Kimchi fermentation and characteristics of the related lactic acid bacteria

Kimchi fermentation and characteristics of the related lactic acid bacteria
Mheen, Tae Ick
Korea Institute of Science and TechnologyInformation
Ⅰ. Introduction
Kimchi is a Korean fermented vegetable food that are salted, blended with
various ingredients and fermented for a certain period of time at ambient
temperature. The characteristics of kimchi differ depending on the varieties of
kimchi. The varieties are due to the raw materials used, processing methods,
seasons, localities and functional properties of kimchi. More than 200 kinds of
kimchi are available in Korea, but kimchi can be classified as two major groups,
ordinary and mul-kimchi. Ordinary kimchi without added water includes
baechu kimchi (diced Chinese cabbage), tongbaechu kimchi (whole Chinese
cabbage), yeolmoo kimchi (young oriental radish) and kakdugi (cubed radish
kimchi). Mul-kimchi includes baik kimchi (baechu kimchi with water), dongchimi
(whole radish kimchi with water) and nabak kimchi (cut radish and Chinese
cabbage). 1)
The raw materials used for kimchi preparation are divided into three groups,
major, sub-ingredients (spices) and optional ingredients. A recipe for the
simplest kimchi may include cabbage 100 g, garlic 2 g, red pepper powder 2 g,
green onion 2 g, ginger 0.5 g, with optimum salt content of 2-3%.2)
The optimum pH for the best taste of kimchi is 4.2-4.5 and the optimum
acidity is 0.6-0.8% as lactic acid. The best taste is attained after 2-3 days of
fermentation at 20℃ with 2-3% salt. Kimchi has a unique sour, sweet,
carbonated taste and usually is served cold. Also, kimchi contains a lot of live
lactic acid bacteria (LAB). In this respect, kimchi differs from western
sauerkraut and Japanese asatsuke, and the former is only acidic in taste and
served warm, and latter is not a fermented product and has few live LAB.
Total amount of kimchi production is estimated to 1,500,000 M/T in 2000 and
one fourth of total consumption of kimchi was commercially produced in the
same year. According to a national survey, an adult consumes 50-100 g/day of
kimchi in summer and 150-200 g/day in winter.2)
During the last 50 years, many genus and species of bacteria, yeasts, and
fungi has been isolated and reported from kimchi samples, but it was confirmed
that major microorganisms responsible for kimchi fermentation are LAB and
yeasts are known to be role for softening of kimchi texture and off-flavor. The
major genus and species of LAB isolated and identified from kimchis are
Leuconostoc mesenteroides, Leuconostoc dextranicum, Leuconostoc citreum,
Lactobacillus brevis, Lactobacillus fermentum, Lactobacillus plantarum, Pediococcus
- 1 -
pentosaceus, and Streptococcus faeculis.1-3)
The sugars in raw materials are converted to lactic acid, acetic acid, carbon
dioxide and ethanol by hetero fermentative LAB during kimchi ripening, and
these acids and carbon dioxide are responsible for the fresh and carbonated
taste of kimchi. However, after a certain period of time, excessive lactic acids are
formed and off flavors are developed due to the growth of homo fermentative
LAB and yeasts. 1,2)
The total number of kimchi microorganisms reaches its maximum level
(1x108-9 cells/ml) at optimum-ripening time and after then number of
nd
microorganisms decrease slowly and again increase and maintains 2
6-7
maximum level (1x10 cells/ml) as kimchi fermentation carried. In the kimchi
fermentation system, it seems clear that hetero fermentative LAB producing
organic acids and carbon dioxide from sugars are major species in the early
stage of fermentation, and homo fermentative LAB producing excessive lactic
acid are major species in the late stage of fermentation.2)
It was also confirmed that low salt concentration and low temperature (eg,
2% and 10o C) favor growth of hetero fermentative LAB, while high salt
concentration and high temperature (eg, 3.5% and 30oC) favor growth of homo
fermentative LAB. Therefore, salt concentration and temperature are the most
important key factors for controlling kimchi fermentation.2)
Besides the two key factors for controlling kimchi fermentation, many other
factors such as raw materials used, processing methods, addition of natural
preservatives and starters affecting kimchi fermentation and preservation has
been reported in previous reviews and books.1-6)
In this article, the factors affecting kimchi fermentation, microbial and
chemical changes during kimchi fermentation, and some characteristics of LAB
from kimchi will be reviewed.
Ⅱ. Factors affectingon kimchi fermentation
Kimchi fermentation occurs mainly by the microorganisms naturally present
in the raw materials that contain numerous microflora including LAB. Various
LAB may initiate fermentation, but hetero fermentative type LAB increased
rapidly with organic acids accumulation and homo fermentative type LAB
increased thereafter. Numerous chemical, physical, and biological factors may
contribute directly to the growth of microorganisms and the extent of
fermentation.
The important factors that affect kimchi fermentation are microorganisms,
temperature,salt concentration, fermentable carbohydrates, other available
nutrients, or any inhibitory compounds in raw materials used, as well as
oxygen and pH. In this chapter, the salts, temperature, raw materials, natural
preservatives and selected starter cultures related to the kimchi fermentation
- 2 -
will be discussed in detail.
1. Salts
Salt is one of the key factors for controlling the kimchi fermentation and
preservation of good quality of kimchi at various temperatures. There are more
than 200 kinds of kimchi available in Korea.However, salt concentrations of
those kimchi are all different depending on the makers. A flow-chart for
processing baechu kimchi is shown in Fig. 1.
Prior to kimchi preparation the major raw materials such as Chinese
cabbages and radishes may be salted with either salt solution or dry salt and
washed with clean water. This treatment is the most important step for
fermentation and maintenance of kimchi quality. It was reported that the
optimum salt concentration of kimchi is about 2.0-3.0%, while acceptable level is
2)
individually determined by housewive's experiences. Therefore, it is necessary
to optimize the salting condition. Of two types of salting methods, direct
addition method is widely used conventionally at household level, but this
method has the disadvantage of difficulty in control of the final salt content of
kimchi. Brine method is more preferable for the commercial production of
kimchi. Satisfactory quality of kimchi could be obtained when cabbages are
salted for 3-6 hours using 15% salt solution. 2,7)
Salting is carried out over a wide range of time from 3 to 15 hr depending on
the salt concentration, temperature, varieties, and cutting way and size of
cabbages. For baechukimchi, the final salt concentration is adjusted to 2.0 - 3.0%
of the overall ingredients, and this concentration is the best for optimum
fermentation. This concentration is maintained during fermentation and
preservation. If the salt concentration is below the optimum concentration,
fermentation proceeds too fast and frequently causes quick acidification and
softening. On the other hand, color and flavors are not acceptable when the salt
concentration is over 6%.2) Depending on the salting time, free sugars and
amino acids were reduced in raw cabbages and texture, chemical and physical
7-10)
properties, and total microflora have been changed during salting.
Generally, salting reduces the moisture content (10-12%), relative volume,
and weight, as well as theinternal void space of the cabbage. These changes
affect the physical properties of the vegetable, especially the flexibility and
firmness of the tissue, which give a typical textural property to the final
product.As a result of brining, the total microorganisms, such as aerobic counts
in salted cabbage are reduced (11-87%) and LAB are increased (3-4 times), and
reducing sugars also decreased (7-17%) .7,11 )
Washing conditions in salted cabbage on the quality of kimchi is also
important for the retention of quality of characteristics.12) Chinese cabbage
treated with1000 ppm solution of grapefruit seed extracts or citric acid at 10oC
- 3 -
showed a retarded increase in titratable acidity and decrease in pH and
reducing sugar content.12), and kimchi made from Chinese cabbage soaked in a
heated 10% salt solution at 40oC has improved quality and shelf-life of kimchi.13)
Fig. 2 shows the effect of salt concentration and temperature on acid
production during kimchi fermentation. Total acid was more at lower salt
content (2.25%) than high concentration of salt at any temperature tested. At the
lower salt content, maximum acidity was reached in a shorter period. At 30oC
and 2.25-3.5% salt content, acidity of kimchi was maintained in the same pattern
throughout. The acidity of 1.55% was reached in 5 days and maintained at 1.6%
thereafter, but at 5.0 and 7.0% salt content, acidity reached 1.4 and 1.1% after 5
and 6 days, respectively.
