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Fermentation of Chinese sauerkraut in pure culture and binary co-culture with Leuconostoc mesenteroides and Lactobacillus plantarum Tao Xiong a, b, * , Fei Peng a, b , Yanyan Liu a, b , Yaojun Deng a, b , Xinyue Wang a, b , Mingyong Xie a a State Key Laboratory of Food Science & Technology, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China b College of Life Science & Food Engineering, Nanchang University, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China article info Article history: Received 3 March 2014 Received in revised form 3 May 2014 Accepted 29 May 2014 Available online 6 June 2014 Keywords: Chinese sauerkraut Lactic acid bacteria Fermentation Pure culture Co-culture abstract The characteristics of Chinese sauerkraut fermented by Leuconostoc mesenteroides NCU1426, Lactobacillus plantarum NCU1121 and binary co-culture (Leu. mesenteroides NCU1426-L. plantarum NCU1121) were studied. The mixture of materials was sterilized rstly, and then was fermented for seven days in the inoculation with lactic acid bacteria. The pH value and number of viable cells of lactic acid bacteria in the brine were monitored during the fermentation. The changes in the concentrations of substrates and products in the three fermentations were analyzed by high performance liquid chromatography. The study has determined the characteristics of Chinese sauerkraut fermentation in pure culture fermenta- tion with either Leu. mesenteroidies NCU1426 or L. plantarum NUC1121 and by binary co-culture as well as the interaction among the two lactic acid bacteria used. © 2014 Elsevier Ltd. All rights reserved. 1. Introduction The products fermented by probiotics such as lactic acid bacteria (LAB) are consumed far and wide. The probiotic potential of LAB has been proved in various fermented foods (Zago et al., 2011). Sauer- kraut, a fermented food, is benecial to human health and plays an important role in human nutrition, because it is rich in minerals, calcium, phosphorus, iron, sodium, potassium and phenolic com- pounds and even has higher contents of vitamin B and C than unfermented cabbage (Pe~ nas et al., 2012; Rabie, Siliha, el-Saidy, el- Badawy, & Malcata, 2011). Chinese sauerkraut fermented mainly by LAB was dated to Zhou Dynasty (Li, 2006) and spread to Europe in the 17th century (Chen, 2007). There are many microorganisms that have been used in the spontaneous fermentation of sauerkraut, such as Leuconostoc mesenteroides, Lactobacillus plantarum, Ped- iococcus pentosaceus, Lactobacillus brevis and some yeasts (Plengvidhya, Breidt, & Fleming, 2004; Tolonen et al., 2004; Xiong, Guan, Song, Hao, & Xie, 2012; Zhong & chao, 1995). Numerous re- searchers have studied the effects of LAB on sauerkraut fermentation. It was reported that Leu. mesenteroides, a hetero- fermentative LAB, was a starter in spontaneous fermentation of sauerkraut, and L. plantarum, a homofermentative LAB, terminated the fermentation of sauerkraut (Fleming, McFeeters, & Daeschel, 1985; Plengvidhya et al., 2004). It is known that natural fermen- tation processes in food are complex, including interactions among fermentable substrates and microbes. Microbial interactions were believed to have an impact on the outcome of food fermentation processes (Eddy & Christophe, 2013; Pe~ nas, Frias, Gomez, & Vidal- Valverde, 2010). In 1950, Pette rstly conrmed the mutualism relationship between Lactobacillus bulgaricus and Streptococcus thermophilus (Wu, Ma, Pei, & Zhang, 2003). Oliveira, Perego, Oliveira, and Converti (2012a, 2012b) found that the co-culture of S. thermophilus and L. bulgaricus produced a higher level of acetoin and a lower level of diacetyl compared with the co-culture of S. thermophilus and L. acidophilus in fermented milk. Gobbetti, Corsetti, and Rossi (1994) reported that the LAB-yeast culture did not modify the yield of mono-culture yeast cells, but the yeast stimulated LAB through its metabolism of carbohydrates. However, the interaction among LAB as well as characteristics of Chinese sauerkraut fermented by binary co-culture fermentation have not been reported. The aim of this study was to investigate the fermentative be- haviors of two LAB in pure culture or binary co-culture fermenta- tion of Chinese sauerkraut including a) formation of lactic acid, * Corresponding author. State Key Laboratory of Food Science & Technology, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China. Tel.: þ86 13697084048; fax: þ86 791 3063627. E-mail address: [email protected] (T. Xiong). Contents lists available at ScienceDirect LWT - Food Science and Technology journal homepage: www.elsevier.com/locate/lwt http://dx.doi.org/10.1016/j.lwt.2014.05.059 0023-6438/© 2014 Elsevier Ltd. All rights reserved. LWT - Food Science and Technology 59 (2014) 713e717

