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Identification of potential probiotics from fermented sour traditional rice

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 Natural Product Research
Formerly Natural Product Letters

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Identification of potential probiotics from

fermented sour traditional rice varieties and in
vitro simulation studies

S. P. Dharsini, Kanagaraj Suganya & Sundaravadivelu Sumathi

To cite this article: S. P. Dharsini, Kanagaraj Suganya & Sundaravadivelu Sumathi (2023):
Identification of potential probiotics from fermented sour traditional rice varieties and in vitro
simulation studies, Natural Product Research, DOI: 10.1080/14786419.2023.2230608

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Natural Product Research
https://doi.org/10.1080/14786419.2023.2230608

Identification of potential probiotics from fermented

sour traditional rice varieties and in vitro simulation
studies
S. P. Dharsini, Kanagaraj Suganya and Sundaravadivelu Sumathi
Department of Biochemistry, Biotechnology, and Bioinformatics, Avinashilingam Institute for Home
Science and Higher Education for Women, Coimbatore, India

ABSTRACT ARTICLE HISTORY

Fermented products contain probiotic organisms that have benefi- Received 24 March 2023
cial and therapeutic effects on the gastrointestinal tract. The main Accepted 23 June 2023
objective of the study is to isolate probiotic bacteria from fer- KEYWORDS
mented sour traditional rice water and to evaluate their probiotic Red rice; white rice;
activity. The microbes were isolated from the fermented rice water fermented sour rice
and the characterization of the organisms was determined using water; probiotics; gut
MALDI-TOF MS. The morphological analysis, biochemical test, and microbiome
carbohydrate fermentation test were done for further characteriza-
tion. The colonization and therapeutic properties of organisms
were evaluated by performing in vitro simulation studies. The
results indicated that the isolated gram-positive organisms
Pediococcus pentosaecus and Lactococcus lactis from traditional fer-
mented sour rice water possessed desirable in vitro probiotic prop-
erties. Consuming fermented sour rice water enriches intestinal
flora with beneficial bacteria and enzymes. Fermented rice water
improves gut microbiome health, immune system function, and is
also used to treat chronic conditions.

CONTACT Sumathi Sundaravadivelu sumathi_bc@avinuty.ac.in Department of Biochemistry, Biotechnology,

and Bioinformatics, Avinashilingam Institute for Home Science and Higher Education for Women, Coimbatore, Tamil
Nadu, India
Supplemental data for this article is available online at https://doi.org/10.1080/14786419.2023.2230608
© 2023 Informa UK Limited, trading as Taylor & Francis Group
2 S. P. DHARSINI ET AL.

1. Introduction
Fermentation is one of the most effective ways for improving the nutritional content
of food (Senthil et al. 2009). Microbes involved in the fermentation process have
recently been linked to a variety of health effects and become a new focus of research
interest (Dharshini et al. 2021). The anti-nutritional compounds in fermented rice are
broken down by the lactic acid bacteria (LAB), resulting in enhanced bioavailability
of nutrients like iron, potassium, and calcium. The phenolic components in fermented
rice, such as p-hydroxybenzoic acid derivatives, syringic acids, and hydroxycinnamic
acid derivatives, promote these activities and boost the immune system (Thilagavathi
et al. 2019).
During fermentation, lactic acid bacteria (LAB) act as probiotic organisms to syn-
thesize vitamins and minerals which produce biologically active peptides with enzymes,
such as proteinase and peptidase, and remove some non-nutrient (Şanlier et al. 2019).
Fermentation enriches the rice, with more therapeutic value by restoring healthy
intestinal flora, and preventing gastrointestinal aliments like infectious ulcerative colitis,
duodenal ulcers, irritable bowel syndrome, Crohn’s disease, and celiac disease, candida
infection, etc. (Choi et al. 2014; Ray et al. 2016; Nath et al. 2021; Gervasi et al. 2022).
Probiotics are considered an emerging alternative to eradicate and manage the patho-
gen (Park et al. 2023) and are more prominent to evaluate their effectiveness against
pathogenic microorganisms (Valdes et al. 2018). Fermented foods replace harmful
bacteria with more beneficial bacteria have been related to long-time survival and
good health (Ashokkumar et al. 2020).
The lactic acid bacterium strain is a safe and promising probiotic. Fermented foods,
vegetables, dairy products, aquatic products, raw animals, and plant products, contains
lactic acid bacteria. According to certain studies, LAB plays a role in the food indus-
tries, and biological applications include increasing the taste and nutrition of food
as an additive (Jiang et al. 2021). As a starter culture, it’s widely used and known for
its therapeutic values. It is safe to eat and is commonly employed in the fermentation
of foods, such as cheese, yogurt, and sauerkraut (Górska et al. 2019). Due to the risks
of consuming synthetic antioxidants, research focused on natural products containing
an antioxidant activity that reduce the toxic effect. Throughout millennia, natural
products have consistently served as a fundamental source, not only for essential
nutrients but also for valuable remedies (Santini and Cicero 2020). Several studies
showed that fermentation can increase bioactive compounds with increased phenolic
acids and antioxidative activity (Nath et al. 2020; Liu et al. 2022; Park et al. 2023).
Intake of fermented products decreases the incidence of atherosclerosis disease,
lowering blood cholesterol, and preventing cancer, kidney stones, and heart diseases
(Ilango et al. 2020). The formulation of culture media specifically tailored for the
growth of microorganisms holds immense potential for achieving significant economic
advantages (Gervasi et al. 2020). In the context of modern life, these molecules have
emerged as highly intriguing substances with great potential as nutraceuticals and
functional foods (Gervasi et al. 2016).
The present study aims for the isolation and in vitro characterization of potential
probiotic microorganisms from fermented traditional sourrice water of red rice
(Mappillai samba rice) and white rice (Kichilli samba rice).
 Natural Product Research 3

