the 6th day
aerobic plate count and their haemolytic of cultivation on the medium based on
properties were analysed after inoculation sprouted avena. On the 1011th day the
of dilutions of 105107 on 5% blood number of CFUs has stabilised around
agar. The potentially pathogenic entero- 1.9-2.0×107 CFU/mL.
bacteriaceae were spotted by inoculation The experimental liquid probiotic sus-
of a drop of suspension (0.05 mL) from pension was a bioactive product. Its
dilutions of 103108 into four sections of a physical properties were revealed through
plate containing Levine’s medium. The its specific odour and colour. The dyna-
total count of Escherichia was determined mics of proteinogenic amino acids corre-
from dilutions of 105108 on the Le- lated with CFU values of probiotic micro-
vine’s medium. The 103 dilution of was organism B. subtilis. The analysis of pro-
used for inoculation on Ploskirev’s me- teinogenic amino acids (Table 1) outlined
dium, and 105 dilution: on Endo agar. the culture liquid as an experimental pro-
The specific media involved in the re- biotic suspension. It is noteworthy that the
search studies were purchased from the weight fraction of crude protein was
Federal Budgetary Institution of Science slightly different in the experimental sam-
State Scientific Center for Applied Mi- ples.
crobiology and Biotechnology (FBIS SSC It is reasonable to assume that the re-
AMB) in the regional settlement of Obo- duction of the crude protein was possible
lensk in Serpukhov, Moscow Region, owing to fermentation of the naked oat
Russia. The content of all types of micro- grains during germination. The qualitative
organisms in 1 g of faeces was evaluated and quantitative composition of the probi-
through the amount of colonies grown on otic suspension featured the complete
the corresponding medium and taking into protein content of the suspension enriched
account the inoculum and its dilution. with organic acids. Along with that, the
Throughout the research period, the ani- analysis of indicators (Table 1) demon-
mals experienced no harm. strated increase in the activity of B. sub-
The statistical data processing in- tilis metabolism after cultivation on a non-
cluded descriptive statistics employing the sprouted avena-based nutrient medium.
statistical analysis package for Microsoft The synthesis of lysine was higher when
Excel. The significance of differences compared to the sprouted grain control. In
between mean values was evaluated by the culture fluid, the amount of amino
Student’s t-test. The differences were con- acids was within the following ranges:
sidered tatistically significant at PV. Popov, N. Naumov & G. Svazlyan
Table 1. Indicators of amino acid composition of the probiotic suspension. Values are presented as
mean±SD, n=3
Control Experiment Control Experiment
Indicators Sprouted
Avena with Sprouted
Avena Avena with
В. subtilis Avena
В. subtilis
1 2 3 4
Weight fraction of 0.80±0.23 0.73±0.31 0.79±0.29 0.70±0.37
crude protein, g/L
Arginine 14.61±0.40 14.40±1.50* 6.55±0.11 3.87±1.25
Lysine 6.91±0.52 9.80±1.80 5.18±0.25 7.67±1.97
Weight fraction of proteinogenic
Tyrosine 10.31±1.10 12.00±0.90* 6.71±1.12 8.93±1.87
Phenylalanine 8.70±0.90 9.12±0.70* 4.38±1.35 5.60±1.21
amino acids, mg/L