Recently, to examine the quality of mul-kimchi, the temperature (4, 15, and
o
25 C for 10 days) and salt concentration (0, 0.2, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0%) in
water was conducted, and found that the pH was lowest and acidity was
14)
highest in the mul-kimchi containing 1.0% salt.
Effect of salt concentration on dongchimi (ponytail Chinese radish kimchi)
fermentation was also studied15) Diced Chinese radishes were fermented at 4oC
with salt concentration of 1.5- 6.3%. The pH level reduced during the
fermentation, while the total acid content of dongchimi increased and the salt
concentration of dongchimi liquid decreased. Equilibrium for salt concentration
between dongchimi liquid and solid radish was achieved after fermentation of
15-22 days.
2. Temperature
The most important factor affecting kimchi fermentation is temperature,
since the kimchi fermentation occurs mainly by the microorganisms naturally
present in raw materials. Kimchi is now available in all year round but the
quality of kimchi differs depending on localities and seasons. Ambient
temperature is applied for making kimchi at household level. Kimchi
fermentation and over-acidification occurs simultaneously at ambient
temperature.
Fig. 3 shows the changes of pH and total acids during kimchi fermentation at
various temperatures. Ripening time of kimchi depending on fermentation
temperature, accordingly the changes in pH and acidity, showed notable
o
differences. At 20 C, pH dropped sharply with increasing acidity, but pH and
acidity at 10oC changed more slowly compare with high temperature tested.
Maximum total acid produced in kimchi at 20oC and 15oC is 1.6%, but it never
exceeds total acidity of 1.2% at 10oC. As a result of panel test, it was evaluated
that the pH and acidity of optimum ripening period of kimchi were 4.2 and
0.6% (as lactic acid), respectively.16)
The optimum-ripening time and the edible period of kimchi varied
- 4 -
depending upon the fermentation temperature and salt content as shown in
Table 1. At 30oC, the optimum-ripening period was 1 day and the edible period
was also 1-2 days. But at lower temperature, the optimum ripening time and the
edible period were longer than those of at higher temperature. At 5oC and
above 5.0% salt content, kimchi was ripened very slowly and at 7.0% salt
16)
content it was not ripened even after 180 days fermentation．
Chemical changes, LAB and yeast counts in kimchi prepared by commercial
manufacturer in large scale were monitored at different fermentation
temperature．17) It has been confirmed that the optimum pH of kimchi was
o
o
o
around 4.2 and reached within 2 days at 25 C, 3 days at 15 C, and 23 days at 5 C
17)
fermentation, respectively．
In order to investigate the fermentation characteristics of kimchi which was
made at
12oC and fermented at 17oC and 4oC, the pH, total acid, total microorganisms,
LAB, dissolved carbon dioxide content, reducing sugars and temperature at the
center of a kimchi jar were studied．The pH and the total acid content of
kimchi that was fermented at 17oC for 4 days were almost the same as those of
kimchi fermented at 4 oC for 48 days. The total cell counts of microorganisms
o
o
and LAB in kimchis which were fermented at 17 C for 2 days and 4 C for 9 days
9
8
8
7
were 1.5x 10 and 6.3x10 cells/ml, and 2.0x10 and 8.7x10 cell/ml, respectivel
y． The results showed that it took 23 and 35 hr, respectively, to reach the
temperature of 17oC and 4oCat the center of a jar during bulk fermentation of
kimchi from the fermentation of initial temperature of 12oC．18)
The effects of fermentation temperature (0-15oC) and salt concentration (1.5,
2.75, 4.0%) on fermentation parameters of kimchi were also analyzed by
response surface methodology． pH decreased and acidity increased with
increasing fermentation time, reduction and incremental rates were increased
as temperature increased and salt concentration decreased. The optimum pH
of 4.2 was achieved within 14-24 days at 5-15oC, but at 5oC, pH was still >4.2
after 24 days. Maximum edible acidity (0.75%) was reached within 8 days at
o
o
15 C, but at 0 C, acidity was only 0.35-0.43% after 24 days of fermentation.
Edible periodsfor kimchi, based on the acidity range 0.4-0.75%, were 4, 10, and
18 days for the fermentation at 15, 10, and 5o C, respectively, with 2.75% NaCl．
19)
Differences in quality characteristics such as pH, acidity, reducing sugar
content, microbial counts and sensory properties between whole Chinese
cabbage kimchi (pogi kimchi) and sliced Chinese cabbage kimchi (mat kimchi)
were examined during the fermentation at 20 oC for 10 days and 5 oC for 50
days. Pogikimchi showed delayed fermentation of approximately 2 days at 20 oC
and 10 days at 5 oC than mat kimchi. Ordor, color and flavor scores of kimchi
were higher in the samples fermented at 20 oC than those fermented at 5 oC,also
there were no great differences between sensory properties of pogi and mat
- 5 -
kimchi. Gas composition of the packages containing the kimchi fermented at 20
C showed increased CO2 concentration and decreased O2concentration after 3
days for both kimchi varieties.20)
The effect of fermentation temperature on the sensory, physicochemical and
microbiological properties of kakdugi(cubed radish kimchi) and on free sugar,
organic acid and volatile compound levels in kakdugi during fermentation was
also investigated． 21-22) After the initial fermentation for 12, 24 and 36 hr at 20
o
C, kakdugi was fermented for 57 days at either 4 oC, 10 oC or 20 oC, respectively.
The pH was decreased to the range of 4.1~4.3 from the initial pH 5.8, and
total acidity was increased 2~4times than that of in the initial period (0.24%).
The number of LAB was remarkably increased in palatable period and was
gradually decreased thereafter.21)
Free sugar levels decreased at each temperature during fermentation (with
the exception of mannitol, levels of which increased) although decreases were
o
less marked in samples fermented at 4 C. Of the organic acids tested, lactic acid
production was the most pronounced, increasing substantially with time and
temperature. In contrast malic acid, which was the most abundant organic acid
initially, decreased in concentration during fermentation, and this decrease was
most pronounced at higher temperature.
Levels of the volatile compound, methyl allyl sulfide, were initially very low,
but increased dramatically up to approximately 45 days after which levels
decreased. The increase corresponded to the increased aroma in sensory
evaluations. These results suggest that fermentation at 4oC, following an initial
o
fermentation at 20 C for 36 hr, is suitable for the production of good quality
kakdugi with high free sugar and organic acid contents.22)
Recently, the characteristics of natural lactic acid fermentation of radish juice
were investigated at different salt concentration (0-2%) and temperature
(10-30oC) with aview of low salt kimchi (a kind of water kimchi). It was found
that LAB isolated from radish juice fermented at 2% salt concentration was
mainly Leu. mesenteroides, Lac. plantarum and Lac. brevis.Growth rate of LAB
increased with increasing temperature at 1% salt concentration and LAB were
o
still active at 10 C. The time to reach pH 4.0 during the fermentation of juice
containing 1% salt was 11~13 days at 10oC and 2~3 days at 30oC.23)
o
3. Raw materials
Kimchi, a fermented vegetable food with various sub-ingredients (spices),
has been the most popular side dish that is served with cooked rice for
hundreds of years in Korea. In total, there are about 200 kinds of kimchi, whose
raw materials are mainly Chinese cabbages and radishes. Dried red pepper
powder, garlic, green onion and ginger are the widely used seasonings. The
types and amounts of seasonings used in kimchi vary greatly between
- 6 -
manufacturers and processors. Therefore, the quality and species of major
ingredients may significantly affect fermentation and the product characteristics
of kimchi.
