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Characterization and probiotic potential of lactic acid bacteria isolated from

dadiah sampled in West Sumatra

Article  in  Food Science and Technology (Campinas) · December 2020

DOI: 10.1590/fst.30020

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DOI: https://doi.org/10.1590/fst.30020

Characterization and probiotic potential of lactic acid bacteria isolated from dadiah
sampled in West Sumatra
Rinita AMELIA1,2, Koshy PHILIP1,3* , Yudha Endra PRATAMA4, Endang PURWATI5

Abstract
Dadiah is a traditional dairy food from West Sumatra. Dadiah is made by fermenting fresh buffalo milk in banana leaves covered
bamboo sticks at room temperature for two days. Dadiah is nutritious because it contains lactic acid bacteria (LAB) that have
probiotic properties. This study aims to determine the characteristics and biochemical properties of LAB by catalase assay and
fermentation type. We identified the LAB found in dadiah using conventional laboratory tests and 16S rRNA sequencing methods
and confirmed that the LAB was Lactobacillus fermentum. Gram staining showed that the isolated bacteria were Gram-positive
bacilli and the catalase assay and fermentation type showed it to be negative catalase and homofermentative.
Keywords: lactic acid bacteria, Dadiah, lactobacillus fermentum, probiotic.
Practical Application: Dadiah, is one of the traditional probiotic dairy foods in West Sumatra that is rich in LAB.

1 Introduction
Dadiah, which is made from buffalo milk fermented in are Lactobacillus, Lactococcus, Bifidobacterium, Tetragenococcus,
bamboo tubes and contains lactic acid bacteria (LAB), is one of Vagococcus, Weissella, Streptococcus, Leuconostoc, Aerococcus,
the famous probiotic foods in West Sumatra. Lintau Buo Utara Oenococcus, Carnobacterium, Enterococcus, Sporolactobacillus,
is one of the regions in Tanah Datar Regency, West Sumatra, and Pediococcus (Yerlikaya, 2019).
noted for its production of dadiah. Dadiah is an integral part
Every dadiah product has different strains of LAB depending
of the food and culture of the Minangkabau people. Dadiah is
on the region of the manufacturer. Each region can use different
also a biological asset that can be developed as a family business
types of bamboo and buffalo species that produce their milk.
to support people’s health and livelihood. This kind of natural
Using 16S rRNA sequencing, LAB in dadiah can be identified.
probiotic food from animal proteins should be supported through
For  years, the dadiah was known to have natural probiotic
the improved development of buffalo farms (Purwati et al., 2017;
properties. This  bacterial strain is non-toxic and safe to consume
Yuniastiti, 2017; Dadih, 2017). In West Sumatra, there are various
and considered as food-grade microorganism (Saputri et al., 2018).
types of bamboo that are used to produce dadiah. The inner
Probiotics are living microorganisms (single or mixed) that
bamboo wall propagates LAB that will help in the fermentation
are present adequately in our food, as much as 106 to 107
process of dadiah. Therefore, the type of bamboo determines the
colony-forming units (CFU) per gram of food (Dwi et al., 2016;
quality of dadiah (Purwati et al., 2017).
Purwati et al., 2017). Commonly, the bacteria are Lactobacillus,
LAB are groups of cocci- or bacilli-shaped Gram-positive Bifidobacterium, Streptococcus, Lactococcus, and Enterococcus.
bacteria. They are facultative anaerobes, catalase-negative, motile, LAB from fermented milk is widely used as probiotics, including
do not produce spores, and create lactic acid as a metabolic Lactobacillus rhamnosus CAN-1, Lactobacillus plantarum,
end-product during carbohydrate fermentation. Probiotic LAB Lactobacillus brevis, Lactobacillus paracasei, Lactobacillus
is classified as homofermentative or heterofermentative based bulin, Streptococcus thermophilus, Lactobacillus fermentum, and
on their metabolic pathways. In homofermentative LAB, they Lactobacillus acidophilus. There is an increased number of new
ferment sugars to produce mainly lactic acid under anaerobic findings of nonpathogenic bacteria and yeast that are considered
conditions. In heterofermentative LAB, sugars are fermented to as probiotics and have health benefits (Saputri  et  al.,  2018;
produce ethanol, CO2, and less lactic acid (Ayyash et al., 2018). Rayavarapu et al., 2019; (Djunaedi, 2007). Furthermore, diet
LAB does not constitute cytochrome and does not form spores. supplemented with yoghurt showed a significant decline in blood
They belong to the order Eubacteriales under Streptococcaceae cholesterol. LAB in the presence of prebiotics were found to be
and Lactobacillaceae families. The genera that comprise LAB effective against increased blood lipid profile (Sarfraz et al., 2019).

