Effects of Initial Air Removal Methods on Microorganisms and Characteristics of Fermented Plant Beverages
The effects of 3 different methods for removing the initial air on the properties of fermented plant beverages produced from phom-nang seaweed (Gracilaria fisheri) and wild forest noni (Morinda coreia Ham.) were investigated. Only method M which covered the space above the fermentation liquid with a water filled plastic bag produced no surface film of yeast, had the highest acidity and also antibacterial activity from both plants after 90 days of fermentation. However, the yeast count still exceeded the standard guidelines for plant beverages. The fermented beverage from wild forest noni showed more antibacterial activity against 3 of 4 pathogenic bacteria tested than that from the phomnang seaweed, probably for its higher levels of acidity and ethanol content. Lactic Acid Bacteria (LAB) isolated from the fermentation samples from days 1-5 using the method M from both fermented plant beverages were Leuconostoc mesenteroides supsp. mesenteroides and Leu. mesenteroides subsp. dextranicum while presence of Lactobacilus plantarum was only recorded at days 4-5 in the wild forest noni beverage. From days 6-14 the isolates were Lactobacillus plantarum, Lactobacillus fermentum and Lactobacillus brevis from wild forest noni beverage, whereas only L. brevis was not detected in the seaweed beverage. During days 21-45 both beverages had a similar LAB population of L. plantarum and L. brevis while L. coryniformis was only found in the wild forest noni beverage. Between days 60-90 in both plant beverages only L. plantarum and Lactobacillius sp. were detected.
In Thailand, fermented plant beverages (FPB or FPBs),
produced from a variety of plants by Lactic Acid Bacteria (LAB), are considered
to be non-alcoholic and contain mainly organic acids, particularly lactic
acid (Kantachote et al., 2005a). Local Thai people who consume
the FPBs believe that they are healthy beverages for its high nutritional
value in addition to the presence of bioactive compounds derived not only
from the raw materials but also the fermentation process (Kantachote et
al., 2005b). However, variable amounts of ethanol and methanol were
detected in some FPBs (Kantachote et al., 2005a). Our previous
study demonstrated that some FPBs were able to inhibit some pathogenic
Gram-negative and Gram-positive bacteria. Their antibacterial activities
depended on total acidity, potassium ions and perhaps some bioactive compounds
extracted from the plants (unpublished data). Although there is not a
lot of scientific information available on these fermentation processes
these FPBs are still household products even though there are always serious
health problems with a high contamination by yeast cells (Prachyakij et
al., 2007). Therefore the beverage product cannot meet guidelines
of microbiological quality (yeast count: not more than 100 cfu mL-1)
based on the Section of Food Analysis, Division of Medical Science, Ministry
of Public Health, Thailand, even though these products are being produced
throughout the country.
Yeast and LAB can be found in fermented plants like pickles
or non alcoholic beverage because their habitats and some of their physiological
properties are similar (Osuntogun and Aboaba, 2004; Okada et al.,
2006). Under limited air conditions, both types of organisms are allowed
to grow as facultative anaerobes and most pickling processes use salt
to inhibit some yeast and spoilage microorganisms (Wood, 1985; Adams and
Moss, 2000). However, salt is not used in producing a fermented plant
beverage as it consists of plant material, sugar and water in a ratio
of 3:1:10 (W/W/V) (Kantachote et al., 2005a). This mixture of raw
materials is placed in a container to leave only a little space on top.
This means that the process of plant beverage fermentation provides suitable
conditions for both yeast and LAB although they favor LAB due to some
yeast preferring aerobic conditions and also their lower proliferation
than bacteria. The aim of this study was to investigate the effects of
initial air removal methods on plant beverage fermentation reactions focusing
on microbiological succession and the properties of the products.