Histidine 5.09±1.30 4.30±1.90 3.45±1.21 2.49±1.37
Leucine + isoleucine 24.94±0.90 25.19±0.30* 19.04±0.90 15.49±0.50
Methionine 3.65±1.70 5.81±1.90 3.78±1.25 3.46±1.37
Valine 11.65±0.70 12.68±0.80* 13.40±0.70 8.72±1.29
Proline 19.27±0.10 22.37±0.30 22.34±0.90 19.97±0.30
Threonine 14.97±0.90 10.06±1.70* 15.59±0.20 7.89±1.33
Serine 20.61±0.90 17.68±1.20* 19.81±0.80 10.83±0.10
Alanine 15.13±0.50 20.50±1.40 23.13±0.40 20.49±0.80
Glycine 10.32±1.50 18.20±1.60* 7.84±1.58 8.66±1.33
Note: * statistically significant difference at P6
Table 2. Dynamics of microbiocenosis formation in piglets (mean ± SD, n=5)
Group 1 Group 2 Group 3
B. subtilis in medium of B. subtilis in medium of Control
Microorganism non-sprouted Avena sprouted Avena
type (CFU/g in
faecalis) Days Days Days
10 25 40 10 25 40 10 25 40
8 9 9 8 9 9 8 8
Bifidobacterium 0.2×10 ± 0.23×10 ± 0.31×10 ± 0.20×10 ± 0.25×10 ± 0.36×10 ± 0.20×10 ± 0.27×10 ± 0.30×108±
0.29×108 0.14×109 0.61×109* 0.72×108 0.31×109* 0.61×109* 0.24×108 0.93×108 0.14×108
Lactobacillus 0.23×108± 0.71×108± 0.8×108± 0.19×108± 0.82×108± 0.84×108± 0.2×108± 0.53×108± 0.78×108±
0.23×108 0.47×108 0.11×108* 0.06×108 0.91×108* 0.09×108* 0.09×108 0.32×108 0.82×108
Enterobacter 0.21×106± 0.23×106± 0.36×106± 0.19×106± 0.21×106± 0.32×106± 0.20×106± 0.30×106± 0.70×106±
0.52×106 0.28×106 0.31×106 0.16×106 0.38×106 0.52×106 0.67×106 0.44×106 0.38×106
Proteus 0.65×104± 0.10×105± 0.47×105± 0.73×104± 0.94×104± 0.40×105± 0.70×104± 0.12×105± 0.30×107±
0.33×104 0.11×105 0.51×105 0.46×104 0.82×104 0.06×105 0.31×104 0.09×105 0.41×107
Staphylococcus 0.27×104± 0.23×106± 0.93×106± 0.32×104± 0.22×106± 0.87×106± 0.31×104± 0.43×106± 0.90×108±
0.64×104 0.37×106 0.88×106 0.13×104 0.17×106 0.56×106 0.09×104 0.12×106 1.01×108
Clostridium 0.30×104± 0.28×105± 0.21×106± 0.27×104± 0.26×106± 0.19×106± 0.27×104± 0.18×106± 0.10×107±
0.17×104 0.19×105 0.07×106 0.61×104 0.17×106 0.21×106 0.12×104 0.09×106 0.06×107
Escherichia 0.27×106± 0.31×106± 0.50×106± 0.26×106± 0.30×106± 0.49×106± 0.25×106± 0.35×106± 0.52×106±
0.14×106 0.26×106 0.72×106 0.54×106 0.26×106 0.54×106 0.36×106 0.24×106 0.91×106
Salmonella negative 0.27×102± 0.30×102± negative 0.20×102± 0.23×102± negative 0.11×105± 0.17×105±
0.14×102 0.37×102 0.39×102* 0.41×102 0.11×105 0.09×105
Candida negative negative 0.30×102± negative negative 0.27×102± negative 0.13×103± 0.18×103±
0.29×102 0.47×102 0.21×103 0.16×103
Effects of metabiotic Bacillus subtilis for microbiocenosis formation in early-weaned piglets
Note: * statistically significant at P≤0.05.
BJVM, ××, No ×V. Popov, N. Naumov & G. Svazlyan
nistic effect of B. bifidum. It is noteworthy nutrition of piglets had a significant influ-
that on the 25th day, Salmonella were ence on the proportion of microorganisms
found in feces of piglets from all three in gastrointestinal tract microbiocenosis .
groups. Their largest count, i.e. 0.11×105
CFU/g, was registered in controls,
DISCUSSION
whereas the lowest one in Group 2,
0.2×102 CFU/g, which was by 26% lower The production of dietary supplements
than that in Group 1. based on probiotic microorganisms is
On the 40th day in Groups 1 and 2, the based on their metabolites obtained during
largest share of total microbial counts was culturing on different nutrient media.