The important raw materials of kimchi are divided into three groups such as
the majorraw materials, sub-ingredients (spices) or fermented fishery products,
and optional (minor) ingredients.
As seen in Table 2, baechu (Chinese cabbages) are the most common majorraw
materials for preparing kimchi and radishes are other raw materials for kakdugi
(cubed radish kimchi) and dongchimi (whole radish kimchi with water)
preparation. Cabbages, whole radish, cucumber, mustard leaves, green onion,
and leeks that are available in various seasons and localities are the raw
materials for making special kimchi in Korea.
The sub-ingredientsinclude garlic, hot pepper powder, green onion, ginger
and fermented fishery products such as shrimp and anchovy. The optional
(minor) raw materials include leek, parsley,glue plant, mustard leaves, pear,
chest nut, oyster, frozen pollack, starches, monosodium glutamate (MSG),
andsweetener. One of the important criteria for making good taste of kimchi is
the selection of good quality of raw materials, and the next is the good
formulation of kimchi ingredients and seasonings.
Table 3 shows the basic ingredients for making baechu kimchi, kakdugi,
dongchimi, and other mul-kimchi (water-kimch, but the simplest kimchi recipe
includes salted cabbages 100 g, hot pepper powder 2 g, garlic 1.5 g, green onion
2 g, ginger 0.5 g and final salt concentration of 2-3%.16)
Generally softer texture and higher sugar content of vegetables are more
desirablefor making good quality and taste of kimchi than harder texture and
lower sugar content. However, harden texture ofvegetables are more favorable
2)
for long-term preservation without softening.
Among the many kind of kimchi, baechu kimchi has been consumed for a long
time as a traditional fermented vegetable food in Korea. The ingredients
involved in baechu kimchi preparation, such as red pepper, garlic, ginger, green
onion, leek, fermented shrimp or anchovy, sugar, etc., affect the kimchi
fermentation rate differing with kinds and amounts of ingredients. Effects of
raw materials and ingredients on kimchi fermentation have been extensively
25,29-32)
studied.
Besides the temperature and salt concentration, types of kimchi are also the
factors for controlling kimchi fermentation. Therefore, three main types of
Chinese cabbage kimchi, baechu kimchi and tongbaechu kimchi (semi-solid types
of the cabbage kimchi prepared with a large amount of hot pepper powder and
a small amount of water) and baek kimchi (a liquidtype of kimchi prepared with
a small amount of hot pepper powder and a large amount of water), were
selected as models to compare fermentation characteristics of kimchi. In this
result, the amount of hot pepper powder and water are believed to be the
- 7 -
primary (or external) and the secondary (or internal) factors, respectively, those
affect and control kimchi fermentation.33)
The difference of qualitative characteristics between whole Chinese cabbage
kimchi (pogi kimchi) and sliced Chinese cabbage kimchi (mat kimchi) was
o
o
examined during the fermentation at 20 C and 5 C. Pogi kimchi showed a
delayed fermentation about 2 days at 20oC and 10 days at 5oC.20)
The growth of microorganisms could be controlled by theappropriate
addition of raw materials. Among the sub-ingredients, radishes,34) hot pepper
powder,29-32) fermented anchovy and shrimp,35-38) starches,35,39) reducing
31,40)
soluble solids,41) and protein sources42) have been probed their
sugar,
accelerated effect on kimchi fermentation, but garlic and leek has showed
delayed effect,29-31,43,44)and green onion and ginger had controversial effect on
kimchi fermentation.30-32) On the other hand, mustard or leaf mustard,45) and
extracts of leek44) were known to delay the fermentation period of kimchi.
Additionof dried methanol extracts of radish stimulated the growth of LAB,
especially Lac. fermentum, Lac. leichmannii, Lac. sake, and Lac. brevis.34)
The composition of pigments in hot pepper consists of 40 different
carotenoids with capsanthin and capsorubin as a major carotenoid and
carotenes as provitamin A. The average amount of hot pepper added to kimchi
was found to be 2.24% with frequency of use of 97.3%. In spite of the fact that
hot pepper was reported to promote the fermentation of kimchi, it did not show
any significant increase in sour taste and did not affect sweet, salty, palatable
and crispy tastes.31)
Garlic is used most frequently as a sub-ingredient (100%) in kimchi. Since
ground garlic is used in kimchi-making, alliin is changed to allicin with an
intensive taste. This allicin takes part in the desirable fermentation of kimchi by
inhibiting the growth of various unnecessary microorganisms derived from
sub-ingredients in the initial fermentation period and to delay the fermentation
of kimchi. Garlic improves storage capacity by prolonging fermentation period
by LAB and is beneficial to less acidification.29,30,32,43,46)With fermentation of
kimchi, the intensive hot taste of garlic was slowly changed to the harmonized
31)
taste and flavor.
Green onion and leek contain various allyl sulfides, carotenes and vitamin C.
The frequency of use in the general cabbage kimchi was 72.8% for green onion
and 32.4% for leek, which both are much lower compared with that of 97.3% for
hot pepper and 100% for garlic. The amounts of green onion and leek used for
kimchi making are still high, ie, 0.6-0.9% for green onion and 2.0-6.0% for
leek.Recently, it has been reported that leek could retard the fermentation of
kimchi because of its antimicrobial activity.44)
Ginger contains unique components like citral and linalol, and hot taste
components such as gingerone and shogaol. Ginger caused a delay in
fermentation and there were no significant differences in the sour, sweet, salty,
- 8 -
hot, palatable, unpleasant and overall tastes, acidic odor and color between the
kimchi fermented with and without ginger.30,31)
Fermented anchovy and shrimp contain a lot of proteins and amino acids,
and have their own unique taste and flavor. Therefore, those sub-ingredients
would affectnot only the nutritional balance but also the improvement of the
sensory quality of kimchi. These fermented fish products and other protein
sources such as skim milk, soy protein isolate, beef extract, and fish protein
produced high lactic acid and promoted the growth of LAB.37,38,42)
The frequency of addition of starch and sugar in kimchi making was 27%
with a concentration of 0.4-3.0%, and sugar was used for sweet and harmonized
tastes. However, since starch and sugar are utilized as a carbon source
byvarious microorganisms present in kimchi, they are expected to affect the
kimchi fermentation and sensory quality. In the results, starch and sugar
promote the fermentation of kimchi and contribute greatly to harmony of tastes
31,39)
by reducing the hot and overall tastes, and acidic and garlic odors.
Yulmoo, a young radish, is a vegetable that has been a major raw material of
kimchi just as much as Chinese cabbage. Compared with Chinese cabbage,
yulmoois chiefly cultivated in summer and thus is cheaper during this season.
Yulmoo kimchi is also different from baechu kimchi in that it requires less
seasoning. Owing to the use of various seasonings like red pepper powder and
fermented fish products, Chinese cabbage kimchi is more expensive and at the
same time more prone to turn sour than yulmoo kimchi in summer. Therefore,
yulmookimchi would not only taste better but also be economical during
summer. To evaluate the effect of starch on yulmookimchi fermentation wheat
flour was used as starch source and compared with glutinous rice. It was found
that both wheat flour and glutinous rice flour hastened the fermentation of
39)
yulmoo kimchi.
4. Natural preservatives
The groups of LAB involved in kimchi fermentation continuously produce
organic acids after theoptimum ripening, and cause changes in the composition
of kimchi. These changes are called the over-ripening or acid-deteriorationof
kimchi, which is often observed in summer kimchi and in winter kimchi stored
for an extended period. The over ripening ofkimchi is the most serious problem
in the storage of kimchi. Since the over-ripening of kimchi is mainly due to
activities of lactic acid-forming LAB, the best way to overcome it is to control
the growth of LABwithout destroying the quality of kimchi.
