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Soyfoods and soybean products: From traditional use to modern applications

Article  in  Applied Microbiology and Biotechnology · August 2012

DOI: 10.1007/s00253-012-4330-7 · Source: PubMed

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Appl Microbiol Biotechnol (2012) 96:9–22
DOI 10.1007/s00253-012-4330-7

MINI-REVIEW

Soyfoods and soybean products: from traditional

use to modern applications
Kuan-I Chen & Mei-Hui Erh & Nan-Wei Su &
Wen-Hsiung Liu & Cheng-Chun Chou &
Kuan-Chen Cheng

Received: 19 May 2012 / Revised: 19 July 2012 / Accepted: 21 July 2012 / Published online: 8 August 2012
# Springer-Verlag 2012

Abstract Soybean products (soyfoods), reported as poten- Bacillus subtilis with their β-glucosidase activity. This arti-
tial functional foods, are implicated in several health- cle presents an overview of soybean’s chemistry, applica-
enhancing properties, such as easing the symptoms of post- tion, state-of-the-art advances in soybean fermentation
menopausal women, reducing the risk of osteoporosis, pre- processing and products as well as their applications in food
venting cardiovascular disease, and antimutagenic effects. and pharmaceutical industries. Different compounds, such
Isoflavone, for example, is one of the most important com- as isoflavone, dietary fibers, and proteins which exhibit
pounds abundantly found in soybean, mainly accounting for significant bioactivities, are summarized. The roles of dif-
the health-enhancing properties as mentioned earlier. How- ferent microorganisms in bioconversion and enhancement
ever, most biological activities of isoflavones are mainly of bioactivities of fermented soybean are also discussed.
attributed to their aglycone forms. It has also been demon-
strated that isoflavone aglycones are absorbed faster and in Keywords Soyfoods . Soybean . Fermentation . Bioactive
greater amount than their glycosides in human intestines. compounds . Food processing
Fortunately, deglycosylation of isoflavones can be achieved
during fermentation process by several strains such as lactic
acid bacteria, basidiomycetes, filamentous fungus, and Introduction

Soybean (Glycine max) is a species of legume which

K.-I. Chen : M.-H. Erh : C.-C. Chou : K.-C. Cheng originated from Asia and was introduced to the USA in 1765
Graduate Institute of Food Science and Technology, by Samuel Bowen (Brachfeld and Choate 2007). The genus
National Taiwan University, name Glycine was first introduced by Carl Linnaeus
No. 1, Sec. 4, Roosevelt Road,
(Linnaeus 1737) in his first edition of General Plantarum.
Taipei, Taiwan
The word glycine derived from the Greek word “glykys”
N.-W. Su (sweet) refers to the sweetness of the pear-shaped edible
Department of Agricultural Chemistry, tubers produced by native American legume. The scientific
National Taiwan University,
name, G. max (L.) Merrill, proposed by Merrill in 1917 has
Taipei 10617, Taiwan
become the official name for this useful plant.
W.-H. Liu Soybean was first considered as sacred for its use in crop
Institute of Biochemical Science and Technology, rotation as a method of nitrogen fixation and did not become
National Taiwan University,
an important crop until 1910s. Soybean played a significant
No. 1, Sec. 4, Roosevelt Road,
Taipei, Taiwan role in the USA after World War I. Due to its nitrogen
fixationability, the drought regions of the USA were able
K.-C. Cheng (*) to regenerate their soil and therefore increase their produc-
Graduate Institute of Biotechnology, National Taiwan University,
tivity that met with government demands.
No. 1, Sec. 4, Roosevelt Road,
Taipei, Taiwan Henry Ford, the founder of Ford Motor Company, was
e-mail: kccheng@ntu.edu.tw noted as a great leader of the soybean industry. The Ford
10 Appl Microbiol Biotechnol (2012) 96:9–22