Received 30 July, 2020

Accepted 21 Sept., 2020
1
Lincoln University College, Petaling Jaya, Selangor, Malaysia
2
Medical Faculty, Baiturrahmah University Padang Indonesia, Padang, West Sumatera, Indonesia
3
Institute of Computer Science and Digital Innovation, UCSI University, Cheras, Kuala Lumpur, Malaysia
4
Doctoral Program, Faculty of Animal Science, University of Andalas, Padang, Indonesia
5
Faculty of Animal Science, University of Andalas, Padang, West Sumatera, Indonesia
*Corresponding author: [email protected]; [email protected]

Food Sci. Technol, Campinas,      Ahead of Print, 2020 1/7 1

 Lactic acid bacteria sampled from dadiah as potential probiotic

LAB is known as food-grade group of microorganisms, generally

recognized as safe, and beneficial to health (Suardana & Suarsana,
2017). LAB that is utilized as probiotics have the following
characteristics: nonpathogenic, viable in medium with low pH,
able to grow on medium with high-concentrated bile salts, able
to be adherent and colonize epithelial cells, have antibacterial
activities, and have health benefits (Son et al., 2017). Probiotics are
known to have many health benefits, including antioxidant activity
(Wang et al., 2017; Tallapragada et al., 2018). Probiotics modulate
the microbial composition associated with conditions such as
allergies, cancer, diabetes, inflammatory diseases, cardiovascular
diseases, and dyslipidemia. In the past decade, the antioxidant
activity of LAB and LAB-related products has been frequently
reported (Ho et al., 2019).
LAB can also produce antimicrobial compounds besides Figure 1. Dadiah from Lintau Buo.
lactic and acetic acids, diacetyl and bacteriocins antagonistic
to a broad spectrum of microorganisms and can inhibit 37 °C. After 48 hours, a single colony of the LAB was observed.
food spoilage and pathogenic bacteria. Those are the reasons The total colony forming units (CFUs) was calculated using the
why LAB is often used as an alternative to food preservation Quebec colony counter (Endang Purwati et al., 2016).
products. Bacteriocins are antimicrobial peptides produced by
bactericidal or bacteriostatic bacteria. Bacteriocins produced 2.3 Morphology identification of Dadiah bacterial culture
by microorganisms does not have any inhibitory effect on the
producing organisms. Bacteriocin can also inhibit the growth A loopful of bacterial culture was taken and then placed into
of contaminant bacteria that cause foodborne diseases. a microscopic glass slide. Crystal violet dye was added on to the
slide and then left to react for 1 minute. After that, it was rinsed
Therefore, this study aims to identify the LAB isolated with distilled water and then air-dried. Iodine drops were then
from dadiah from Lintau Buo Utara as a potential probiotic and added and left to react for 1 minute. Next, the slide was rinsed with
evaluate its antioxidant effects. Dadiah has long been known to distilled water and air-dried before dipping in ethanol for 20 minutes
have benefits as a natural probiotic. Moreover, the probiotics followed by counterstaining with safranin for 30 seconds. The result
contained in dadiah from Lintau Buo Utara are considered halal. was observed under the microscope at 400× magnification.