2. Results and discussion

Fermented products contain probiotic organisms that have beneficial and therapeutic
effects on the gastrointestinal tract. Several in vitro experiments were performed to
assess the probiotic properties of isolated bacteria to confirm the isolates as probiotics.

2.1. Collection of fermented rice water samples

The cooked rice was soaked in water and allowed to ferment. The overnight fermented
sour rice water samples of red rice (Mappillai Samba) and white rice (Kichilli Samba)
were collected and stored aseptically in a container which is shown in Figure S1.

2.2. Isolation of bacterial strains from fermented sour rice water samples by
plating
Serial dilution was used to obtain a culture plate that yields a countable number of
separate colonies. Figure S2 shows the spread plate of the organism growth which
was incubated at 37 °C for 16–24 h. Two types of bacterial strains were isolated from
the traditional fermented sour rice water. The isolated colonies appear creamy,
white-colored, round-shaped, and non-spore-forming, for red and white rice. The
isolated cultures were then subsequently cultured on MRS agar medium by quadrant
streaking method which was shown in Figure S2. The obtained pure culture was
stored for further use.

2.3. Identification of bacterial species

MALDI-TOF identified the bacterial species of the rice water. The spectrometry iden-
tified Pediococcus pentosaecus in red rice and Lactococcus lactis in white rice. Pediococcus
pentosaecus showed a higher score value of 2.25 and L. lactis showed a score value
of 2.04 which is mandatory to secure genus and probable species identification. The
score values for the probiotic species are shown in Figure S3 and the species were
selected according to the peak mass values.

2.4. Gram staining and biochemical characterization

The isolated bacterial strains from fermented sour rice water samples are purple-colored,
gram-positive, spherical, or cocci-shaped bacteria having a thick peptidoglycan layer
which is shown in Figure S4. Commonly used probiotic strains are lactic acid bacteria
(LAB) which are gram-positive, rod, and cocci-shaped that have been used for cen-
turies for their probiotic activity in the gut microbiota (Somashekaraiah et al. 2019).
Thilagavathi et al. (2019) conducted a study on the probiotic and anticancer activity
of fermented rice water in gram-positive bacteria. Biochemical test results demon-
strated positive results for indole, Voges Proskauer (VP), Methyl Red (MR), citrate, and
nitrate, and negative results were observed for catalase, oxidase, and starch hydrolysis
as depicted in Figure S5 and Table S1. The isolated test organisms were able to utilize
4 S. P. DHARSINI ET AL.

the carbohydrates, such as glucose, lactose, maltose, sucrose, or mannitol as shown

in Figure S6 and Table S2.