Company spent around US$ 1,250,000 on soybean research Table 1 Nutritional

value of soybeans Energy 466 kcal
during 1932–1933. The “Soybean Car” unveiled by Henry
(per 100 g)
Ford in 1941 was actually a plastic-bodied car. Lowell E. Carbohydrates 30.2 g
Overly, the man who was instrumental in creating the car, Sugars 7.3 g
claims that it was “…soybean fiber in a phenolic resin with Protein 36.49 g
formaldehyde used in the impregnation” (Davis 1941). Trytophan 0.59 g
Soybeans are one of the most valuable crops in the world Threonine 1.77 g
not only as the staple food in most Asian countries, provid- Isoleucine 1.97 g
ing a good source of protein for human diet, but also as an Leucine 3.31 g
oil seed crop, feed for livestock and aquaculture, and biofuel Lysine 2.71 g
feedstock. According to the Statistics Division of the Food Methionine 0.55 g
and Agriculture Organization (FAO-STAT 2010), the world Phenylalanine 2.12 g
annually produced 43.7 million metric tons of soybeans in Tyrosine 1.54 g
1970 and reached 261.6 million metric tons in 2010. The top Valine 2.03 g
five producers of soybean are the USA, Brazil, Argentina, Arginine 3.15 g
China, and India, producing more than 92 % of the world’s Histidine 1.1 g
soybeans (USDA-WASDE 2012). Alanine 1.92 g
To date, soybean becomes an important global crop and
Aspartic acid 5.12 g
is one of the “biotech foods” which has been genetically
Glutamic acid 7.87 g
modified (GM) and being used in an increasing number of
Glycine 1.88 g
food products. In 1995, Monsanto Company first introduced
Proline 2.38 g
Roundup Ready soybeans that exhibit herbicide-tolerant
Serine 2.36 g
ability and were engineered to enable crops to withstand
Fat 19.94 g
high doses of herbicides that would otherwise kill them. In
Saturated 2.89 g
1997, around 8 % of all commercial soybeans were genet-
Monounsaturated 4.4 g
ically modified and now it reaches 93 % in 2010 (Acreage
Polyunsaturated 11.26 g
NASS 2010). Although the overall estimated benefits of the
Water 8.54 g
GM soybeans in the USA was $310 million, the use of GM
Vitamin A 1 mg
soybeans has caused some concerns about biodiversity as
Vitamin B6 0.4 mg
well as problems when exporting to some regions, such as
Vitamin C 6.0 mg
European Union, where consumers are reluctant to use GM
products. Vitamin K 47 mg
Calcium 277 mg
Iron 15.7 mg
Soybean and its bioactivity Magnesium 280 mg
Phosphorus 704 mg
Ingredients of soybean Potassium 1797 mg
Sodium 2 mg
Source: USDA National Zinc 4.9 mg
Soybeans are rich in protein and oil content, which accounts
Nutrient Database 2004
for about 60 % of dry soybeans by weight (Table 1). The
remainder consists of 35 % carbohydrates and about 5 %
ash. Many valuable vitamins, flavonoids, and polysacchar- ingredients and their bioactivities are discussed in the suc-
ides also exist within soybeans. The high soy protein con- ceeding text.
tent makes soybeans an excellent source of complete
protein, containing significant amounts of the essential ami- Soy oil
no acids that cannot be synthesized by the human body
(Henkel 2000). Soybean contains about 20 % oil. The extracted oil from
The quality of soy protein also receives a very high score, soybeans are refined and blended for different applications,
74, by the Protein Digestibility Corrected Amino Acid Score and most of them are served as dietary oil. Soy oil contains
(PDCAAS) standard, a criterion of nutritional equivalent of no trans-fat and is low in saturated fat. As for the unsaturat-
meat, eggs, and casein for human growth and health (Protein ed fatty acid, soy oil comprises 21 % of the monounsaturat-
Quality Evaluation 1989). Whole soybeans has a score of ed oleate, 55 % of the polyunsaturated linoleate, and 8 % of
96, soybean milk 91, and eggs 97. Other important the polyunsaturated linolenate (Deckelbaum and Torrejon
Appl Microbiol Biotechnol (2012) 96:9–22 11

2012). Soy oil can reduce cholesterol in the human body due LNCaP prostate cancer cells, and BG-1 ovarian cancer
to its high content of polyunsaturated fatty acid (Bennett et cells), antiestrogenic effect (through estrogen receptors α
al. 2003; Hammond et al. 2005). Studies have shown that a and β), antibacterial action, antinematode activity, and anti-
diet high in these unsaturated fatty acids had significant fungal activity (Ng et al. 2011). S-equol, another metabolite
reduction on elevated levels of the total cholesterol, without of daidzein, is not present in soybeans but is produced
affecting the level of high-density lipoprotein (HDL) naturally in the gut of certain individuals, particularly
(Kinsell et al. 1954; Grundy and Denke 1990). Recently, Asians, by bacterial biotransformation (Jackson et al.
Hassan and Abdel-Wahhab (2012) indicated that bilateral 2011). A positive outcome for osteoporosis, prostate cancer,
ovariectomized rats fed on 15 % of soy oil-supplemented diet cardiovascular disease, and vasomotor symptoms was ob-
for 2 months had significantly exhibited the restoration of served when >5–10 ng/mL of S-equol was applied (Park et
changed lipid profile, improved cardiac biomarker near to al. 2009; Bolanos et al. 2010; Liu et al. 2010; Weaver and
standard value, and better inflammatory and antioxidant Legette 2010).
status.
Anthocyanin
Dietary fibers
Black soybean [G. max (L.) Merr.], a variant of soybean, has
The insoluble carbohydrates in soybeans consist of the a black seed coat because of the accumulation of anthocya-
complex polysaccharides cellulose, hemicelluloses, and nins (Choung et al. 2001; Xu and Chang 2009; Zhang et al.
pectin and can be classified as dietary fiber (Erdman and 2011). These anthocyanins have been elucidated as
Weingartner 1981). These dietary fibers can absorb water delphindin-3-glucoside, cyaniding-3-glucoside, and
throughout the digestive system and ease defecation. On the petunidin-3-glucoside by structural analysis (Choung et al.
other hand, water-soluble oligosaccharides such as sta- 2001). The content of delphindin-3-glucoside, cyaniding-3-
chyose and raffinose can facilitate endogenous bifidobacte- glucoside, petunidin-3-glucoside, and total anthocyanin in
ria in the colon against putrefactive bacteria (Anderson et al. seed coats of ten black soybeans has been reported to be in
2009). Lately, Inoguchi et al. (2011) conducted an in vivo the ranges of 0–3.71, 0.94–15.98, 0–1.41, and 1.58–
study of the effects of fermented and non-fermented soymilk 20.18 μg/g, respectively. It has been suggested that antho-
intake on the fecal microbiota and metabolic activities of ten cyanin exhibits free radical scavenging effects (Tsoyi et al.
healthy subjects. Results revealed that raffinose and sta- 2008) and acts as a potential antineoplastic agent (Katsuzaki
chyose were utilized by probiotics, thus promoting the et al. 2003; Park et al. 2007; Kim et al. 2008; Nizamutdinova
growth of most bifidobacteria and lactobacillus species, et al. 2009). Many in vitro and in vivo studies indicated that
whereas most isolates of Escherichia coli and Clostridium the anthocyanin isolated from black soybean exhibited
pefringens do not use them. In addition, the number of anti-inflammatory and anti-proliferative effect by suppress-
bifidobacteria and lactobacilli in feces was found to be ing the proliferation of human HT-29 colon cancer cells
significantly increased, whereas clostridia were decreased (Kim et al. 2008) and human leukemia Molt 4B cells
upon the subjects’ intake of fermented soymilk. These (Katsuzaki et al. 2003). The inhibitory effect of black soybean
results suggested that intake of soybean oligosaccharides is anthocyanin on inflammatory processes has also been studied
related to improvement of intestinal environment. (Nizamutdinova et al. 2009). In this study, results indicated
that pretreatment of cells with anthocyanin inhibited VCAM-1
Isoflavone expression as well as reduced the nuclear levels of GATAs
and IRF-1.
Soybeans have been reported to contain a high concentra-
tion of isoflavones (~1–5 μg/g dry soybean) with potential Vitamins
health-enhancing properties, such as easing the symptoms of
postmenopausal women (Nagata et al. 2001; Setchell et al. Soybeans also contain vitamins, A, B6, B12, C, and K. These
2003), reducing the risk of osteoporosis (Lydeking-Olsen et chemical compounds cannot be synthesized in sufficient
al. 2002; Cotter and Cashman 2003), preventing cardiovas- quantities by an organism and must be obtained from the
cular diseases (Goodman-Gruen and Kritz-Silverstein diet (Tsukamoto et al. 2000; Yamaguchi et al. 2000; USDA
2001), and antimutagenic effects (Fioravanti et al. 1998; National Nutrient Database 2004).
Cappelletti et al. 2000; Barnes 2010). Glyceollin, a metab-
olite of daidzein (a soy isoflavone), is one of the major Health benefits of soybeans
phytoalexins and phytoestrogens, and an important prenyl-
flavonoid in soybean. Its biological activities include anti- There are many health benefits from the intake of soybean
proliferative/antitumor action (toward B16 melanoma cells, or soy products, including prevention of breast cancer,
12 Appl Microbiol Biotechnol (2012) 96:9–22