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Fermentation of Chinese sauerkraut in pure culture and binaryco-culture with Leuconostoc mesenteroides and Lactobacillus plantarum

Tao Xiong a, b, *, Fei Peng a, b, Yanyan Liu a, b, Yaojun Deng a, b, Xinyue Wang a, b,Mingyong Xie a

a State Key Laboratory of Food Science & Technology, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR Chinab College of Life Science & Food Engineering, Nanchang University, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China

a r t i c l e i n f o

Article history:Received 3 March 2014Received in revised form3 May 2014Accepted 29 May 2014Available online 6 June 2014

Keywords:Chinese sauerkrautLactic acid bacteriaFermentationPure cultureCo-culture

* Corresponding author. State Key Laboratory of Fo235 Nanjing East Road, Nanchang, Jiangxi, 33013697084048; fax: þ86 791 3063627.

E-mail address: [email protected] (T. Xiong)

http://dx.doi.org/10.1016/j.lwt.2014.05.0590023-6438/© 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

The characteristics of Chinese sauerkraut fermented by Leuconostoc mesenteroides NCU1426, Lactobacillusplantarum NCU1121 and binary co-culture (Leu. mesenteroides NCU1426-L. plantarum NCU1121) werestudied. The mixture of materials was sterilized firstly, and then was fermented for seven days in theinoculation with lactic acid bacteria. The pH value and number of viable cells of lactic acid bacteria in thebrine were monitored during the fermentation. The changes in the concentrations of substrates andproducts in the three fermentations were analyzed by high performance liquid chromatography. Thestudy has determined the characteristics of Chinese sauerkraut fermentation in pure culture fermenta-tion with either Leu. mesenteroidies NCU1426 or L. plantarum NUC1121 and by binary co-culture as well asthe interaction among the two lactic acid bacteria used.

© 2014 Elsevier Ltd. All rights reserved.

1. Introduction

The products fermented by probiotics such as lactic acid bacteria(LAB) are consumed far andwide. The probiotic potential of LAB hasbeen proved in various fermented foods (Zago et al., 2011). Sauer-kraut, a fermented food, is beneficial to human health and plays animportant role in human nutrition, because it is rich in minerals,calcium, phosphorus, iron, sodium, potassium and phenolic com-pounds and even has higher contents of vitamin B and C thanunfermented cabbage (Pe~nas et al., 2012; Rabie, Siliha, el-Saidy, el-Badawy,&Malcata, 2011). Chinese sauerkraut fermentedmainly byLAB was dated to Zhou Dynasty (Li, 2006) and spread to Europe inthe 17th century (Chen, 2007). There are many microorganismsthat have been used in the spontaneous fermentation of sauerkraut,such as Leuconostoc mesenteroides, Lactobacillus plantarum, Ped-iococcus pentosaceus, Lactobacillus brevis and some yeasts(Plengvidhya, Breidt, & Fleming, 2004; Tolonen et al., 2004; Xiong,Guan, Song, Hao, & Xie, 2012; Zhong & chao, 1995). Numerous re-searchers have studied the effects of LAB on sauerkraut

od Science & Technology, No.047, PR China. Tel.: þ86

.