Screening of natural preservatives such as edible plants, herbs and spices,
antimicrobial agents and related compounds to inhibit kimchi fermentation
47)
were studied extensively. Among 42 oriental medicinal plants tested, Baicall
skullcap (Scutellaria baicalensis), and Assam indigo (Cimicifuga foetida) were very
- 9 -
effective for preserving kimchi. Among 32 herbs and spices tested, peppermint
(Mentha piperita L.), cinnamon (Cinnamomum verum Presl), lemon balm (Melissa
officinalis L.), clove (Eugenia caryophyllate Thunb.), hop (Humulus lupulus L.),
rosemary (Rosmarinus officinalis L.), sage (Salivia officinalis L.), horse radish
(Moringa oleifera Lam.) and thyme (Thymus vulgaris L.) showed high
antimicrobial activity against microorganisms in kimchi. Clove was themost
effective microbial inhibitor, when added to fresh kimchi. However, sensory
test was not good for evaluation of the effect of herbs and spices, since their
highly specific flavors affected the taste of kimchi. Among 28 fruits, vegetables
and related plants tested, leaves of pine tree (Pinus rigida), persimmon
(Diospyros kaki) and oak leaves (Quercus glauca) also demonstrated a significant
bactericidal effect. In addition, of 21 natural preservatives added individuallyto
fresh kimchi, only nisin and caffeic acid were able to inhibit fermentation.47)
The changes of pH and acidity of baechu kimchi and mul kimchi were
remarkably inhibited by adding the tea catechins at the level of 2 mg/g fresh
baechu, results suggesting that the tea catechins can be successfully used for the
extension of shelf-life of kimchi.48)
Studies were carried out to investigate the effects of Lithospermum
erythrorhizon, Glycyrrhiza uralensis (LG) with and without dipping of salted
Chinesecabbage in 1% chitosan solution (LGDC) on fermentation of kimchi at
o
10 C during25 days. The sour taste of LG and LGDC added kimchi was
changed more slowly than that of control during fermentation of kimchi. The
shelf-life of LGDC added kimchi was extended over 10 days compared with
control.49)
By the addition of 1% mixed extracts of Lithospermum erythrorhizon and
Scutellaria baicalensis and 1% crab shell treated with ozone to kimchi, color,
flavor, and sourness were slightly inferior, while texture and overall
acceptability were found to be the same or slightly superior compared with
untreated kimchis.50)
It was also found that the kimchi containing 2% of ozone treated crab shell
powders showed both strong neutralization action for 0-25 days and buffer
o 51)
action after 25 days during fermentation at 10 C.
Addition of 500 ppm grape fruit seed extract showed the highest pH during
fermentation at 20oC and lowest titratable acidity compared with control
kimchi. The total microbial counts were higher than LAB counts right after the
preparation of kimchi,but they were similar after three days. However, sensory
evaluation of 3 day old kimchi samples showed a significant difference (P<0.05)
between the control and the treatment in odor, color and taste, except for the
one with 50 ppm.52)
Recently, fermentation characteristics of mustard leaf kimchi added with
green tea and pumpkin powder has been studied and found that the sensory
scores of flavor, aroma and overall acceptability were highest in the kimchi with
- 10 -
0.3% pumpkin powder and 0.2% green tea powder.53)
The effect of chitosan (0.5%) on properties of kimchi was studied during the
fermentation at 20 oC for 8 days. It was confirmed that chitosan reduced the
total number of microorganisms and levels of Leuconostoc sp. and Lac. plantarum
in kimchi, and the lower mol. wt. chitosan fraction had the greatest effect on
levels of Leuconostocsp. Also, chitosan reduced the intensity of sour and stale
flavor notes in kimchi, and the content of reducing sugar in control kimchi
samples was lower than in those containing chitosan for the first 6 days of
fermentation at 20oC. Malic acid content was lower and lactic and acetic acid
contents were higher for control kimchi than in those with chitosan for the first
4 days of fermentation. Control kimchi contained more succinic acid than those
with chitosan for the first 2 days of fermentation.54-55) Leuconostoc sp. and Lac.
plantarum were higher in the control than in the kimchis containing chitosan
dissolved in 0.3% acetic acid and 0.05% sodium benzoate.55) It is also found that
addition of chitosan to kimchis influences pectic substance levels and improves
their textural properties.56)
Two % ginseng in kimchi had the best overall preservative and quality, and
promoted the growth of Lac. plantarumand Lac. fermentum and inhibitedthe
growth of Leu. mesenteroides and Ped. cerevisiae.57)
One or two % of omija (Schizandra chinensis, a fruit of maximowiczia
typica)extracts had strong growth inhibitory properties against isolated LAB
were shown by fumaric and itaconic acid among various organic acids of
Schizandra chinensis.58) The growth of Sac. cerevisiae and Lac. casei in the culture
media containing 1.0 and 1.5% of methanol extracts of kukija (Lycii fructus, a
fruit of the Chinese matrimony vine) were increased, where as that of E. coli was
59)
somewhat decreased.
Addition of sap from pine needles (Pinus densiflora) delayed kimchi
fermentation by slowing down the decrease in pH and inhibiting the growth of
Lactobacillus sp.60)
Water extract of pine needles had more inhibitory effects against Lac.
plantarumthan against Leu. mesenteroides,and the vascularity of kimchi tissue of
control kimchi was degraded more than that of water extracts of pine needles
added kimchi.61,62)
It was found that mustard oil (200 ppm) had antimicrobial effect on the major
LAB of kimchi such as Lac. plantarum, Lac. brevis, Leu. mesenteroides and Ped.
cerevisiae, and mustard and mustard oil could control the shelf life after 15 days
storage at 15oC.63)
The extract of bamboo leaves had a wide range of antimicrobial activity
against Brettanomyces custersii, Klebsiella oxytoca, Pichia membranaefaciens which
cause kimchi softening.64)Recently, the effects of Sepiae os, cuttlefish
born,65)enoki mushroom (Flammulina velutipes),66) Monascus koji,67) and
boiled-dried fusiforme, a kind of seaweed 68) on the fermentation and quality of
- 11 -
kimchi have been studied.
5. Starters
Qualities of kimchi can be controlled bydesirable microorganisms,and
various fermentation conditionssuch as temperature, salt concentration, and
nutrients in raw materials.
The major preparation procedure for kimchi includes lactic acid fermentation
by the addition of various kinds of vegetables, spices, edible salt to Chinese
cabbage and radishes. Kimchi is generally acknowledged to be more nutritious
than other vegetable foods such as sauerkraut, pickles, and Japanese tsukemono
or asatsuke. In addition,it is also known that the fermentation processes of
kimchi involve more complex biochemical and microbiological processes
compared with other fermented vegetable foods.2,16,69)
During the entire stage of natural fermentation of kimchi, lactic
acid-producing bacteria are major population, and after prolonged
fermentation, various and excess organic acids are produced by the LAB
species. Those excess organic acid productions in kimchi fermentation are called
the acidification of kimchi. After that stage, other microorganisms including
yeasts grow on the surface of kimchi, and that growth causes the softening of
the texture of the ingredients.70) Therefore, generally, it can be defined that the
edible good taste of kimchi is obtained before the texture softening and the
acidification.
A hetero fermentative type of LAB, Leuconostoc mesenteroides, is a major
bacterial population of kimchi from the initial to the middle stage of
fermentation. During those stages, hetero fermentative type LAB produce
various metabolites such as lactic acid, acetic acid, ethanol, carbon dioxide,
mannitol, and dextran which are associated with the taste of kimchi, and the
number of LAB reaches the highest during the optimum- ripening period.
However,the total number of Leu. mesenteroidesdecreases sharply when the pH
of kimchi is decreased to 4.0. On the other hand, a homo fermentative type LAB,
Lac. plantarum, whichhas a strong pH tolerance under high organic acid
concentrations, has been continuously increased in their number during kimchi
fermentation to the last stage.It has been reported that the acidification of
kimchi is mainly caused by Lac. plantarum.16)
As already mentioned, kimchi fermentation and ripening are carried out by
the microorganisms present in raw materials. Sugars in raw materials are
converted to lactic and acetic acid, carbon dioxide,ethanol and mannitol by the
LAB growing at 1-3% salt concentration.