prostate cancer, menopausal symptoms, heart disease, and intake is much more effective than animal protein in dietary
osteoporosis (McCue and Shetty 2004; Takahashi et al. therapy for patients with type 2 diabetes. In addition, iso-
2005; Xu and Chang 2008; Slavin et al. 2009; Zhang et al. flavones isolated from soybean and soy products have been
2011). Isoflavones derived from soybean play a key role in reported to fight against the oxidation of LDL cholesterol
the contribution of health benefits. In the scientific area, (Tikkanen et al. 1998; Takahashi et al. 2005; Chen et al.
isoflavones attract tremendous attention since more than 2011).
17,000 scientific publications have isoflavones mentioned It is hypothesized that isoflavonoid antioxidants isolated
in their title or abstract in Web of Knowledge (http://pcs. from soy could be associated with lipoprotein and possibly
webofknowledge.com/). Due to the similarity of its chemi- enable to protect them against oxidation. The results show
cal structure to estrogen which is produced by the human that lag phases of LDL oxidation curves were prolonged by
body, most of these studies have shown that isoflavones a mean of 20 min during soy intake (2 weeks) compared
possess some health benefits as summarized in the following with values obtained from volunteers without soy consump-
text. tion, which indicates the contribution of soy intake to reduce
oxidation (Tikkanen et al. 1998). This suggests that the
Reduce risk of cardiovascular disease intake of soy protein provides a good strategy to prevent
the oxidation of LDL cholesterol. Furthermore, the antiox-
Over the past decades, coronary heart disease such as car- idant activity of black soybean against LDL oxidation in
diovascular disease (CVD) has been suggested to be closely comparison to yellow soybean has also been studied
related to personal diet preference (Hu and Willett 2002; Hu (Takahashi et al. 2005). The extract from black soybean
2009). Saturated fat and high cholesterol from food intake exhibited longer LDL oxidation lag time than that from yellow
are reputed to be significant factors to cause cardiovascular soybean (205±16 and 65±3 min, respectively). The seed coat
diseases (Zyriax and Windler 2000). Stroke or high blood and the mixture of the germ and cotyledon obtained from both
pressure mainly resulting from the accumulation of the two soybeans were investigated separately for their inhibitory
excess saturated fat and cholesterol in the blood vessel has effect on LDL oxidation. The results demonstrate that the
been the leading cause of death at present (Bronner et al. diluted extract solution from the black soybean with darker
1995; Siri-Tarino et al. 2010). Some reports have pointed seed coat prolonged the lag time significantly more than the
out the long-term intake of soy protein as being beneficial to original extract of the yellow bean seed coat, whereas the
reduce the amount of cholesterol in blood for the prevention antioxidant effects of the mixture of the germ and cotyledon
of cardiovascular diseases (Potter et al. 1993; Baum et al. of both soybeans were similar, suggesting that the antioxidant
1998; Potter et al. 1998). In animal studies, soy protein activity against LDL oxidation was mainly contributed by
derived from soybean or soyfood was found to be capable the seed coat of soybean.
of reducing the level of low-density lipoprotein (LDL) cho-
lesterol in the plasma (Khosla et al. 1991). The amount of Cancer prevention
plasma cholesterol and LDL cholesterol detected in rabbits
fed with soy protein was 1.84±0.28 and 0.67±0.1 mmol/L, The research which emphasized on studying diet intake has
respectively, which were both significantly lower than those revealed that daily consumption of soybean is one of the
in rabbit fed on casein (7.37±0.59 and 2.66±0.41 mmol/L). major reasons for the relatively lower rates of hormone-
Moreover, clinical trials have evidenced that soy protein related cancers, such as breast cancer, prostate cancer, and
plays an important role in lowering serum total and LDL endometrial cancer. Diet has been believed to have a major
cholesterol in humans (Sirtori et al. 1993; Tikkanen et al. influence on disease risk and one group of compounds, the
1998; Wangen et al. 2001; Taku et al. 2007). Taku et al. so-called phytoestrogens, has been suggested to play a cru-
(2007) have demonstrated that soy isoflavones significantly cial role in cancer protection (Chiechi 1999; McCue and
reduced serum total cholesterol by 0.1 mmol/L (3.9 mg/dL Shetty 2004). Soyfoods and soybean products contain high
or 1.77 %) and LDL cholesterol by 0.13 mmol/L (5.0 mg/dL levels of isoflavones, which have been classified to be a
or 3.58 %). Soy protein exhibited enriched isoflavones, main group of phytoestrogens. Evidences provided in epi-
decreasing LDL cholesterol by 0.18 mmol/L (7.0 mg/dL demiological studies support that isoflavones such as daid-
or 4.98 %) (Taku et al. 2007). Moreover, the efficiency of zein and genistein found in soybeans and soy products are
soy protein intake has also investigated in comparison to protective against breast cancer and prostate cancer (Severson
milk protein intake in adults with type 2 diabetes (Pipe et al. et al. 1989; Jacobsen et al. 1998; Magee and Rowland 2004;
2009). Serum LDL cholesterol was dramatically decreased Sakamoto et al. 2010; Andres et al. 2011). In Asian countries,
by 0.17 mmol/L after 57 days of soy protein consumption, especially in Japan, women and men taking Japanese tradi-
which is twice more reduction compared with milk protein tional diet, such as consumption of tofu, miso soup, and natto,
consumption (0.08 mmol/L). This indicates that soy protein have low mortality with breast cancer (Smith 1956; Dunn
Appl Microbiol Biotechnol (2012) 96:9–22 13