2 Materials and methods 2.4 Biochemical properties

2.1 Materials The assay was carried out by inoculating the LAB isolates
into 5  mL of MRS Broth (Merck) contained in test tubes.
Buffalo milk samples were taken from the village of Tanjung Durham  tubes were inserted in inverted positions and then
Bonai, district of Lintau Buo Utara, Tanah Datar Regency, West incubated for 48 hours at 37 °C. Then, the presence or absence
Sumatra. The breeders milk the buffaloes early in the day to make the of bubbles in the Durham tubes were observed.
dadiah. Before milking, the farmer first washes the udder. The milk
obtained is immediately poured into the prepared bamboo tubes 2.5 Acid resistance assay
which were then covered with banana leaves. The milk was left for
48 hours at room temperature to ferment naturally. The bamboo Using 9 ml of MRS media broth, 1 ml bacterial culture was
used for the container is Gigantochloa asper (Schult) Kurz species inoculated and incubated at 37 °C for 24 hours with the pH
usually referred as bamboo rope or Aru by the locals (Figure 1). adjusted to 4 using 5N HCl addition. Furthermore, the dilution
was carried out using the spread method to the MRS media and
2.2 Macroscopic identification of Dadiah bacterial culture incubated at 37 °C for 48 hours. The CFU number of the bacteria
that survived were calculated. The number of the survived colonies
De Man-Rogosa-Sharpe (MRS) broth (Merck) enriched media was expressed as LAB viability. The higher the LAB viability, the
and MRS Agar (Merck) media were prepared. As much as 1 g of higher will be the LAB resilience against acid.
dadiah was dissolved in 9 ml of MRS Broth solution in a test tube
and vortexed until homogeneous for the initial 10-1 dilution of
2.6 Bile salt resistance assay
dadiah. Then, the solution was placed into an anaerobic jar and
then incubated for 24 hours at 37 °C. After that, 1 ml (1000 µL) One ml of bacterial culture was inoculated into 9 ml of MRS
of the first dilution was taken, added into a test tube with 9 mL broth medium and incubated at 37 °C for 5 hours with 0.5% bile
of MRS broth solution and then vortexed until homogeneous salt. The mixture was then serially diluted to 10−6, spread on MRS
for the 10−2 dilution. This procedure was repeated until the 10−9 agar medium and incubated at 37 °C for 48 hours. The number of
dilution is attained. From the last dilution, 100 µL of the sample bacteria that grew was calculated. The number of colony forming
was taken and spread on the MRS agar media. The inoculum units (CFUs) was expressed as LAB viability count. The higher the
was placed into the anaerobic jar and incubated for 48 hours at LAB viability the higher will be the LAB resilience against bile salt.

2 2/7 Food Sci. Technol, Campinas,      Ahead of Print, 2020

 Amelia et al.

2.7 Antimicrobial assay then heated in a microwave for 30 seconds. After the solution
was made lukewarm, 2 ul of redsafe / Gelview was added as
Antimicrobial activity assays were carried out using the disk
a coloring agent. The agar height was about 0.5 mm and the
diffusion method with Escherichia coli O157, Listeria monocytogenes,
electrophoresis comb arranged in the agar. The comb was
and Staphylococcus aureus ATCC 25923 bacteria as test bacteria.
removed after the agar was set.
One mL of LAB culture was placed into sterile Eppendorf tubes
and then centrifuged at 10000 rpm for 5 minutes. 0.4 g of nutrient
media was prepared (using 20 g of nutrient agar in 1000 mL of 2.12 Running gel electrophoresis
distilled water). Then 0.2% enriched bacteria colony was added The agar was placed in the electrophoresis apparatus and
to the medium and left to culture. The test strains mentioned then added with TAE solution until the agar is immersed. As
were assayed for inhibition. Then, 50 μL of LAB supernatant was much as 5µL sample and 5µL DNA ladder were injected into the
inserted onto the disk. The tested antibiotics were ampicillin 40 µL, agar well. The agarose run was set to 100V for 40 minutes and
and kanamycin 30 µL for controls compared to the supernatant. the result was seen under the UV light. After the PCR results
The petri plates used were then incubated anaerobically at 37 °C. were read, the amplified DNA was then purified to be sent to
The antibacterial activity was expressed as the diameter of the Genetika Lab for sequencing.
clear zones of inhibition caused by the antibiotics controls and
the LAB supernatant. 2.13 Analysis of sequencing data