As seen in Table 4, many LAB were isolated from kimchi, and among them,
Lac. plantarum, Lac. brevis, Lac. acidophillus, Lac. bavaricus, Lac. homohiochii, Ped.
cerevisiae, Leu. mesenteroides, Leu. dextranicum, and Leu. paramesenteoides have
- 12 -
beentried as kimchi starters to improve the quality and shelf-life extension of
kimchi.71-76)
The combination ofvarious strains such as Leu. mesenteroides, Lac. brevis, Lac.
plantarum and Ped. cerevisiae which were isolated from kimchi could be used as
starters for kimchi fermentation. These starters increase the fermentation rate,
and mixed strains are more effective than a single strain to produce better
organoleptic quality of kimchi.71)
Generally,kimchi fermentation has been carried out relatively at low
temperature, and psychrotrophic LAB were isolated and characterized from
kimchi fermented at 5oC. 24,75) Therefore,psychrotrophic LAB isolated from
kimchi fermented at low temperature were studied as starters for their effect on
kimchi fermentation. The results indicated that the fermentation period could
be shortened by using the LAB starters which isolated from low temperature
kimchi. Among the LAB used as kimchi starters, it was confirmed that
Leuconostoc species were more effective than any other Lactobacillus species
tested for kimchi fermentation.76)
Because the acid production from the hetero fermentative type LAB is lower
than that of the homo fermentative type LAB, the addition of an acid-tolerant
mutant strain of Leu. mesenteroides as starter of a kimchi fermentation may
inhibit the rapid pH decease and lactic acid production during kimchi
fermentation. Therefore, a mutant strain, Leu. mesenteroides M-10 which could
grow in low pH (3.0) at 10oC and produce more CO2 than wild type was
mutagenized to be improved as akimchi starter. With respect to total
acceptability, the kimchisprepared using the mutant strain M-10 were better
than the other strains, and use of the mutant strain extended the
optimum-ripening period of kimchi by two fold compare with that of control.
This report suggested that a mutant strain of Leu. mesenteroideswhich has more
stable growth ability in acidic conditions was able to extend the edible period of
kimchi.77)
Psychrotrophic yeast, Saccharomyces fermentati YK-19 that showed better
o
o
growth at 10 C than at 25 C in the medium containing 0.3% lactic acid and 0.6%
acetic acid,was isolated from kimchi and used as a kimchi starter in order to
prevent over-acidification of kimchi.78) The addition of Sac. fermentati YK-19
prolonged the period of optimum fermentation (at pH 4.2 and 0.6-0.8 acidity) by
>63%. The lactic acid content increased rapidly in control samples, followed by
the kimchi with Sacharomyces sp. Yk-17 and Sac.fermentati YK-19 as starters. The
growth of Lactobacillus species was inhibited by the addition of yeast starter,
particularly by Sac. fermentati YK-19. Furthermore, sensory scores such as acidic
and moldy flavor were reduced by starter addition, while flavor scores for
freshness were increased.79)
Leu. paramesenteroidesP-100, a psychrotrophic mutant which grow well at pH
4.0, and 10oC, and in organic mixture (lactic acid:acetic acid;1:2) was improved
- 13 -
from wild type Leu. paramesenteroides Pw. A wild strain Pw and a mutant strain
P-100 were inoculated as starters and the total acceptability of the kimchi were
evaluated.80,81) Kimchi added with mutant strain had better tastethan that of
control kimchi by sensory test and the optimal pH range of kimchi extended up
to about 2.2-2.5 times. In the kimchi added with Leu. paramesenteroides P-100 ,
the succinic acid content was higher than that of others, and the total number of
Lac. plantarumwas reduced about 2.5 fold with respect to control kimchi.80)
The effects of the addition of Leu. mesenteroides M-100, an acid-tolerant mutant
improved from wild type strain Leu. mesenteroides Mw,82) and Sac. fermentati
YK-19, an acid-utilizing and aromatic flavor-producing yeast, were tested for
the retardation of acidification and the prolongation of the edible period of
kimchi. The addition of Leu. mesenteroidesM-100 to kimchi preparation may
induce the prolonged acidification of kimchi because of its low production of
lactic acid and increased growth in comparison with Lac. plantarum. Also Sac.
fermentati YK-19 may lengthen the edible period of kimchi by reducing the
content oflactic acid and acetic acid in the later period of kimchi fermentation,
and the good flavor in the starter-added kimchi group may be due to the
various compounds, carbon dioxide, and succinic acid produced by Leu.
mesenteroides M-100 and Sac. fermentati YK-19.83)
Recently, the effects of the addition of mutant strains of Leu. mesenteroides and
Leu. paramesenteroides which have increased adipic acid resistance compared
with wild type species on shelf life of kimchi were evaluated.84) The addition of
a combination of both mutants was more effective than that of single strain in
extending shelf-life of kimchi. The optimum inoculation was 0.005% of a 1:10
mixture of Leu. mesenteroides: Leu. paramesenteroides according to the results from
84)
acidification tests and sensory analysis.
To extend the storage period and inhibit contamination of E. coli, conditions
for kimchi brining in lactic acid solution and effect of the halophilic
Lactobacilllus HL-48 starter were investigated. The results showed that the pH
value of the starter inoculated kimchi was 4.2 after 18 hr fermentation at 25oC,
while the pH of the starter non-inoculated kimchi was 3.3 at the same
85)
condition.
Ⅲ. Microbial and chemical changes during kimchi fermentation
1. Microbial changes
The number and species of major microorganisms in kimchi fermentation
vary widely, and are influenced by raw materials and other ingredients.
However, the growth, activity, and role of the microorganisms participating in
the fermentation are influenced more by environmental conditions, especially
by temperature and salt concentration.
- 14 -
Generally, total LAB was highly distributed throughout the whole
fermentation period. However, they were slightly declined as the acidity
increased. The growth pattern of the major LAB during fermentation at 20 to 30
o
C is that the number of Leuconostoc species increase initially, and then at pH 4.0
to 4.5 they decrease rapidly with an increase in the number of Lactobacillus
o
species. However, at 5 to 15 C, the times for the increase and decrease of LAB
are delayed.16,69)
The total counts at the optimum-ripening time were 1x10 8-9 cells/ml and
Leuconostoc spp. appeared maximum levels at this time, and after then total
counts decreased and increased again by little. Lactobacillus and Pediococcus
6-7
16,69)
The number of
appeared maximum level at this period (1x10 cells/ml).
Leu. mesenteroides reached its maximum value at the optimum-ripening stage of
kimchi and decreased when kimchi became acidic. At the same fermentation
temperature, the total number of Leu. mesenteroides was higher at lower salt
content than at higher one. The maximum number reached after 1 day at 30oC, 3
days at 20oC, 6 days at 14oC, and 27 days at 5oC. It is very interesting to note that
the number of Leu. mesenteroidesreached maximum with the corresponding
increase in the total viable count. Lac. brevisgrew better at higher temperature
and lower salt content at over-ripening period of kimchi. Ped. cerevisiae was
dominant at higher salt content (5-7%) and also appeared generally at
over-ripening stage of kimchi. Lac. plantarum appeared at the time when the Leu.
mesenteroides decreased in number and after the appearance of Lac. brevis and
Ped. cerevisiae. The population of Lac. plantarum was dominant at the
over-ripening and acid-deteriorated stage of kimchi. Lac. brevis, Ped. cerevisiae,
and Lac. plantarum were not detected at any levels of salt contents at 5oC. Str.
faeculis appeared rarely at all temperature and salt contents but its number was
16)
negligible.