1975; Nomura et al. 1978) and prostate cancer (Breslow et al. et al. 1999). According to the results of numerous studies,
1977). An investigation examining the isoflavones extracted soybean isoflavones have a beneficial effect on bone health,
from urinary excretion has shown that Japanese women con- which facilitates not only the prevention of estrogen-related
suming a traditional Japanese diet exhibit ten times higher bone loss but also the improvement of bone strength
amount of daidzein (Da; ~ 2.6 μmol/day) compared with (Picherit et al. 2000; Arjmandi et al. 2003; Chen et al.
women who resided in Boston (Da~0.32 μmol/day) and in 2003; Atkinson et al. 2004; McCue and Shetty 2004). The
Helsinki area (Da~0.22 μmol/day) (Adlercreutz et al. 1986; effect of soy isoflavone supplementation on bone health has
Adlercreutz et al. 1991). Moreover, the values of the other two been testified by a statistical analysis in 403 postmenopausal
estrogenic compounds, equol (Eq) and O-desmethylangolen- women (Wong et al. 2009). The adjusted whole-body bone
sin (O-Dma), analyzed from urinary excretion in Japanese mineral density (BMD) values in the group with daily intake
women were 2.6±0.4 and 0.7±0.6 μmol/day, respectively, of 120 mg soy isoflavone at 1 and 2 years were estimated to
which were both 20–30 times more than those in women be 1.093 and 1.083 g/cm2, respectively. Those are both
living in Boston (Eq~0.1 μmol/day; O-Dma~0.03 μmol/day) significantly higher than the values analyzed from the pla-
and in Helsinki (Eq~0.07 μmol/day; O-Dma~0.03 μmol/day) cebo group (at 1 year, 1.087 g/cm2; at 2 years, 1.076 g/cm2).
(Adlercreutz et al. 1986). In addition, Wu et al. have demon- The results indicate that a suppression of whole-body BMD
strated that the increased intake of tofu associates closely with reduction took place in the subjects receiving a daily sup-
the reduced risk of breast cancer in a case–control study plement of 120 mg soy isoflavone in comparison with the
of pre- and post-menopausal Asian-American women (Wu placebo group both at 1 and 2 years of treatment, which
et al. 1996). implies that soy isoflavone possesses a potential for protec-
Men living in Eastern countries having more soyfoods tion against osteoporosis. Moreover, an observational study
intake exhibit much higher levels of isoflavone and lower has been performed to assess the effects of genistein on bone
prostate cancer mortality in comparison with those living in metabolism in 389 postmenopausal women (Marini et al.
Western countries. For instance, the amount of plasma iso- 2007). After a daily intake of 54 mg genistein for 24 months,
flavonoid in Japanese men has been found to be 7–110 times an increase of BMD was observed both at the anteroposte-
higher than that of Finnish men (Adlercreutz et al. 1993). rior lumbar spine and the femoral neck by 0.049 and
This implication of isoflavonoid related to prostate cancer 0.035 g/cm2, respectively. On the contrary, the placebo
has been demonstrated in animal studies by investigating the recipients experienced a decrease of BMD after the same
protective effect against the development of prostate cancer. period. Conclusively, 24 months of treatment with the phy-
The investigation of the development of adenocarcinomas in toestrogen genistein exhibits positive effects on BMD in
the prostate and seminal vesicles of F344 rats with a treat- osteopenic postmenopausal women.
ment of a diet containing an isoflavone mixture (74 % Various studies have been lately reported to verify the
genistein and 21 % daidzein) has shown lower carcinoma effect of long-term soy isoflavone consumption on bone
incidence in both prostate and seminal vesicles of rats fed by health (Chen et al. 2004; Marini et al. 2007; Brink et al.
isoflavone diet (carcinoma incidence: control, 60 %; 100 2008). However, the duration of trials recording the changes
parts per million isoflavone diet, 38 %; 400 parts per million was almost more than 1 year. Treatment with 57.8 mg iso-
isoflavone diet, 30 %) (Onozawa et al. 1999). Inhibition of flavone per 100 g diet on growing female rats for 9 weeks
tumor incidence by soybean isoflavones further suggests a provides a more direct evidence to assess the effect of soy
possible relationship between isoflavones intake and reduced isoflavone on bone health (Jo and Choi 2008). The results
risk both in breast cancer and prostate cancer (Constantinou show that the group with isoflavone-supplemented diet
et al. 1996; Kim et al. 2008). tended to have higher BMD than the control group between
Moreover, high consumption of soyfoods brings the pos- three and nine experimental weeks, which implies that iso-
sibilities to reduce the risk of endometrial cancer among flavone affects positively the formation of spine and femur
Chinese women in Shanghai (Xu et al. 2004). On the other BMD of growing female rats. As a result, long-term soybean
hand, black soybean extract has also been proved to suc- or soy product intake has strongly been recommended and
cessfully suppress the growth of gastric cancer cells (Zou suggested to lower the risk of osteoporosis in nutriology.
and Chang 2011).
Antioxidant activities
Protection against osteoporosis
Free radicals formed in the human body serve a significant
Osteoporosis is a progressive systemic skeletal disorder role to fight against intruders such as bacteria and viruses.
characterized by reduced bone mass and poor bone quality, However, free radicals reacting with some essential mole-
especially taking place in postmenopausal women due to the cules such as DNA, membranes, and proteins may cause
dramatic decrease of estrogen during menopause (Meunier life-threatening damages. By virtue of the property in
14 Appl Microbiol Biotechnol (2012) 96:9–22