MATERIALS AND METHODS
Preparation of plant beverage fermentation:
Fruit of wild forest noni (Morinda coreia
Ham) was selected for this study due to the fact that this tree is a medicinal
plant and that the fermented beverages from the fruit had the highest
activity to control enteropathogenic bacteria when compared to other medicinal
plants according to our previous study (unpublished data). In case of
phomnang seaweed (Gracilaria fisheri), it has been selected because
it is used as edible seaweed and its bioactive compounds is a subject
for many recent researches (Watanabe et al., 1990). Phomnang seaweed
and wild forest noni were purchased from local markets, sugarcane from
a supermarket and water was normal potable tap water. Unripe fruits of
wild forest noni were used in this study because ripe fruits have unpleasant
smell and it is likely to contain spoilage organisms. The effects of initial
air removal on the beverage fermentation process were tested as follows:
1) the traditional method (T) using a plastic bucket only 4/5 full and
a space under the lid, 2) the space above the fermentation liquid was
filled with a water filled plastic bag to make the fermentation virtually
anaerobic (M) and 3) a small gas release pipe was fitted into the lid
used to seal the bucket prepared as in T except for the sealed lid (N).
Each bucket (28 L) contained 6 kg of plant material, 2 kg of sugarcane
and 20 L of tap water. Three replicates were conducted in each treatment
and sampling occurred at days 0, 1, 2, 3, 4, 5, 6, 7, 14, 21, 30, 45,
60, 75 and 90 in order to monitor the characteristics of the FPBs and
microbiological succession. Plant are commonly fermented for 90 days prior
using as beverages due to people who prepare the beverages believe that
is a suitable time for drinking based on their taste and benefits to consumer`s
health. Some chemical properties and antagonistic activities of the FPBs
were also monitored.
Investigation of chemical property of FPBs:
The following chemical properties were examined for all
sampling times, using standard analytical methods (AOAC, 2002), pH, titratable
acidity and Total Acidity (TA) was calculated as lactic acid. Total Sugar
(TS) as glucose was also determined at all sampling times by the phenol
sulfuric method (Dubois et al., 1956). Elemental composition, some
organic compounds that could be involved with antibacterial activity and
the antibacterial activity were investigated at 0, 30, 60 and 90 days.
Elements (potassium: K and sodium: Na) were determined using inductively
coupled plasma-atomic emission spectroscopy (ICP-AES) according to the
instructions for the instrument. Organic acids, alcohols and acetaldehyde
were determined by gas chromatography as described by Yang and Choong
Determination of antagonistic activity of FPBs:
Antagonistic activity of FPBs was examined using
the cup well diffusion method (Schillinger and Lucke, 1989) with test
organisms Staphylococcus aureus PSSCMI 0004, Escherichia coli
PSSCMI 0001, Salmonella sp. PSSCMI 0002 and Vibrio parahaemolyticus
VP 4. The stock cultures were obtained from the Department of Microbiology,
Faculty of Science, Prince of Songkla University, Thailand. At least two
additional subcultures (24 h, 37°C) were did on fresh (TSA: tryptic
soy agar or TSA plus 2% NaCl for V. parahaemolyticus VP 4) plates
prior to use in the experiment. The turbidity of each actively growing
culture was adjusted to 0.5 (McFarland standard) and then swabbed over
the surface of a TSA. The FPBs were sterilized using 0.45 μm filter
and 125 μL of a fermented plant beverage was introduced into each
Microbial enumeration and isolation of LAB:
Standard methods using ten fold dilutions beginning
with 25 mL of each sample added to 225 mL normal saline solution to obtain
a 10-1 dilution and then appropriate dilutions were used for
the pour plate counting (FDA, 2001) of LAB and Total Bacterial Counts
(TBC). De Man Rogosa Shape (MRS) medium was used for LAB and Plate Count
Agar (PCA) for TBC. Potato Dextrose Agar (PDA) was used for counting molds
and yeasts by the spread plate technique. All plates were incubated at
room temperature (28±3°C) because fermentation buckets were
kept at room temperature. For each sample, representative colonies of
LAB were isolated from MRS medium based on their distinct morphology.
Pure cultures of each isolate that were Gram positive and catalase negative
were maintained on the same medium for further identification. In addition,
at the end of fermentation (90 days), the beverage yielded from all methods
(M, N and T) were visually inspected to check the presence or absence
of yeast film on the top of the beverage.