Film-forming yeasts appear on the surfaces of the kimchi preserved for long
term period, and they produce polygalacturonase and contribute to softening
the texture of kimchi by degrading of pectic substances.70)
The number of fungal flora during kimchi fermentation decreased in number
o
at higher temperature (30 C), but the total number of fungi decreased and
remained constant at temperature below 20oC. However, yeast population
during kimchi fermentation showed typical changes depending upon the
temperature and salt concentration. Total number was not changed at 20-30oC,
but it showed gentle curve of initial increase to slow decrease in the later phase
at lower temperature (14-5oC).16)
The typical changes of major LAB during kimchi fermentation at 20oC are
shown in Fig. 4. The patterns of microbial changes in each lactic acid bacterial
group, Leuconostocs, Lactobacilli, and Streptococci, were similar at different
fermentation temperature, and the microbial changes accelerated by increasing
the temperature. Among them, Leuconostocs showed higher number at high
- 15 -
temperature than the others. The numbers of Leuconostocs and Streptococci
increased the beginning but they rapidly decreased after the optimum-ripening
period. Pediococci increased their number after Streptococci, but they rapidly
disappeared later.69)
The strains of Leuconotocs, Streptococci, Pediococci and Lactobacilli were
identified as Leu. mensenteroides subsp. mesenteroides, Str. faecalis, Str. faecium,
Ped. pentosaceus, Lac. plantarum, Lac. sake and Lac. brevis. Among the LAB
isolated, Lac. brevis and Lac. plantarum appeared mainly at the beginning and
around the over-ripening period of fermentation, respectively.69)
o
Kimchi fermentation is dominated by Lactobacillus spp. at 25 C and
o 86)
Leuconostoc spp. at 5 C. The levels of Streptococcus and Pediococcus species are
lower than those of Leuconostoc and Lactobacillusspecies and decrease
considerably at lower temperature. Like Leuconostoc species, Streptococcus and
Pediococcus species increase initially, and then decrease rapidly after the
optimum-ripening period during the fermentation. Lac. sake and Lac. brevis also
are included among the Lctobacillus species. The Lac. sake especially is isolated
from an early stage and is not able to survive under pH 4.0 at the later stages.
Lac. brevis are also isolated at early stages, but smaller numbers are only found
in the later stages. Lac. plantarumis isolated from all the stages during the
fermentation period, but especially at the later stages after the
optimum-ripening period.69,86)
Lactobacillus sp. and Leuconostoc sp. were the main bacteria isolated from
optimumripened kakdugi(53 and 43%, respectively) as well as from over-ripened
kakdugi. (63 and 37%, respectively). Leuconostoc mesenteroides subsp.
paramesenteroides was the dominant strain among the LAB from kakdugi. The
isolates from optimum-ripened kakdugi required more amino acids for growth
compared to those fromover-ripened samples, while no difference was
observed with respect to vitamins. The physiological characteristics of the
isolates, such as amino acid and vitamin requirements, were different from
26)
those of 9 type strains of various Leuconostoc spp.
Recently, 88 strains of LAB were isolated from dongchimi, and the
predominant strains were identified as Leu. mesenteroides subsp. mesenteroides at
the initial stage of fermentation (on the 5th day), Lc. lactis subsp. lactis at the
middle stage (30th day), and Lac. curvatus and Lc. lactis subsp. lactis at the final
stage (50th day). The 88 strains of isolates were classified into 15 groups
according to the fermentation properties, of which, 6 groups of Leu.
mesenteroides, 3 groups of Lac. curvatus, 2 groups of Lac. cellobiosus, and each of 1
group of Leu. citreum, Lc. lactis. subsp. lactis Lac. acidophilus and Lac. delbrueckii
subsp. delbrueckii.87)
In the early 1960's, LAB such as Lac. brevis, Lac. plantarum, Leu. mesenteroides,
Ped. cerevisiae, and Str. faeculis were isolated from kimchi and it was reported
- 16 -
that the main microorganisms responsible for kimchi fermentation are Leu.
mesenteroides, Lac. brevis, Ped. cerevisiae, and Lac. plantarum which was just
thesame as in sauerkraut fermentation.88,89) However, kimchi is less acidic than
sauerkraut and the optimum acidity and pH of kimchi are 0.6-0.8% and 4.5-4.2,
respectively, while those of sauerkraut are 1.6-2.0% and 3.7-3.5. Also, sauerkraut
fermentation is completed after 20 days at 23oC with 2.25% salt content, whereas
kimchi fermentation is completed only within 3 days under similar
fermentation conditions. Therefore, it has been suggested that the main
microorganism in kimchi fermentation is Leu. mesenteroides rather than Lac.
plantarum and Lac. plantarum is a main acid-deteriorating organism in kimchi
fermentation unlike in sauerkraut where it constitutes main responsible
microorganism.16)
Recently, many new LAB were isolated and identified from various kimchis
using molecular techniques. However, the role of new LAB has not yet been
confirmed by testing as kimchi starters. New LAB from kimchi will be
discussed more in chapter IV-1.
2. Chemical changes
The chemical compositions of kimchi may be different basically depending
on the varieties of cabbage, kinds and amounts of minor ingredients such as
garlic, green onion, leek, hot pepper powder, ginger, and fermented anchovy or
shrimp. However, kimchi fermentation was carried out continuously by LAB
existing in the raw materials. The sugars in kimchi raw materials were
converted to organic acids, carbon dioxide, ethanol, and other flavoring
compounds by lactic acid fermentation.
Generally, the best quality of kimchi can be obtained at pH 4.2-4.5 and at the
time being maximum levels of carbon dioxide production. Acidity at the
optimum- ripening period is 0.6 -0.8% as lactic acid, and reaches 1.5% upon
over-ripening and becomes 1,5-2.0% at the stage of acid-deterioration of kimchi.
The optimum-ripening time and shelf-life of edible period were changed
depending on the salt content, fermentation temperature and time as seen in
previous Table 3.
In most cases, the kimchi fermentation process has several stages based on
the changes of pH, acidity and reducing sugar content. The first stage has a
rapid decrease of pH, an increase of acidity and a decrease of reducing sugar.
The second stage shows a gradual decrease in pH, an increase in acidity, but a
rapid decrease of reducing sugar. The last stage has no or only gradual changes
in pH, acidity, and reducing sugars.16)
Generally, during the kimchi fermentation, pH and reducing sugars decrease
while total acids increase. The pH starts from 5.5-6.0, reaches 4.5-4.2 at optimum
- 17 -
ripening period, and drops further down upon over-ripening period. High
temperature and low salt content showed faster fermentation than low
temperature and high salt content.