isoflavones to scavenge free radicals, the long-term intake of soybeans, dehydrated soybeans, soy sprouts, whole-fat and
soybean exhibits the antioxidant potential to reduce the risk defatted soybeans, soy flour, soymilk and its products, tofu,
of cancer by preventing free radical damage to DNA (Wei et okara, and yuba (Su 1999). Fermented soyfoods include
al. 1995; Arora et al. 1998). In addition, isoflavone with miso, soy sauces, natto, tempeh, and fermented tofu. West-
potent antioxidant activity may be a useful therapy to lower erners have adopted some of these soyfoods as their daily
LDL cholesterol oxidation (Patel et al. 2001; Takahashi et diet, whereas others, especially the fermented ones, still
al. 2005). Previous studies have shown that genistein is the need more time to be accepted. Soymilk, tofu, soy sauce,
most potent antioxidant among the soy isoflavones, followed and miso are the most popular soyfoods in the USA (Fig. 1).
by daidzein (Wei et al. 1996; RuizLarrea et al. 1997). More- Americanized soyfoods such as tofu hot dogs, tofu ice
over, in the field of medical science, genistein has been creams, veggie burgers, soymilk yogurt and cheese, and
addressed to provide in vivo protection from acute myelotox- soy flour pancake are available in both supermarkets and
icity through extended quiescence followed by reduced senes- traditional markets. A brief introduction of these four pop-
cence of marrow repopulating LSK (+) (Davis et al. 2008). ular soyfoods is provided.
Genistein treatment on adult mice reveals a protection against
ionizing radiation injury (Landauer et al. 2003). Recently, the Soymilk
in vitro antioxidant potential and in vivo radioprotective abil-
ity of soy isoflavones have been investigated (Dixit et al. Soymilk is one of the traditional drinks in the Eastern world,
2012). Male rats were orally fed with soybean isoflavones providing eight essential amino acids for human beings
(60 mg/kg) for 21 days followed by gamma irradiation expo- (Rivas et al. 2002). The heating process is an inactivating
sure. The pretreatment of rats with isoflavones prior to gamma step that will remove the beany flavor within soymilk. Raw
irradiation delayed or reduced the severity of irradiation sick- soymilk also serves as the base of a variety of soy products,
ness and increased the 30-day survival rate to 33.3 %. Pre- including tofu, soy yogurt, and cheeses (Dwyer et al. 1994;
treatment with isoflavones also reduced lipid peroxidation and Trindade et al. 2001; Liu et al. 2006).
enhanced the activity of antioxidant enzymes, which suggests
that intake of isoflavones not only brings in more potent Tofu
antioxidant activity but also acts as a radioprotector against
gamma radiation-induced oxidative damage. Tofu (Fig. 2) appeared in American supermarkets in 1980s.
With the exceptional nutrient content and health benefits They are usually served as desserts and side dishes as well as
mentioned earlier, soybeans become an indispensable food ingredients of soup. The extracted soymilk was coagulated
material in our daily life. Most importantly, many ingre- (by salt or acid) and pressed to form tofu. Tofu can be stored
dients of soybeans can be used as health supplement. Recent up to 1 year with novel pasteurization and packing techniques.
studies on the health benefits of soyfoods intake are sum-
marized in Table 2. Soy sauce

Soy sauce originated in China 2,500 years ago and it is a

Soyfoods: processing and products fermented soybean condiment produced by Aspergillus ory-
zae and/or Aspergillus soyae molds (Su 1999). The fer-
Non-fermented and fermented soyfoods mented paste was pressed to yield liquid. This savory
seasoning sauce is now widely used in both Oriental and
Asian people have been consuming soybeans in various American cuisine. The manufacturing process is significant-
ways for more than 1,000 years (Su 1999). In the past ly affected by temperature and sodium chloride concentra-
decades, those soyfoods begun to be introduced into Western tion (Su et al. 2005). Our study demonstrated that the
cultures and diets. There are many choices of soyfoods avail- optimal temperatures for both protease and amylase were
able in the world today (Table 3). Some of them are produced found in the range of 50–55 °C. However, protease was not
through modern processing techniques in large food compa- stable at 55 °C and retained only at around 20 %. A com-
nies, whereas others are produced in more traditional ways bination of 5 % sodium chloride and fermentation at 45 °C
and even by an individual family. was considered as the best condition for the prohydrolysis of
Soybeans must be cooked in order to destroy the trypsin koji for making soy sauce.
inhibitors which reduce the availability of trypsin, an en-
zyme essential to the nutrition of many monogastric ani- Miso
mals, before being served as food. Soyfoods are usually
divided into two categories: non-fermented soyfoods and Miso is a traditional Japanese fermented product using
fermented soyfoods. Non-fermented soyfoods include fresh soybeans, rice, and/or barley with salt and molds (Yamabe
Appl Microbiol Biotechnol (2012) 96:9–22 15