fermentation. It was reported that Leu. mesenteroides, a hetero-fermentative LAB, was a starter in spontaneous fermentation ofsauerkraut, and L. plantarum, a homofermentative LAB, terminatedthe fermentation of sauerkraut (Fleming, McFeeters, & Daeschel,1985; Plengvidhya et al., 2004). It is known that natural fermen-tation processes in food are complex, including interactions amongfermentable substrates and microbes. Microbial interactions werebelieved to have an impact on the outcome of food fermentationprocesses (Eddy & Christophe, 2013; Pe~nas, Frias, Gomez, & Vidal-Valverde, 2010). In 1950, Pette firstly confirmed the mutualismrelationship between Lactobacillus bulgaricus and Streptococcusthermophilus (Wu, Ma, Pei, & Zhang, 2003). Oliveira, Perego,Oliveira, and Converti (2012a, 2012b) found that the co-culture ofS. thermophilus and L. bulgaricus produced a higher level of acetoinand a lower level of diacetyl compared with the co-culture ofS. thermophilus and L. acidophilus in fermented milk. Gobbetti,Corsetti, and Rossi (1994) reported that the LAB-yeast culture didnot modify the yield of mono-culture yeast cells, but the yeaststimulated LAB through its metabolism of carbohydrates. However,the interaction among LAB as well as characteristics of Chinesesauerkraut fermented by binary co-culture fermentation have notbeen reported.

The aim of this study was to investigate the fermentative be-haviors of two LAB in pure culture or binary co-culture fermenta-tion of Chinese sauerkraut including a) formation of lactic acid,

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Fig. 1. Acidification profiles of sauerkraut fermentations by starter cultures and binaryco-culture (n ¼ 4).

T. Xiong et al. / LWT - Food Science and Technology 59 (2014) 713e717714

acetic acid and ethanol from sugar and organic acid, b) change of pHvalue, and c) biomass growth.

2. Materials and methods

2.1. Microorganisms

The strains used in this study, Leu. mesenteroides NCU1426(L.eu1426) and L. plantarum NCU1121 (L.p1121), were isolated fromspontaneous fermentation of Chinese sauerkraut in our laboratory.

2.2. Preparation of Chinese sauerkraut

All materials including garlic (3%), Chinese prickly ash (1.5%), hotred pepper (4%), ginger (2%), salt (4%) and crystal sugar (4%) werepurchased from a supermarket in Nanchang, Jiangxi Province,China. The percentages above were determined by the weight ofwater used in the fermentation. Cabbages were washed, dried, cutinto small pieces and then were put into 5 L pickle jars togetherwith the other materials except crystal sugar and salt. Crystal sugarand salt together with water were put into a 5 L triangular flask. Allmaterials abovewere sterilized at 105 �C for 20min. It was reportedthat there were little differences in chemical composition ofvegetable juice medium by heat treatment (110 �C, 10 min)compared with untreated control (Gardner, Savard, Obermeier,Caldwell, & Champagne, 2001). When the temperature of thesematerials dropped to room temperature after sterilization, themixture of crystal, salt and water was added to the 5 L pickle jar.

2.3. Preparation of inoculum and fermentation

LAB was prepared in MRS broth by inoculating its colony. Thecell number was approximately 9 Log CFU/mL after activation inMRS broth at 37 �C for 18 h. Cells of LAB were harvested bycentrifugation at 4500 rpm for 15 min and thenwashed twice with0.9% saline. For all cultures, the initial cell counts in the fermenta-tion were about 3e4 Log CFU/mL.

The pickle jar was filled with water to exclude air, and then keptat ambient temperature (25e27 �C). The culture system wasmonitored for seven days to ensure the growth of LAB, substratemetabolism and metabolite formation.

2.4. Analytical methods

Brine samples were collected at different time points duringfermentation. The enumerations of LAB (L.eu1426 and L.p1121)were performed in MRS agar media supplemented with 0.4% (w/v)bromocresol purple (Guoyao Chemical Company, China). Brinesamples (1 mL) were aseptically transferred to 9 mL sterile physi-ological saline and then appropriately diluted (Vergara, Blana,Mallouchos, Stamatiou, & Panagou, 2013). Three appropriatelydiluted samples were chosen to determine the number of viablecells of LAB. The species in the MRS agar flat were distinguished bycolonial morphology. The pH value in the brine was monitoredusing a pH meter (PHS-25, Shanghai Precision Scientific In-struments Company, China).