2.5. Motility test and antibiotic resistance

Isolated organisms are identified as non-motile and the majority of lactic acid bacteria
do not move (non-motile). Our isolates also possess probiotic characteristics by
expressing negative results for motility. A study conducted by Jiang et al. (2021)
showed non-motile organisms for the isolation and characterization of Pediococcus
sp. Bacterial isolation showed an absence of bacterial movement during the incubation
period indicating that our test organism does not contain flagella is an important
characteristic of probiotic bacteria. Antibiotic resistance testing is still required for
probiotic characterization. Table S3 represents the resistance and susceptibility of the
bacterial colonies for different antibiotics expressed in millimeters. According to our
study, the isolates P. pentosaecus and L. lactis were found to be susceptible to cefo-
taxime and had a zone of inhibition of more than 10 mm they were also intermediately
sensitive to kanamycin and spectinomycin, with inhibition of <10 mm. The zone of
inhibition was shown in Figure S7.

2.6. Probiotic assessment for bacterial isolates

2.6.1. Tolerance to pH
The most significant quality of the probiotic microorganism is to survive in an acidic
environment to reach the small intestine and express the colonization effect on the
human gastrointestinal system (GI). Probiotic bacteria must have the potential benefit
to travel through the harsh, stressful, acidic conditions of the stomach (small intestine)
for their storage and distribution. Two pH levels of the growth medium were adjusted
with HCl, ranging from 3.0 (fasting) and 7.2 (after taking a meal) considering the stom-
ach acidity which varies from individual to individual. Figure S8 showed the acid tol-
erance of the test organisms. The survival rate of P. pentosaecus and L. lactis showed
>80% for 3 h. Pediococcus pentosaecus and L. lactis showed significant growth at pH 3
without any loss in viability. After 2 h of incubation, the growth of these two bacteria
was not affected by low pH and could survive in the harsh acidic environment of the
stomach. Manovina et al. (2019) studied the effect of pH on traditionally fermented
rice and the isolated organism showed tolerance to low pH. Nath et al. (2020) reported
the effect of acid tolerance by studying its in vitro screening of probiotics and have
shown tolerance to low pH. Hence these organisms exhibit their colonization effect in
the gastrointestinal tract during varying pH in the stomach and show probiotic activity.

2.6.2. Gastric tolerance

To determine the efficiency of probiotic characteristics, the bacterial strains were tested
for their capacity to survive in a stressful gastric environment to demonstrate their ther-
apeutic function. Figure S8 showed that P. pentosaecus and L. lactis were able to tolerate
simulated gastric juice at pH 3 by showing 83% of survivability for P. pentosaecus and 86%
for L. lactis for 3 h. As a result, these strains have the potential to proliferate and colonize
 Natural Product Research 5

in the stomach’s acidic environment. Zommiti et al. (2018) studied the tolerance for the
gastric environment (pH 3) by in vitro assessment of the probiotic properties, and the
organism has shown the capability to withstand the harsh environment. Pediococcus pen-
tosaecus and L. lactis strains showed good and steady tolerance activity to the gastric juice
and these organisms execute beneficial effects in the stomach.

2.6.3. Bile tolerance

The probiotic organism’s tolerance to bile salts is a crucial criterion for colonization
and metabolic activity. Probiotics that can grow and metabolize at physiological bile
concentrations have a greater chance of surviving in the GI tract. After digestion the
concentration of bile salt in the gut is well-known to vary, ranging from 1.5 to 2%
after that decreasing to around 0.3%. The present study reported an 85% of survival
rate for both P. pentosaecus and L. lactis in the presence of bile are shown in Figure
S9. The findings revealed that the probiotic organism survived in the bile and indicates
possible probiotic activity. Bile tolerance is a significant parameter of probiotic bacteria
that allows them to survive, develop, and exert their effects on the gastrointestinal
tract (Somashekaraiah et al. 2019). The present study shows steady and exponential
growth without any lag in the survival of bile salt, which notably signifies their effi-
cacy and further use as a potential probiotic strain.

2.6.4. Pancreatic tolerance

Pancreatic enzymes (such as amylase, lipase, and protease) are released into the small
intestine via the pancreatic duct and aid in the digestion of proteins, carbohydrates,
and lipids in meals. In recent times, many studies have been conducted to demon-
strate the interaction of bacteria with pancreatic enzymes, and their survival by in
vitro screening becomes an important criterion for probiotic selection. Figure S9
showed >80% tolerance level of the test organisms to 0.5% pancreatin for both bac-
terial isolates. A study conducted by Shokryazdan et al. (2014) on the probiotic strains
showed good tolerance against pancreatic tolerance. The isolated organisms can grow
in the presence of pancreatic enzymes and possess probiotic properties by migrating
from the intestine to the pancreas.