Table 2 Summary of health benefits of soyfoods and soy products

Health benefits Significances References

Anti-inflammatory Fermented soymilk prepared with lactic acid bacterium and bifidobacterium Liao et al. 2010
activity dose-dependently suppress nitric oxide production of lipopolysaccharide-
induced macrophages
Reduce risk of Soy isoflavones significantly reduced serum total and LDL cholesterol Taku et al. 2007
cardiovascular but did not change the level of HDL cholesterol
disease Consumption of soy protein is capable of modulating some serum lipids Pipe et al. 2009
for reducing CVD risk in adults with type 2 diabetes
Fermentation of black soybeans with Aspergillus awamori significantly enhanced Chen et al. 2011
the LDL oxidation inhibitory activity, total phenolics, and amino nitrogen contents
Fermentation of soybean with Bacillus spp. as a bioprocess to enhance Juan et al. 2010
anthocyanin content, the angiotensin-converting enzyme inhibitory effect
Cancer prevention Phytoestrogens exhibit safe and positive response for hormone replacement Sakamoto et al. 2010
therapy and breast cancer prevention by investigating the effect of daidzein,
genistein, coumestrol, and resveratrol on cell growth
Soy extract is more potent than a diet containing genistein in the inhibition Kim et al. 2008
of tumor growth, suggesting that the soy extract possesses the synergistic
effect of the various bioactive components in cancer prevention
Black soybean extract could be used as an apoptosis inducer in AGS cells Zou and Chang 2011
and a natural chemopreventive agent in the treatment of human gastric cancer
Protection against Daily supplementation with 120 mg soy hypocotyl isoflavones reduces whole-body bone loss Wong et al. 2009
osteoporosis but does not slow bone loss at common fracture sites in healthy postmenopausal women
Genistein statistically significantly lowered urinary excretion of pyridinoline and Marini et al. 2007
deoxypyridinoline, increased levels of bone-specific alkaline phosphatase and insulin-like
growth factor I, and did not change endometrial thickness compared with placebo control
Isoflavone supplementation increased spine BMD per weight in the 6th week of Jo and Choi 2008
feeding and affected the increase of femur BMD in the 9th week, which implies
that it affects positively the formation of spine and femur BMD of growing female rats.
The possibility that the effects of isoflavone on the pattern of BMD formation
might differ from the parts of bones has also been suggested
Antioxidant activities The antioxidant properties of isoflavones are structurally related and the hydroxy group Wei et al. 1995
at Position 4′ is crucial. Dietary administration of 250 ppm genistein for 30 days significantly
enhances the activities of antioxidant enzymes in the skin and small intestine of mice
Pretreatment with soy isoflavone, prior to gamma irradiation resulted in the increased Dixit et al. 2012
survival rate of the animals as compared to irradiated group. The results suggest that
consumption of isoflavone has potent antioxidant activity and that it acts as
probable radio protector against gamma radiation-induced oxidative damage
The inhibitory activity of black soybeans on LDL oxidation being more effective Takahashi et al. 2005
than yellow beans is attributed to the dark seed coat of black soybeans

et al. 2007). Different molds will help to make different The US Food and Drug Administration (FDA) has accepted
flavors of miso (El-Shenawy et al. 2012). In addition to SBIFs as safe for use as the sole source of nutrition.
many Japanese-style meals, miso is now used in the devel-
opment of New Age cooks and health diets due to its rich Meat and dairy substitutes
flavors and healthful benefits.
Nowadays, more soybean products have been commer- Soybeans can be processed to produce a texture and appear-
cialized ranging from dietary supplement to animal hus- ance similar to many other foods such as meat and dairy
bandry because of its high nutrition content and many products. Extra nutrients including calcium, vitamins, and
bioactive ingredients (Fig. 3). minerals are also added by many manufacturers to make soy
products nutritionally equivalent to animal protein (Key et
Infant formula al. 2006; Craig 2009).

Soy-based infant formula (SBIF) is used for infants who are Cattle feed
allergic to pasteurized cow milk proteins (Badger et al.
2009; Chen et al. 2009). Partawihardja (1990) first reported Cattles are often fed soybeans because they are relatively
that the usage of tempeh-formula infant foods in infant and cheap. Spring grasses are rich in omega-3 fatty acids where-
children-under-five diets can overcome diarrheal problems. as soy predominantly has omega-6. Moreover, due to its
16 Appl Microbiol Biotechnol (2012) 96:9–22

Table 3 Some popular traditional fermented soyfoods and their sources

Products Description Origin of cuisine

Chungkookjang/Cheonggukjang Steamed black soybean fermented with B. subtilis for Korea