Identification of lactic acid bacteria in FPBs:
Only representative colonies isolated from the fermentation
method M were identified because this method seemed to be the most appropriate
method with which to persevere. Sixty representative isolates (30+30)
of LAB which collected at various fermentation times from the method M
of each FPB were identified. The identification of LAB was performed according
to morphological characters, arrangement of cells, biochemical tests as
well as physiological properties as described in Bergey`s Manual of Systematic
Bacteriology,(Kandler and Weiss, 1986) and Lactic Acid Bacteria (Axelsson,
2004). Gas production from glucose was tested for identification to genus
level in coccobacilli LAB. In order to identify to species level, carbohydrate
fermentation profiles of all isolates of coccobacilli LAB was conducted
in MRS fermentation broth where glucose was replaced by 2% (W/V) of one
of the following sugars (arabinose, fructose, galactose glucose, lactose,
maltose, mannitol, raffinose, ribose, sucrose and trehalose). In addition,
growth in 4 and 6% NaCl and hydrolysis of esculin were examined. The lactobacilli
were identified to species level by testing ability of gas production
from glucose utilization, ability to ferment the following 17 carbohydrate
compounds (arabinose, cellobiose, fructose, galactose, lactose, maltose,
mannitol, mannose, melezitose, raffinose, rhamnose, sorbitol, sucrose,
glucose, ribose, xylose and trehalose) were tested to identify bacilli
To analyze the effects of initial air removal on
the characteristics of a fermented plant beverage and their microbial
populations two ways ANOVA was used by the SPSS version 12 for Windows.
Means and Standard Deviation (SD) are presented. p-value results considered
as non significant (p>0.05) and significant p from 0.00 to 0.05.
Effect of initial air removal methods on characteristic of FPBs and
film yeast: Significant differences were observed in the chemical
properties and microbial populations among the beverages yielded from
the different fermentation processes carried out using different methods
of air removal (Table 1). For the fermented beverages
produced from phomnang seaweed, each fermentation method gave significant
differences for values of most of the monitored parameters (TA, TS, K,
acetic acid, lactic acid, ethanol, methanol, acetaldehyde, LAB and yeast),
but no significant difference was found for the following parameters:
Na, pH and TBC. For the fermented wild forest noni beverages all parameters,
except TS and K, were significantly different. At the end of fermentation
(90 days) potassium levels in each beverage produced from wild forest
noni (800-1000 mg L-1) were higher than in phomnang seaweed
(120-180 mg L-1), whereas the amounts of Na were similar in
the range of 20-30 mg L-1 in both FPBs. After 90 days of fermentation,
only the method M produced no film of yeast at the surface in both fermented
plant beverages (Fig. 1). Therefore as yeast is a non
preferred microbe, further results and discussion are focused on the results
obtained by the method M.
film yeast occurrence at the end of fermentation in traditional
method (T) for plant beverage fermentation and two modified methods
(water filled plastic bag to fill space under the lid (M) and small
air release pipe with sealed lid (N) to withdraw initial air at
the start of fermentation
of some chemical properties and microbial populations in fermented
beverage from phomnang seaweed and wild forest noni using 3 different
methods for removing air
S = Significance;
NS = Non Significance
Changes of chemical properties in FPBs: Amongst the 3 simple
fermentation methods used, method M gave the highest TA. Changes of pH,
TA and TS showed similar tendencies in both FPBs under the method M with
decreasing amounts of TS corresponding with increasing amounts of TA and
the TA values were inversely related to the pH values (Fig.
2a-b). In both FPBs, the initial TS (roughly 13%)
sharply decreased to about 9% after only 1 day of fermentation with a
corresponding decrease of pH from 6.1 to 3.9 in phomnang seaweed and from
4.1 to 3.5 in wild forest noni and then gradually decreased to around
3% TS at the end of fermentation (90 days). However, the increase in TA
of fermenting phomnang seaweed was slower than with wild forest noni and
at the end of fermentation, the former beverage had only 1.0% TA with
a pH of 2.7 and the latter beverage had 1.5% TA with a pH of 3.1.