Lactic, acetic, citric, malic, fumaric, succinic, oxalic, tartaric, malonic, maleic,
and glycolic acid were identified from kimchi samples. Among the organic
acids identified, lactic acid and acetic acid are the major acid that increased by
fermentation. However, the kimchi fermented at lower temperature (6-7oC)
contains more lactic and succinic acid, and less oxalic, malic, tartaric, malonic,
maleic and glycollic acid than the kimchithat fermented at higher temperature
(22-23oC), while no difference is noted in citric acid level.90) Higher salt
concentration brings about a lower acetic acid, and large amounts of acetic acid
and carbon dioxide make kimchi tasteful.16,91-93)
The production of carbon dioxide during kimchi fermentation was stimulated
by higher temperatures and was affected by seasonal factors. Kimchi made
from winter baechu (Chinese cabbage) produced much more fermentative gas
than that made from summer baechu. It was suggested that the changes in
carbon dioxide concentration could be used as a characteristic index for
indicating the fermentation course of packaged kimchi products.94)
The changes of the content of organic acids, carbon dioxide, alcohols and
carbonyl compounds of the various kimchi which were made from cabbage
o
o
with green onion, garlic, ginger, and red pepper fermented at 12 C-16 C were
investigated. The identified nonvolatile organic acids were acetic, formic,
propionic, butyric, valeric, n-caproic and malic acid. The identified carbonyl
compounds were acetaldehyde and acetone. The content of lactic acid was
increased with fermentation, and higher in kimchis containing red pepper,
garlic and green onion. The content of acetic acid wasincreased with
fermentation, especially in the kimchi containing garlic. The content of carbon
dioxide was higher in the kimchi containing garlic. Alcohols identified in all
kimchis were only ethanol. Carbonyl compounds had no direct effect on
off-flavor of kimchi.92)
The production of free non-volatile and volatile organic acids in kimchi
during fermentations at 30, 20, and 5oC, were determined by gas
chromatography. The order in the amount of non volatile organic acid, soon
after preparation, was malic,citric, tartaric, pyroglutamic, oxalic, lactic, succinic,
and L-ketoglutaric acids. The major non volatile acids at the optimum ripening
time were malic, tartaric, citric and lactic acids, and as the temperature was
lowered, the amount of lactic, succinic, oxalic, pyroglutamic and fumaric acid
increased, while that of malic, and tartaric acids decreased. The order in the
amount of volatile acids at the beginning was acetic, butyric, propionic and
formic acids. Among these acids, acetic acid was significantly increased in its
amount during fermentation. The kimchi fermented at low temperature
produced more acetic acid than that fermented at high temperature.90,95)
- 18 -
Of 17 volatile flavor components tentatively identified from kimchi, ethanol
was the most abundant, and increased in fermented kimchi while the others
decreased with the time of fermentation.96) It was also found that the ratio of
volatile to non volatile acids found to be highest at the optimum-ripening time
16)
of kimchi.
Vitamin B1, B2, B12, and niacin reachedthe highest levels -twice the original
content- at maturation. It was also found that kimchi had the most palatable
taste at this period and subsequently there was a sharp decrease in B vitamins
with a sudden development of acids. On the other hand, although both vitamin
C and carotene decrease during fermentation, their residual contents were still
97)
significant.
Many kinds of free amino acids were identified from mustard leaf kimchi
samples, and it was found that major free amino acids were proline, glutamic
acid, alanine and histidine. It was also found that nucleic-acid related
compounds were hypoxanthine, inosine monophosphate (IMP), and guanine
monophosphate (GMP).98)
Major flavor components were identified as dimethyl disulfide, dimethyl
trisulfide, dipropyl disulfide, 1-butane-1-isothiocyanate, and diallyl disulfide
from kimchi fermented at 5oC by GC and GC-MS. The contents of organic acids
such as lactic and citric acid increased during fermentation. Free amino acids
were importantin kimchi flavor. Total concentration of free amino acids
increased from 316 to 600 mg/100g of kimchi on fermentation, and glutamic
acid, alanine, valine, leucine, lysine and arginine levels were high. Sensory
evaluation showed that kimchi flavor was closely related to the contents of
non volatile organic acids and free amino acids and pH.99)
In wooung kimchi, a specialty kimchi prepared form burdock (Arctium lappa
L), fermented at 15oC, it was found that the major volatile components were
identified as ethanol, hexanol, 2-hexanol, disulfidedi-2-prophenyl, zingiberene,
and beta-sesquiphellandrene. The relative amounts of hexanal, 1-hexanal and
ethanol decreased, while the relative amounts of acetic acid ethyl ester,
3-hydroxy-2-butanone and acetic acid increased gradually during
fermentation.100)
Aroma-active compounds in kimchi prepared with or without fish sauce
were analyzed. The most intense aroma compounds in kimchi included
dimethyl trisulfide, diallyl disulfide isomers, diallyl trisulfide, and methylallyl
disulfide. However, addition of fish sauce did not noticeably affect the aroma
profile of kimchi.101)
Recently, flavor compounds of dongchimi soup fermented at different
temperature and salt concentration were analyzed. In this study four organic
acids including acetic, lactic, malic, and succinic acid were identified. The flavor
compounds of dongchimisoup were composed of mainly dimethyl disulfide and
ethanol followed by 3-(methylthio)-1-propene. Acetic acid and dimethyl
- 19 -
trisulfide were also detected significantly. Dongchimi soup fermented at 4 oC
after prefermentation at 12 oC for 12 hr contained the largest amount of flavor
compounds.28)
The taste and flavor components have been identified from various kimchi
samples. However, the exact amounts of those compounds during kimchi
fermentation were not clearly analyzed. Further researches are needed to
improve the tastes and quality of kimchis.
Ⅳ. Characteristics of LAB from kimchis
1. Identification of kimchi microorganisms
Kimchi fermentation and ripening were carried out by the microorganisms
present in the raw materials. Sugars in the raw materials are converted by the
LAB surviving at 2~3%salt concentration to lactic, acetic acid, carbon dioxide,
ethanol and mannitol.
The qualityof kimchi depends on the composition of the LAB involved in
the fermentation process. Therefore, in order to study the ecology of kimchi
microorganisms, it is important to understand the components of the microbial
community and identification of the physiologically active microorganisms for
kimchi fermentation.
Isolation and identification of microorganisms have long been attempted in
kimchi, conventionally prepared and fermented with the mixture of salted
cabbage and spices such as sliced radish, red peppers, garlic, ginger, green
onions, and fermented fish sauces. Kimchi is a fermented food with the variety
of vegetables. Therefore, it is expected that various LAB propagate in its
habitat.
Since 1960, many aerobic bacteria, anaerobic bacteria including LAB, yeast,
and fungi were isolated and identified from kimchi and other vegetable
fermented products and were reported in Korea as seen in Table 5 and 6.
Seven genera of LAB include Lactobacillus, Leuconostoc, Weissella,
Pediococcus, Streptococcus, Lactococcus, and Enterococcus were isolated and
identified from kimchis as seen in Table 5. Among them, Lac. brevis, Lac.
plantarum, Leu.citreum, Leu. lactis, Leu. mesenteroides subsp. mesenteroides, Leu.
mesenteroides subsp. dextranicum, Weis. pramesenteroides, Str. faecium, and Ped.
pentosaceus have been commonly isolated.
Six genera of aerobic bacteria from kimchi were Achromobacter,
Flavobacterium, Pseudomonas, Aerococcus, Aeromonas, and Bacillus, and ten
genera of yeast from kimchi wereBretanomyces, Candida, Cryptococcus,
Citeromyces, Debaryomyces, Kluyveromyces, Pichia, Rhodotorula, Saccharomyces and
Torulopsis as seen in table 6. However, there is no clear evidence how those
aerobic bacteria and yeasts except Saccharomyces species have been involved
- 20 -
and affected kimchi fermentation.
Recently, Leu. mesenteroides, Lac. curvatus, Lac. cellobiosus, Leu. citreum,
Lactococcus lactis subsp. lactis, Lac. acidophilus and Lac. delbrueckii subsp.
delbrueckii were isolated from dongchimi made by traditional method.87) Also,
ethanol and low acid producing Weis. paramesenteroides P30 were isolated from
kakduki (cubed radish kimchi) and used as kimchi starter for reduced acid
production.111) Lac. plantarum and Lac. pentosus from low salt (0.2-1.0%)
mul-kimchi and Lac. plantarum, and Lac. brevis from medium salt (3.0%)
mul-kimchi were isolated and identified. Other identified LAB were Leu.
citreum, Leu. mesenteroides subsp. mesenteroides and dextranicum and Str. faecium
in mul-kimchi containing 0-3.0% salt, while Pediococcus sp. was not detected. As
gram-negative organisms, Aeromonas hydrophyla, Pseudomonas fluorescens,
Pseudomonas aureofaciens and yeast Candida pelliculosa, Cryptococcus laurentii were
identified in the mul-kimchi.27)
Lactic acid bacteria are widely distributed in Korean traditional fermented
food such as kimchi. Also many LAB have been isolated from kimchi,
particularly, the genera Lactobacillus, Leuconostoc, Weissella and Pediococcus are
known to play an important role in kimchi fermentation.69,89,111)Traditional
identification methods based on physiological phenotypes are labor intensive
and time consuming. Until recently, the identification of the LAB isolated from
kimchi has mostly depended on traditional phenotypic analyses. However, this
type of identification method using biochemical and morphological
characteristics is limited in its discrimination and accuracy.108) Therefore, studies
104,106,118,119)
Accordingly, the
on their systematic taxonomy have been reported.
effective study of kimchi fermentation requires the development of rapid and
accurate LAB identification methods, such as genotypic approach using modern
103,109,120)
molecular typing and identification tools.