2.6.5. NaCl tolerance

NaCl is an inhibitory substance that can prevent certain bacteria from colonization.
If the NaCl concentration is too high, the bacterial cell membrane will be destroyed.
Tolerance to 0.5, 1, and 5% NaCl was found in P. pentosaecus and L. lactis as depicted
in Figure S10. A study conducted by Dey et al. (2019) on the salt tolerance of L. lactis
observed growth under 0, 1, 3, and 5% NaCl. As a result, the identified organism was
able to flourish in the salty environment, indicating that it had a probiotic function.

2.6.6. Cell surface hydrophobicity and cellular autoaggregation of the isolated

organism
The probiotic organism’s capacity to attach to both hydrophobic and hydrophilic envi-
ronments is regulated by the bacteria’s cell surface hydrophobicity (CSH), which is an
6 S. P. DHARSINI ET AL.

essential selection parameter for a possible probiotic organism. The isolates were tested
for their affinity for hydrocarbons and their ability to interact with the cell membrane
of the host’s gastrointestinal tract and adhere to the cell surface using non-polar mol-
ecules (toluene, xylene). The experimental data showed that the cell surface hydropho-
bicity of P. pentosaecus and L. lactis strains on toluene was 17.94 and 49.36% and xylene
was 27.4 and 43.47%, respectively which is shown in Figure S11. This indicates that the
organisms exhibit, a moderate percentage of hydrophobicity. Bacteria with a high per-
centage of hydrophobicity have a high capacity for adherence to intestinal mucosal
cells (Nath et al. 2021). Pediococcus pentosaecus showed comparatively increased cell
surface hydrophobicity on xylene hydrocarbons, whereas, L. lactis had adhesion capability
on toluene, exhibiting the potential probiotic property.
The capacity of bacteria to attach to epithelial cells and the mucosal surface of
the gastrointestinal system is known as auto-aggregation. One of the most important
physicochemical properties that promote interactions between bacteria and the host’s
intestinal wall for the execution of health effects is cellular auto-aggregation. The
cellular auto-aggregation of P. pentosaecus and L. lactis strains was 36.4 and 39.2%,
respectively. Through this probiotic assessment, the percentage of auto-aggregation
was recorded as moderate, as shown in Figure S11. Bacterial auto-aggregation is
essential for bacterial adherence, colonization, and persistence in the mouth cavity,
gastrointestinal system, and urogenital tract (Nath et al. 2020). Pediococcus pentosaecus
and L. lactis strains have the moderate absorbing capacity in the intestine and gut
microbiota which shows potential probiotic activity.

2.6.7. Safety assessment

The test organisms P. pentosaecus and L. lactis, when grown on sheep blood agar,
exhibited γ-hemolysis which means no hemolytic activity occur as shown in Figure
S12. The absence of hemolytic activity implies that these bacteria are non-virulent,
and shows that the isolated probiotic bacteria have a beneficial effect.

2.6.8. Evaluation of antagonistic activity

When different food sources are fermented, probiotic strains release compounds like
organic acids, hydrogen peroxide, bacteriocins, or other inhibitory substances that
prevent pathogenic and damaging microorganisms from growing. The probiotic organ-
isms P. pentosaecus and L. lactis both have antimicrobial compounds that effectively
inhibited the strains of Pseudomonas aeruginosa and Bacillus cereus. The zone of inhibition
was found to be 7 and 8 mm for P. aeruginosa and for B. cereus, it was found to be 8
and 8 mm which are given in Table S4. This shows that the isolated beneficial organisms
have a promising antimicrobial agent to control the growth of unfavourable microor-
ganisms in food and are considered as healthy to consume.

3. Conclusion
Pediococcus pentosaecus and L. lactis isolated from fermented sour rice water met the
probiotic criteria by demonstrating considerable survival features in artificial digestive
circumstances as well as intestinal adhesion capacity without virulence. According to
 Natural Product Research 7

the study, drinking fermented rice water helps digestion, relieves constipation, boosts
the immune system, and keeps the gut healthy. However, more research is needed
to better understand their nutritional characteristics and health beneficial qualities in
real-life situations for human use.

Acknowledgements
The authors are thankful to Avinashilingam Institute for Home Science and Higher Education for
Women, Coimbatore for providing lab facilities.

Disclosure statement
No potential conflict of interest was reported by the author(s).

Funding
The author(s) reported there is no funding associated with the work featured in this article.

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