Organic acids and alcohols in FPBs: Both FPBs under the method
M after 90 days of fermentation contained acetic acid, lactic acid, ethanol
and methanol (Fig. 3). The major products detected in
the phomnang seaweed beverage were lactic acid (3.9 g L-1)
and acetic acid (2.3 g L-1), with only a small amount of each
alcohol. The main product in the wild forest noni was ethanol (9.9 g L-1),
followed by acetic acid (3.7 g L-1), lactic acid (3.2 g L-1)
and methanol (2.3 g L-1). Acetaldehyde was also detected in
very small amounts in both FPBs (0.001 g L-1).
Antibacterial activities of FPBs against pathogenic bacteria:
Among the 3 simple methods of plant beverage fermentation,
both FPBs gave similar antibacterial activity results with the least activity
found in method T (control set) while the other 2 methods gave similar
results (data not shown). In addition, the maximum inhibition of
Changes of chemical
properties in fermenting plant beverages under a modified method
using a water filled plastic bag cover at the top of the liquid
Organic acids and
alcohols contents of fermented plant beverages after 90 days of
fermentation collected from the method M
of 125 μL of 90 days fermented plant beverages collected from
the method M
test organisms was found at day 90, hence only the results of the inhibition
obtained with method M at 90 days of fermentation are presented in Table
2. The zones of inhibition from the fermented wild forest noni beverage
were generally larger than from the fermented phomnang seaweed beverage
for test organisms S. aureus PSSCMI 0004, Salmonella sp.
PSSCMI 0002 and V. parahaemolyticus VP 4, but not E. coli
PSSCMI 0001. V. parahaemolyticus VP 4 was the most sensitive to
both FPBs (inhibition zone: 13.8-16 mm), followed by Salmonella
sp. PSSCMI 0002 (inhibition zone: 10-12 mm) and S. aureus PSSCMI
0004 (9-10 mm). E. coli PSSCMI 0001 was the least sensitive to
both FPBs and in this case the inhibitory effect of the phomnang beverage
(inhibition zone: 6.5 mm) was higher than for the wild forest noni (4.2
Changes of microbial populations in FPBs: Molds were not detected
in any sample of the plant beverages throughout the monitoring period.
The initial TBC of the fermented plant beverage using method M and phomnang
seaweed was about 1 log cfu mL-1 higher than with wild forest
noni (Fig. 4a-b). However, both FPBs
reached their maximum TBC at day 7, 7.3 log cfu mL-1 in the
phomnang seaweed and 8.6 log cfu mL-1 in the wild forest noni
beverage. In both situations TBC`s then declined over the 90 days to 4.2
log cfu mL-1 for the phomnang seaweed and 4.6 log cfu mL-1
for the wild forest noni. No yeasts were detected in either preparation
at the start of the fermentation but increased until day 7 to between
7-7.3 log cfu mL-1 then sharply decreased to between 2.5-2.8
log cfu mL-1 at the end of fermentation (Fig.
4a, b). There were significant differences between
the growth of LAB in the 2 preparations. In the phomnang seaweed beverage
LAB increased slowly to about 2.5 log cfu mL-1 until about
day 6 then rapidly to 6.2 log cfu mL-1 at about day 14 (Fig.
4a). With the wild forest noni preparation, growth of LAB mirrored
the TBC reaching a maximum of 8.7 log cfu mL-1 during days
6-7 (Fig. 4b). In both cases populations of LAB`s then
declined until the end of fermentation to 3.7 and 4.5 log cfu mL-1,
respectively (Fig. 4a, b).
Identification of the dominant LAB in FPBs:
As LAB were the most abundant microorganisms detected
during the fermentation their activities probably play the most
changes in fermented plant beverages using a modified method with
a water filled plastic bag placed at the top of the liquid
important role in the characteristics of the fermented beverages. It
was of interest to identify the LAB species present during the fermentation
processes to establish if there was any correlation between the characteristics
of the beverages and the identity of the LAB. During the early stages
of fermentation, in both FPBs Leu. mesenteroides subsp. mesenteroides
and Leu. mesenteroides subsp. dextranicum were the main
species detected. However, at days 4-5 in the wild forest noni fermentation
the LAB had changed from cocci to rods with Lactobacillus plantarum
and Lactobacillus sp. predominating (Table 3).