Recently, LAB in kimchi were identified and differentiated rapidly by using
the Biolog system. Leuconostoc and Lactobacillus are reported as the main genera
associated with kimchi fermentation.118,106). The former genus was generally
o
found at less than 15 C and wascomprised of isolated strains such as Leuconostoc
mesenteroides subsp. mesenteroides, Leu. citreum, Leu. gelidum, and Leu.
kimchi.107,112) All species of the genus Leuconostocisolated from kimchi have been
found to produce slime from sucrose so far, which is a dextran, and dextran
producing Leuconostoc lactis from sucrose media was also isolated from
kimchi.108)
Until 90's most taxonomic studies on isolates from kimchi have been based on
phenotypic characteristics, but after 90's a polyphasic approach including
phenotypic, chemotaxonomic, and molecular methods is applied to determine
the taxonomic position of kimchi microorganisms. Recently, novel strains such
as Leuconostoc kimchi,112) Lactobacillus kimchi,113) Weissella koreensis,114) and
Weissella kimchi117) from kimchi have been reported. However, further studies
- 21 -
are needed to understand the real role of those new strains on kimchi
fermentation.
Aerobic yeasts and molds appear on the surface of the upper layer and on
improperly covered vegetables at the later fermentation stages. Undesirable
kimchi with an off-flavors and softened texture is positively due to the
excessiveaerobic growth of moulds and film-forming yeasts. Particularly the
film-forming yeasts appeared in long term stored kimchi at low temperature
produce a polygalacturonase which degrade pectin to make kimchi's texture
soft.70) However, yeast appearing in low temperature (below 15℃) fermented
79)
kimchi has a certain role in kimchi's flavor and odor.
2. LAB producing bacteriocins from kimchi
Kimchi is prepared with various kinds of vegetables, spices and other
ingredients and becomes palatable through proper fermentation. Kimchi
fermentation initiated by various microorganisms present in the raw materials,
but the fermentation is gradually dominated by LAB.1,5) The LAB play an
important role in the taste of kimchi, as in dairy products such as cheese and
fermented milk. The strains belonging to the genera Leuconostoc, Lactobacillus,
Streptococcus, Pediococcus and Lactococcus in kimchi have been reported1,16,24,104)
Accordingly, kimchi has been one of the important sources of LAB in Korea for
a long time. Generally, the LAB are known to have the potential to inhibit the
growth of microorganisms, especially pathogenic and spoilage bacteria. The
antimicrobial activity of LAB is known to be due to the produced organic acids,
hydrogen peroxide, diacetyl and bacteriocins. Many LAB have been isolated
from kimchi in Korea and some of them have been shown to have antimicrobial
121-123)
activity and other useful properties
The LAB have long been known to produce antimicrobial proteins called
bacteriocins. Certain bacteriocins inhibit various food-born pathogens,
including Bacillus cereus, Clostridium perfringens, Listeria monocytogenes, and
Staphylococcus aureus. This suggests that bacteriocin-producing LAB may be
useful in biocontrol of kimchi either by applying the culture directly or by
adding the produced bacteriocin as a natural preservative. From this point of
view, there are many reports on the isolation of bacteriocin-producing LAB
from various kimchi samples.
As seen in Table 7, bacteriocins are produced by the genera of Pediococcus,
Lactobacllus, Leuconostoc, and Lactococcus in kimchis.
The LAB isolated from kimchi have antimicrobial activity against E. coli,
Staphylococcus aureus, Bacillus cereus and other microorganisms. Major LAB
responsibile for this activity are Pediococcus pentosaceus, Leuconostoc spp., Lac.
plantarum and Lactococcus lactis. The properties of the inhibitory substances
from these bacteria have been determined and purified. These bacteria could
- 22 -
produce adverse circumstances for the growth of other microorganisms.124,125)
Due to the antibacterial activity of nisin against wide range of gram- positive
bacteria and its stabilityunder acidic conditions, nisin have been studied on its
effectiveness in preventing over-acidification of kimchi. It has been reported
that nisin added kimchi showed a slower rate of acid production.47)However,
controversial result was found that the use of nisin to prevent over acidification
of kimchi was not effective because of the nisin inactivation by vegetable
components and the presence of nisin-resistant LAB on kimchi.125-127)
Ⅴ. Conclusion
Kimchi is characteristic in its palatability giving sour, sweet and carbonated
taste with medium texture in tissue of kimchi. In this respect kimchi differs
greatly from sauerkraut that is popular in the West. The optimum acidity, pH
and salt content of kimchi are 0.6% (as lactic acid), 4.5 and 2.0-2.5%,
respectively. Kimchi fermented at low temperature (7-14℃) was more tasty
than that at higher temperature (20-30℃).
The total number of kimchi microorganisms reaches its maximum level
(1x108-9 cells/ml) at optimum-ripening time, and after then the number of LAB
decreases slowly and maintains its 2nd maximum level (1x106-7 cells/ml).
Many aerobic and anaerobic bacteria, especially LAB were isolated and
identified from kimchi. However, in kimchi fermentation system, it seems clear
that hetero fermentative LAB producing organic acids, carbon dioxide, and
dextrans from sugars are major species in the early stage and optimum
fermentation period. Homo fermentative LAB producing excessive lactic acid is
a major species in the final stage of fermentation. The total aerobic bacteria and
fungi decreased and the yeasts somewhat increased and slowly decreased in
number at lower temperatures (10-14℃).
Carbon dioxide and organic acids such as lactic, acetic, succinic and citric
acids were detected during kimchi fermentation. Vitamin B1, B2, B12, and
niacin increased two fold at optimum ripening period and decreased during
over-ripening, while vitamin C and carotenoid decreased. It was also found
that the ratio of volatile to nonvolatile acids and carbon dioxide reached
maximum at optimum-ripening period of kimchi.
Kimchi fermentation is complex and is due mainly to certain LAB and yeasts
naturally present in raw materials. Several physicochemical and biological
factors such as salt and sugar concentration, temperature, raw materials, natural
preservatives and starter culture influence the quality of kimchi. Among the
many factors affecting kimchi fermentation, salt content and temperature are
the most important, and the next is the quality of raw materials and
microorganisms specially hetero fermentative LAB.
Many homo and hetero fermentative LAB, such as genus Lactobacillus,
- 23 -
Leuconostoc, Weissella, Lactococcus, Streptococcus and Pediococcus were isolated
and identified from various kimchi samples, but genus Leuconostoc, Weissella
and other LAB producing organic acids, carbon dioxide and bacteriocins are the
most important microorganisms for the controlled fermentation of kimchi.
However, further studies are need to understand the real mechanism of those
LAB on kimchi fermentation and improved classification techniques using
modern taxonomies such as polyphasic and molecular methods are necessary to
understand kimchi microorganisms.
After optimum ripening is reached, kimchi fermentation may continue until
the product has acidic taste and softenedtexture, which cause the acid
deterioration. So far the preservation of kimchi under refrigeration at around
5oC is known to be the best way for long-term preservation up to 6 months.
Finally, further researches are needed to develop the technology necessary for
the controlled fermentation using starters and long-term preservation of
commercial kimchi.
And also, further studies are needed to fully understand the mechanisms of
action and to gain a complete knowledge, even though systematic research is
difficult because of the complexity of kimchi.
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