2.8 Identification of LAB using 16S rRNA The sequencing data analysis is performed using the DNASTAR
software program. For the sequence alignment analysis, the
Microbial DNA extraction was conducted using the Promega obtained sequences were compared with those already deposited
USA KIT. As much as 1000 µL of the single colony from MRS broth in the GeneBank (http://www.ncbi.nlm.nih.gov) using BLAST
containing the LAB isolate was put in a new Eppendorf tube and (Basic Local Alignment Search Tool). The  phylogenetic analysis
then centrifuged at 14,000 rpm for 2 minutes. Then the pellet was was done using MEGA v7.0 tools with the Maximum Likelihood
taken, added with 480 μL of 50mM EDTA and 120 μL of Lysozyme. and the kimura -2 mode algorithm.
The mixture was incubated in 37 o C water bath for 60 minutes
and then centrifuged for 2  minutes at 14,000 rpm. Then  the 3 Results and discussions
supernatant was removed, the pellet was taken, then 600 µL of
nuclei lysis solution was added and then homogenized. After that,
3.1 Macroscopic identification
the mixture was incubated at 80 oC for 5 minutes. After that, 3 µL
of RNase Solution was added, homogenized, and incubated in The formed single colony from dadiah had these characteristics:
37 °C water for 60 minutes. Next, 200 µL of Protein precipitation round-shaped, slick edges, smooth and convex surface, white-beige
solution was added, vortexed, incubated in ice for 5 minutes, and color, and 1.8 mm in diameter. In contrast to probiotics from
then centrifuged for 3 minutes at 14,000 rpm. The supernatant was prato cheese that show brightness color (Silva  et  al.,  2018).
transferred to a new tube and the pellet is removed, added with The  total number of LAB in dadiah was 7.1 × 1010 CFU/ml
600 µL isopropanol and homogenized, and then centrifuged for
2 minutes at 14,000 rpm. Then, the pellet and the supernatant were Table 1. The primer 16S rRNA.
removed, 600 µL of 70% ethanol was added and homogenized,
Composition Volume
and centrifuged for 2 minutes at 14,000 rpm. Lastly, the pellet
was taken and aerated for 15 minutes, and then rehydrated with Master Mix PCR 12.5 µL
50 µL of rehydration solution for 30 minutes at 65oC. Primer F 1.0 µL
Primer R 1.0 µL
2.9 Preparation of PCR primary (16S rRNA) dH2O 9.5 µL
The R primer (16S-1492R, Tm 47 C, 5’GTT TAC CTT GTT
o
24.0 µL
ACG ACTT-3) and F primer (16S- 27F, Tm 54.3 oC, 5’AGA DNA 1.0 µL
GTT TGA TCC TGG CTC AG-3) were prepared at 10pM
Total number 25.0 µL
concentrate. The primer was taken at 90 µL dH2O + 10µL of R
and F primers. The R and F primers were dissolved in TE buffer
with 100µM concentrate. Table 2. The PCR programme.
Stages Temperature Time
2.10 Preparation for 16S rRNA gene amplification
Pre denatured 95 °C 2 minutes
Preparation for 16S rRNA gene amplification are based on the Denatured 95 °C 45 seconds
primers for 16S rRNA (Table 1) and the PCR programme (Table 2).
Anneling 56 °C 45 seconds
Extention 72 °C 1 minute 40 seconds
2.11 Preparation of 1.5% agarose for PCR electrophoresis
Final extention 72 °C 10 minutes
As much as 0.6  gram of agarose (obtained from 1.5% x
Cooling 4 °C ~
40 mL = 0.6 gram) was dissolved in 40ml of TAE buffer and

Food Sci. Technol, Campinas,      Ahead of Print, 2020 3/7 3

 Lactic acid bacteria sampled from dadiah as potential probiotic

(Table 1). According to Suryono (2003), a good quality dadiah 400× (Figure 2). Gram-positive, catalase-negative, cocci, and
contains more than 106-108 CFU/g of LAB. According to the rod-shaped LAB were defined and tested for growth at different
FAO/WHO (Food and Agriculture Organization of the United temperatures (15o C and 45o C) (Bostan et al., 2017)
Nations, 2001), dadiah as a probiotic food should contain
106-108 CFU/g of LAB (Table 3). 3.3 Biochemical properties
This study has compared LAB research on kefir produced The results showed no presence of bubbles in the Durham
from fresh milk’s fermentation by adding kefir grains as carrier tubes placed in broth inoculated with the LAB to confirm
ingredients for probiotic organisms with an indigenous source its homofermentative characteristic. The genus Lactobacillus
of LAB. It suggests that kefir can be used for fortification with consists of 70 species that are grouped into three subgroups,
probiotics. The population of bacteria in kefir ranged between mostly homofermentative or heterofermentative. In general,
6.4x104 and 8.5x108 CFU/g (Mitra & Ghosh, 2020). Others, shown Lactobacillus is resistant to acids compared to other LAB.
the color From the catalase assay, it was obtained that the LAB isolate
in this study does not produce catalase. Ibrahim et al. (2015)
3.2 Morphology identification reported about LAB identification from mango had a negative
result in catalase assay, which means that LAB do not produce
From the gram staining, LAB from dadiah showed the
the catalase enzyme to transform hydrogen peroxide into water
rod-shaped Gram-positive bacteria. According to Purwati et al.
and oxygen. It also indicates that LAB need only slight oxygen
(2017), the LAB in dadiah could be cocci or bacilli. The result
to live. LAB  constitutes a diverse group of Gram-positive,
was observed under the microscope with a magnification of
catalase-negative bacteria that produce lactic acid as the primary
end- product of carbohydrate fermentation (Table 4).
Table 3. Macroscopic identification.
Size Total LAB Count 3.4 Acid resistance assay
Sample Color Shape Surface
(mm) (CFU/ml)
Bron et al. (2004) explained that probiotic bacteria is exposed
White- Smooth, to the stomach acidity when consumed. Hence acid resistance
Dadiah Round 1.8 7.1 × 1010 CFU/mL.
beige convex
assay was performed on dadiah LAB at pH 4 and 3. The number