Lactobacillus fermentum was present at days 6-7 of the fermented
wild forest noni beverage and later at day 14 in the phomnang seaweed
preparation, in which L. plantarum had predominated at days 6-7.
During days 14-45, similar species of lactobacilli (i.e., L. brevis,
L. plantarum and Lactobacillus sp.) were detected in both FPBs,
except that L. coryniformis was found only in the wild forest noni
fermentation at day 21. During days 60-90, Lactobacillus
sp. and L. plantarum were the only LAB found in both fermented
of lactic acid bacteria isolated from the method M in beverages
of phomnang seaweed and wild forest noni at varying days of fermentation
Effect of initial air removal on the characteristics of FPBs and film
yeast: In order to establish the most appropriate method to produce
fermented plant beverages that might assist local communities, tests were
conducted and comparisons made between the traditional method (control
set) and two simple modified methods. The most significant result was
that one method, M, produced no surface film yeast whereas there were
plenty of film yeast in the other two methods. The method M, allowed for
the immediate removal of oxygen and retention of CO2 produced
by heterofermentative LAB (Table 3), providing conditions,
long known to prevent the growth of film yeast (Wood, 1985; Jay, 2000)
and stimulate the growth of many lactobacilli that produce a high TA (Table
3, Fig. 2a, b). In the 3 different methods used for the phomnang seaweed
beverage fermentation, TBC were not significantly different and as a consequence
neither was the pH. Also in these cases, bacteria other than LAB were
the predominant bacterial population although obviously some LAB would
grow with PCA (Fig. 4a). In contrast with the wild forest noni fermentation,
the only non significant differences between the 3 processes were with
the K and TS levels. The K content is obviously derived from the plant
tissue and does not undergo microbial induced transformations.
Effect of microbes on the chemical properties of FPBs:
Both plant fermentation processes using method M
were initiated by Leu. mesenteroides supsp. mesenteroides
and Leu. mesenteroides supsp. dextranicum (Table 3). Leuconostoc
species are obligate heterofermentative cocci that can tolerate fairly
high concentrations of sugar (up to 50%) (Battcock and Azam-Ali, 1998;
Okada et al., 2006), therefore they grew well in the plant beverage
fermentation which had an initial TS of about 13% (Fig. 2a, b). Heterofermenting
LAB metabolize glucose via the 6-phosphogluconate/phosphoketolase pathway.
They produced carbon dioxide and acids (lactic acid and acetic acid) which
rapidly lower the pH; however, they do not tolerate high acidity (Axelsson,
2004; Bergqvist et al., 2005) so they were detected only during
the initial stages of fermentation (days 1-5). After the initial rapid
removal of TS to about 8% that occurred over the first few days Lactobacillus
fermentum, L. brevis and L. plantarum became the dominant LAB.
Both L. fermentum and L. brevis are also obligate heterofermenters
(Hammes and Vogel, 1995; Battcock and Azam-Ali, 1998) and they produce
intermediate amounts of acid. Interestingly, the facultative heterofermenters
such as L. plantarum were detected from day 5 until the end of
the fermentation and it was among the most lactobacilli in both FPBs.
Hence, it would be useful to use this bacterium as a starter culture as
it can utilize sugar by either the Embden-Meyerhof pathway or phosphoketolase
pathway depending on the conditions of growth (Hammes and Vogel, 1995).
Normal conditions required for the glycolytic pathway by lactic acid bacteria
are excess sugar and limited oxygen (Battcock and Azam-Ali, 1998; Jay,
2000). Another facultative heterofermenter (L. coryniformis) was
found only in the wild forest noni fermentation (Table 3). Similar observations
on microbial succession have been made with sauerkraut fermentations (Wood,
1985; Jay, 2000). It has long been recognized that Lactobacillus spp.
are the most frequently detected in fermented vegetables (McDonald et
al., 1990; Djeghri-Hocine et al., 2007) and it is normally
detected at later stages of many vegetable fermentations prevail over
that of Leu. mesenteroides due to its higher acid tolerance (McDonald
et al., 1990; Battcock and Azam-Ali, 1998).