that of B. bifidum: 79% and 80.73% re- Grain-based nutrient media are the best
spectively. Lactobacilli reached 0.4% in choice for obtaining biologically active
feces of Group 1, and 18.83% in Group substances from probiotic microorga-
2. Other types of microorganisms reached nisms. The outcome of studies in view of
0.52% and 0.43% respectively. B. subtilis cultivation are consistent with
Staphylococci predominated in the the focus of the research and with the
control group: 44.28% of total count. The findings of other authors (Parker, 1974;
share of lactobacilli was 38.38%, bifido- Nguyen et al., 2016).
bacteria were only third with 14.76%. The However, the production of medicines
share of Proteus was 1.47%, and that of and dietary supplements based on B. sub-
other types of microorganisms 1.1% of tilis was done in Russia and Germany only
the total count. When compared to Group in medical practice (Bactistatin and Hylak
2, the count of bifidobacteria in faeces in Forte products). The research studies re-
piglets from Group 1 was lower by 13.9%. lated to the production and administration
In control group 3, the count of bifidobac- of dietary supplements based on metabio-
teria was lower by 91.7% than in Group 2. tics in animal husbandry and veterinary
The present research studies contri- medicine are at their initial stage of re-
buted to the justification of a reasonable search (Shenderov, 2013; Lebeer et al.,
opportunity to use Avena nuda as a nutri- 2018).
ent medium to produce metabolites during Several recent research papers (Plot-
cultivation of the probiotic microorganism nikova, 2018; Singh et al., 2018) discuss
B. subtilis. Cultivation of the probiotic an analogue of the capsulated metabiotic
microorganism B. subtilis allowed obtain- and prove that it can be used to correct
ing a metabolite composition by way of microbiocenosis gastrointestinal tract dis-
proteinogenic amino acids. The experi- orders in animals.
mental probiotic suspension when B. sub- In our research studies, B. bifidum
tilis was cultivated on the grain-based prevails in formation of microbiocenosis
nutrient medium, both non-sprouted and in piglets through metabiotics. The use of
sprouted, was a dietary supplement con- probiotic metabolites, according to some
taining probiotics in an amount of at least authors, not only stimulates the activity of
2.0×109 CFU/mL enzyme systems, producing beneficial
Research studies involving animals effect on metabolism in body systems of
proved that the use of the probiotic sus- animals, but also improves the ecological
pension of B. subtilis with a grain-based environment of intestine from physiologi-
nutrient of naked oat (Avena nuda) in the cal point of view in order to create and
BJVM, ××, No × 7Effects of metabiotic Bacillus subtilis for microbiocenosis formation in early-weaned piglets
maintain own microflora, as well as regu- biotic microorganism B. subtilis helps
lates symbiotic relationships with the host colonisation of microbiome in normal
(Wang, 2014; Patel & DuPont, 2015; Ne- intestinal microflora, consistent with other
schilyaev et al., 2016; Bai et al., 2017). studies (LeBlanc, 2014; Ardatskaya,
Published research on B. subtilis 2015; Fedorova et al., 2016; Sánchez et
(Huang, 2013; Orel, 2014; Patel & Du- al., 2016).
Pont, 2015; Ardatskaya et al., 2017;
Strekalovskikh & Belousov, 2018) re-
CONCLUSION
vealed a significant correlation between
the content of Bifidobacterium and Lacto- The administration of grain-based B. sub-
bacillus, as well as significant negative tilis probiotic suspension from Avena
correlation between Enterobacterisceae nuda to piglets greatly influenced the pro-
and Clostridium perfingens. The results portion of microorganisms in the micro-
from intestinal microflora studies makes it biocenosis composition of the gastrointes-
possible to affirm that the use of probio- tinal tract. In piglets treated with an ex-
tics influences positively microbial com- perimental probiotic suspension, the con-
position: the count of lactobacilli and bifi- tent of B. bifidum in faeces was signifi-
dobacteria increases. There is an estab- cantly higher than in controls. The micro-
lished tendency towards reduction in the biome was predominantly represented by
number of Escherichia and staphylococci, bifidobacteria and lactobacilli, with the
and absence of lactose negative Es- remaining microflora being less than 1%.
cherichia. A more prominent antagonistic effect was
The experimental data obtained in revealed through B. subtilis on the me-
these studies are consistent with research dium based on the Avena sprouts.
data (Pajarillo et al., 2015; Sánchez et al.,
2016), confirming the favourable effect of
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