several days without salt
Doenjang A traditional Korean condiment made from fermentation Korea
of soybean paste block and rice by B. subtilis
Fermented bean curd/Chinese cheese/ A soft cheese-type mold-fermented product which is made from soybean China, Taiwan
pickled tofu/ sufu/tao-hu-yi/fu-su/ curd by the action of fungal culture, such as Mucor spp., Actinomucor spp.,
fu-zu/, to-fu-zu and A. oryzae, then soaked in brine with select flavorings
Gochujang A savory and pungent fermented Korean condiment made Korea
from red chili, glutinous rice, fermented soybeans and salt.
In shi, tau si, douchi Dried by-product of the mash black soybean sauce China, Taiwan,
fermented with A. oryzae Philippines
Miso A traditional Japanese seasoning produced by fermenting Japan
rice and soybeans with salt and the fungus kōjikin
Natto A traditional Japanese soybean product fermented with B. subtilis Japan
Soy sauce Sauces made by mixing defatted soybean and wheat grains with mold Asian countries
cultures such as A. oryzae and other related microorganisms and yeasts
Stinky tofu A strong-odor fermented tofu prepared by marinating fresh China, Taiwan ,
tofu in a fermented stinky liquid or brine for a few hours Hong Kong
Sweet bean sauce/Tianmianjiang A thick, dark brown- or black-colored Chinese sauce made from wheat flour, China
sugar, salt, leaving agent, and by-product of fermented yellow soybean,
which is left over from the fermentation of soybeans to make soy sauce
Tauco A Chinese-Indonesian cuisine paste made from preserved fermented soybeans Indonesia
Tempeh A traditional fermented soybean cake from black or yellow Indonesia
soybean fermented with R. oligosporus
Thua-nao A traditional non-salted wholesoybean fermented like Japanese Thailand
natto by mixing with Bacillus spp.
Tuong A salty paste with thick consistency made from roasted soybeans Vietnam
fermented with A. oryzae or B. subtilis

ability to offer lysine, soybean meal (SBM) has been used as value of soybean meal proteins for ruminants (Elwakeel et
a good protein supplement for ruminants (Schingoethe al. 2012).
1996). In general, SBM is always heated to destroy anti-
trypsin factors. However, it is questionable that the high Other products
heating temperature would cause the degradation of proteins
in SBM. Elwakeel et al. have demonstrated the evidence to Soybeans are also commercialized in many industrial prod-
reveal that the heating process disables to affect the nutritive ucts including oils, soap, cosmetics, resins, plastics, inks,

Fig. 1 Commercial soyfoods in an Asian supermarket (photo by Fig. 2 Consumers are purchasing tofu in a Chinese grocery market
Kuan-Chen Cheng) (Pittsburg, PA, USA; photo by Kuan-Chen Cheng)
Appl Microbiol Biotechnol (2012) 96:9–22 17

Fig. 3 Flow diagram of Miso

soybean processing to Tempeh
commercial soy products Soy oil
Natto steamed/
Douchi fermentation

steamed
Soy paste Defatted
soy flour
fermentation water/ hot water
ethanol
Soy sauce Soybeans
hot water solvent
extraction
Soy protein
Soy milk concentrate Low fat soy milk
calcium
fermentation
coagulation Bioactive
compounds:
Tofu Soy yogurt isoflavones,
Soy custard Soy cheese anthocyanin
etc.

crayons, solvents, and clothing. Soybean oil is the primary food materials exist in glycosylated form and cannot be
source of biodiesel in the USA (though with some ethical easily absorbed in the intestine. Some reports address the
concerns), accounting for 80 % of domestic biodiesel pro- aglycosylation process of isoflavones during fermentation
duction (Siqueira et al. 2008; Kim and Dale 2009). Soy- by lactic acid bacteria, filamentous fungi, basidiomycetes,
beans have also been used since 2001 as fermenting stock in and Bacillus subtilis with their high β-glucosidase activity
the manufacture of a brand of vodka (Sustainability Fact (Kuo et al. 2006; Wu and Chou 2009; Cheng et al. 2010).
Sheet, National Biodiesel Board, 2008). Fiber-rich materials We have reported that the isoflavone conversion of black
including desalted shoyu mash residue, alcohol-insoluble soybean can be achieved by immobilized Rhizopus spp.
solid, and water-insoluble solid were prepared from shoyu (Cheng et al. 2010). In our study, R. oligosporus NTU-5
mash residue, which is a filtration cake obtained during the isolated from our lab has the highest DPPH radial scaveng-
isolation of shoyu by press filtration of fermented matrix in ing effect and isoflavone aglycosylation rate among the
the final process (Yeh et al. 2005). These fiber-rich materials strains studied and, therefore, was chosen for scaled up
might be a potent fiber source for health foods. black soybean fermentation in a 5-L bioreactor with Luffa
cylindrica fiber. Results indicated that the isoflavone agly-
cosylation rate of daizin and genistin was 77.7 and 31.8 %,
Microorganisms enhance the bioactivity respectively. Moreover, an unknown compound was
of fermented soyfoods obtained from the ethanol extract of 2-day fermented black
soybean milk by immobilized R. oligosporus NTU 5 which
Fermented soybean with enhanced bioactivity has a strong DPPH effect (76 %). Fermented black soybean
milk that possesses high antioxidative activity as well as
Food microbiology is a study of the interaction between cytotoxic activity toward cancer cells was due to the higher
microorganisms and food products. The first application of daidzein and genistein (aglycone form) content compared
microorganism on food processing can be traced back to with the unfermented milk (Cheng et al. 2011). In our study,
around 1600 BC (Su 1999). Yeast, especially Saccharomyces cell viability assay demonstrated that the fermented black
cerevisiae, is used to leaven bread, brew beer, and make wine. soybean extract exhibited selective cytotoxic activity towards
Food fermentation includes ancient technologies that utilize human carcinoma cells Hep 3B ( IC50 0150.2 μg/ml) but
microorganisms and their enzymes to improve the human diet. did not significantly affect normal human lung fibroblasts
Fermented foods have enhanced flavors, textures, and aromas (MRC-5). Soybean itself may possess enzymes with β-
and may also possess certain health benefits, including higher glucosidase activity with strict specificity toward glucosyl
bioactivity and superior digestibility (Su 1999). isoflavones but not malonyl-glucosidic conjugates (Chiou et
Aglycone isoflavones, for example, exhibit many bioac- al. 2010). In this study, a novel β-glucosidase was isolated
tivities, such as antioxidation, antimutagenic effects, and from soybean okara, which was inhibited by 1 mM of Hg2+ or
reduction of symptoms of post-menopause (McCue and 10 mM of Al3+ion, and glucose and mannose also affected the
Shetty 2004). However, most of the isoflavones in natural activity.
18 Appl Microbiol Biotechnol (2012) 96:9–22