As similar species of LAB were found in both plant beverage
fermentations, the changes of pH, TS and TA were also similar. However,
the amount of TA in the beverage produced from the wild forest noni was
higher than from the phomnang seaweed (Fig. 2a, b). This may be caused
by higher amount of LAB in the former beverage (Fig. 4a, b). Higher amounts
of ethanol (1%) are also found in the wild forest noni beverage perhaps
due to there being roughly 0.5-1 log more yeast cfu mL-1 during
the whole fermentation period (Fig. 3, Fig. 4a, b). Therefore to reduce
the amount of yeast in the finished product, it may be necessary to provide
an inoculum do so. A small amount of methanol (0.25%) was also detected
in the wild forest noni beverage because unripe fruits were used and their
pectin was probably being modified by a pectin methylesterase that cleaved
methoxyl groups and produced methanol, poly-garacturonate and H+
(Whittaker, 1990; Moat and Foster, 1995).
Effect of FPBs on antibacterial activity:
The sensitivity of the test bacteria to both FPB`s
which collected from the method M was V. parahaemolyticus VP 4>
Salmonella sp. PSSCMI 0002> S. aureus PSSCMI 0004 and
E. coli PSSCMI 0001 and the fermented wild forest noni beverage
gave a stronger inhibition to all test organisms, except E. coli
PSSCMI 0001, than did the phomnang seaweed beverage (Table 2). Fermented
wild forest noni beverage as stated earlier contained higher levels of
TA, acetic acid, ethanol, methanol and potassium (Fig. 2a, b, 3). The
results indicate that inhibition of the food borne pathogenic bacteria
by FPBs was mainly dependent on the amounts of organic acids and alcohols
(Fig. 3, Table 2) although the amount of alcohols was very low in the
beverage of phomnang seaweed. Therefore, no doubt that the phomnang seaweed
beverage had antibacterial activity less than that found in the wild forest
noni beverage. Many research reports have concluded that inhibition of
some enteropathogens was mainly dependent on organic acids and antibiotic-like
substances (Gonzales et al., 1993; Ivanova et al., 2000;
Soomro et al., 2002; Cadirci and Citak, 2005). However, in this
study alcohols showed a synergistic inhibitory action with the organic
acids and this is expected as the alcohols actually can act as disinfectants
(Pelczar et al., 1986). In addition, it is possible that alcohols
may help to extract some bioactive compounds from the fruit of wild forest
noni. The 6 times higher amount of K in fermented beverage produced from
wild forest noni than in phomnang seaweed might also assist in the antibacterial
activities. A similar result was found by Stella and Burgos (2001) who
reported that potassium ion increased the susceptibility of Saccharomyces
cerevisiae strain S288c to fluconazole. In contrast, E. coli
PSSCMI 0001 seemed to be more sensitive to fermented phomnang seaweed
beverage than fermented wild forest noni even though it had lower levels
of those compounds. It means that E. coli PSSCMI 0001 was sensitive
to some extracted compounds from phomnang seaweed or some bioactive compounds
from indigenous LAB in phomnang seaweed fermentation. The results are
supported by Chung and Yousef (2005) who demonstrated that Lactobacillus
curvatus isolated from a fermented food produced a bacteriocin-like
agent against Salmonella enterica serovar Enteritidis
and E. coli 0157: H7. On the other hand, the seaweed itself may
contain some compounds that inhibited E. coli PSSCMI 0001.
To conclude, the present study highlights the possibility
to prevent film yeast, it is necessary to immediately remove air at the
start of the plant beverage fermentation process. Over the 90 days of
natural fermentation the numbers of yeast exceeded standard guideline
for plant beverage although the amounts of LAB were higher than yeast.
Therefore, the use of a selected LAB inoculant may be necessary to meet
the standard guideline and it is currently conducted. Antibacterial activity
increased with increasing fermentation time and antibacterial activities
of FPBs mainly related to their organic acids and alcohols contents.
The authors gratefully acknowledged National Science
and Technology Development Agency (NSTDA), Thailand for providing funding
for this work (CO-B-22-2C-18-601. Dr. Brian Hodgson was gratefully acknowledged
for his critical reading.
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