Figure 2. Gram staining of lactic acid bacteria.

4 4/7 Food Sci. Technol, Campinas,      Ahead of Print, 2020

 Amelia et al.

of colonies that grew on the control was higher (7 × 108 CFU/L 14 mm and 14 mm for C. albicans, S. typhi, S. sonei, S. Aureus,
than the pH 3 (4 × 108 CFU/ml), with a survival rate of 57.1% and E. coli (Açik et al., 2020).
(Table 5). The viability value varies depending on the type of bacteria
that survive at a low pH and depending on the bacterial strain. 3.7 Molecular identification by 16S rRNA Methods
The results of PCR sequencing are presented in Figure 3
3.5 Bile salt resistance assay below. The results indicate that the amplified DNA was 1540 bp
In addition to acid resistance, LAB resistance to bile salts is and the specific primer used in this study was able to identify the
required by probiotics. The 0.5% concentration is high enough to bacteria. The 16S rRNA gene is universally distributed and has
select a strain that is resistant to bile salts (Gilliland & Walker, 1990). a rational measure for sequence analysis (Vaughan et al., 2000).
The results showed 24 × 108 CFU of cell count in control and Based on the PCR results and BLAST analysis, the isolated
reduced to 16 × 108 CFU after 0.5% bile salts addition, so the bacteria from dadiah had 99.99% similarity with L. fermentum
LAB viability was 66.7% (Table 5). (Figure 4). A study by Syukur & Fachrial (2014) obtained the

3.6 Antimicrobial activity

The results showed that the widest inhibition zone was
observed with E. coli (23.28 mm), followed by L. monocytogenes
(12.12 mm), and then S. aureus (7.63 mm). The results of this
study have a higher inhibition zone than that of Syukur & Fachrial
(2014), where the dadiah from Solok had ±12 mm inhibition
zone against E. coli. Antimicrobial effect of the LAB from dadiah
against pathogenic bacteria showed significance.
The results showed that LAB from dadiah also had high
inhibitory effect on E. coli compared to kanamycin and
ampicillin (Table 6). Following Morales  et  al. (2003) study,
the zone of inhibition is grouped into four categories, weak
(<5 mm), medium (5-10 mm), strong (>10-20 mm), and very
strong (>20-30 mm). Thus, the dadiah LAB inhibition activity
towards E. coli is categorized as very strong. In another study,
L. acidophilus from fermented milk has been tested to have an
antimicrobial effect on bacteria such as E. coli and S. aureus
(Shafi et al., 2019). Potential LAB in Kefir grains obtained from
brown sugar promotes antimicrobial activity by developing a
halo zone of inhibition corresponding to 35 mm, 14 mm, 12 mm,

Table 4. Biochemical test of Dadiah.

Biochemical Test Result
Catalase Test Negative (−)
Type of Fermentation Homofermentative

Table 5. Acid resistance and bile salt resistance.

Resistance Test Control Viability
Acid Resistance 7 × 108 CFU 4 × 108 CFU
Bile Salt Resistance 24 × 108 CFU 16 × 108 CFU

Table 6. Antimicrobial activity of Dadiah LAB.

The Size of Clear Zone (mm)
Inhibitory
Source L.
E. coli O157 S. aureus
monocytogenes
Dadiah 23.28 7.63 12.12
Kanamycin 11.16 5.00 5.10
Ampicillin 13.68 10.15 7.63
Figure 3. PCR sequencing results (isolate 1).

Food Sci. Technol, Campinas,      Ahead of Print, 2020 5/7 5

 Lactic acid bacteria sampled from dadiah as potential probiotic

Figure 4. Phylogenic tree sample L in dadiah from Lintau Buo.

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