Miso is another excellent example as a fermented soy- used in processed foods and oriental cuisine, making it
bean product. The fungus kōjikin was used to ferment challenging to avoid. The good news is that the majority
steam-cooked soybeans. The taste, aroma, texture, and ap- of babies who have soy allergies outgrow them by the age of
pearance of miso vary by region and season since a different 3 (Cordle 2004). Although soy protein has been used in
kōjikin was incorporated. Miso is high in vitamin B12 which infant feeding for more than 100 years, the popularity of soy
can reduce the risk of pernicious anemia. Some even suggest infant formula (SIF) varies substantially in different parts of
that miso can help treat radiation sickness. Miso is also a the world. The controversies regarding SIF concern mainly
source of Lactobacillus acidophilus considered to have pro- the adverse effects, related to its content in phytate, alumi-
biotic characteristics (Ljungh and Wadström 2006). Leci- num, stachyose, raffinose, and especially phytoestrogens
thin, a type of phospholipid resulting from fermentation, is (Vandenplas et al. 2011)
effective in the prevention of high blood pressure. Table 4
summarizes the microorganisms that are used as the work- GRAS microorganisms
ing strains in soybean industry.
FDA classifies chemicals, substances, and microorganisms
added to food that are considered safe by experts as gener-
Safety concerns of soybeans ally recognized as safe (GRAS) (Federal Food, Drug, and
Cosmetic Act 1938). These additives are exempted from the
Allergy usual Federal Food, Drug, and Cosmetic Act (FFDCA) food
additive tolerance requirements. As mentioned previously,
Soy allergy is common and usually happens among younger many soy products exhibit higher or novel bioactivities after
children, especially babies. Soy is one of the so-called big having been fermented with microorganisms. Although
eight allergens, and along with egg allergies and milk aller- nearly all microorganisms used for food fermentation are
gies, it is one of the three allergies children are most likely to not disease causers (pathogens) and in that sense would be
outgrow (Cordle 2004). Soy allergy may cause serious “safe,” the FDA regulations remain strict with food process-
urticaria and angioedema and can happen within minutes ing because of concern of public health. Fermented food
to hours after consumption. While soy products are not as products with non-GRAS organisms are subject to premar-
prevalent in the USA as they are in Asia, they are widely ket approval mandated by the FFDCA.

Table 4 Microorganisms used for fermented soybean products

Microorganisms Products Beneficial effects References

A. oryzae, A. soyae Soy sauce Contains ten times the antioxidants of red wine Su 1999
and helps prevent cardiovascular diseases
L. acidophilus (kōjikin) Miso Different molds will help to make Yamabe et al. 2007; Ljungh
different flavors of miso and Wadström 2006
B. subtilis Black soybean paste Enhancement of aglycone, vitamin K2, and Wu and Chou 2009
superoxide dismutase activity of black soybean
Natto produces a distinctive smell, somewhat akin Shurtleffand Aoyagi, 2012
to a pungent cheese; nattokinase is available
as a dietary supplement
Black soybean drinks Enhanced isoflavone aglycones Kuo et al. 2006
Rhizopus spp. Black soybean drinks Enhanced antioxidant activity (DPPH radial Cheng et al. 2010;
scavenging effect) and isoflavone aglycones; Cheng et al. 2011
cytotoxicity toward Hep 3B cancer cells
L. acidophilus, L. paracasei, Soy frozen dessert The frozen soy dessert was a suitable food Heenan et al. 2004
B. lactis, L. rhamnosus, for the delivery of bacterial probiotic strains
S. boulardii with excellent viability and acceptable
sensory characteristics
B. longum, L. paracasei, Soymilk Enhanced isoflavone aglycones Pham and Shah 2007
B. animalis, B. breve
Rhizopusmicrosporus, Tempeh Enhanced protein hydrolysate content Nout and Rombouts 1990
R. microsporus, R. oligosporus, with a pleasant sensory characteristics
R. rhizopodiformis, R. chinensis
Actinomucor spp., Mucor spp., Sufu or furu Creates a cheese-like product with a spreadable Han et al. 2001
and Rhizopus spp. creamy consistency and a pronounced flavor
Appl Microbiol Biotechnol (2012) 96:9–22 19

Future and prospects Adlercreutz H, Fotsis T, Bannwart C, Wahala K, Makela T, Brunow G,

Hase T (1986) Determination of urinary lignans and phytoestro-
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Hasegawa T, Okada H (1991) Urinary excretion of lignans
Novel technologies to enhance soybean productivity are there-
and isoflavonoid phytoestrogens in Japanese men and women
fore necessary. The whole soybean genome project was initi- consuming a traditional Japanese diet. Am J Clin Nutr 54(6):1093–
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aiming at the genetic manipulation of high yield potential, Waters V, Williams CL (2009) Health benefits of dietary fiber.
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Andres S, Abraham K, Appel KE, Lampen A (2011) Risks and benefits
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of dietary isoflavones for cancer. Crit Rev Toxicol 41(6):463–506
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Phytoestrogens, especially aglycone isoflavones, can act like Wild RA (2003) Soy protein has a greater effect on bone in
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of free radicals. These make soybean products very competi- isoflavones and their biological metabolites in a liposomal sys-
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Atkinson C, Compston JE, Day NE, Dowsett M, Bingham SA (2004)
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Industry suffers from a lack of employment for its surplus Am J Clin Nutr 79(2):326–333
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