The concentrations of substrates (sucrose, glucose, fructose,critic acid, malic acid and pyruvic acid) and products (lactic acid,acetic acid and ethanol) were determined by a high performanceliquid chromatograph (HPLC) (Model 1200, Agilent, USA). Thesystem was composed of a refractive index detector, a UV detectorand four pumps. Separation was achieved using an Aminex HPX-87H, 300 � 7.8 mm ion-exchange column (Bio-Rad, Hercules, CA,USA) at 45 �C with 6 mM sulfuric acid as an eluent at a flow rate of0.5mL/min. The detectedwavelength of the UV detector for organic

acids was 205 nm. The samples were centrifuged at 12,000 rpm for10 min, and then the supernatant was filtrated through 0.22 ummembrane filter.

2.5. Statistical analysis

Data were expressed as mean values ± standard deviations.Influences of the various parameters were assessed by one wayanalysis of variance (ANOVA). They were compared by Data Anal-ysis and Graphing Software Origin 8.5 at a significance level ofp < 0.05.

3. Results and discussion

3.1. Acidification profiles

Fig.1 showed the acidification curves of the culture withL.eu1426 or L.p1121 and binary co-culture with both L.eu1426 andL.p1121. Important differences in the acidification profiles wereobserved. The initial pH values in different brines were between 5.3and 5.5, which were lower than the initial pH values in sponta-neous fermentation in our previous study perhaps due to therelease of vegetable by heating (Xiong et al., 2012). The pH valuesdeclined notably before the 1.5th day in the three fermentations,and then reduced tardily until the end of the process. A rapiddecrease in pH value was reported to help reduce the risk for theproduction of other spoilage microorganisms during the first day offermentation (Pistarino et al., 2013). The pH value was found toreduce gradually until it reached to an appropriate level in pure LABcultures fermentation of sauerkraut (Tolonen et al., 2004). Thechange profiles of pH values in L.p1121 culture fermentation and inthe co-culture fermentation were almost overlapped in the latefermentation stage, but the pH values in both fermentations werelower than that in L.eu1426 fermentation. The main reason forthese observations may be that homofermentative L. plantarumdominated Chinese sauerkraut fermentation.

3.2. Growth of bacteria

As shown in Fig.2, the cell counts in pure culture fermentationincreased quickly at the first day of fermentation. The population in

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Fig. 2. The viability of cells in sauerkraut fermentations by starter cultures and binaryco-culture (n ¼ 4).

T. Xiong et al. / LWT - Food Science and Technology 59 (2014) 713e717 715

L.p1121 fermentation kept at approximately 8.5 Log CFU/mL duringthe later period of fermentation. The enumeration in L.eu1426fermentation reached to 9.3 Log CFU/mL firstly at a great speed,followed by a slow decline (6.2 Log CFU/mL), which was probablydue to its poor acid tolerance. Gardner et al. (2001) found that theenumeration of Leu. mesenteroides declined quickly after the secondday of culture, and then maintained at about 6.5 Log CFU/mL in thevegetable juice medium fermentation. Although the viable cells ofL.eu1426 multiplied sharply at the early stage of the co-culturefermentation, it was not significantly (p > 0.05) different fromthat in the L.eu1426 fermentation. The enumeration of L.eu1426 inthe co-culture fermentation declined significantly (p < 0.05) after1.5 days fermentation because of the low pH value. It was reportedthat the internal pH value in Leu. mesenteroides was higher thanthat in L. plantarum when they stopped growing (McDonald,Flening, & Hassan, 1990). The number of viable organisms ofL.p1121 in the co-culture fermentation was lower than that inL.p1121 fermentation after 18 h. The lower concentration of sucrosein the co-culture fermentation compared with that in L.p1121fermentation may influence the growth of L.p1121.

3.3. Substrates metabolism

Fig.3 showed the fermentative properties of L.eu1426, L.p1121,in pure cultures and binary co-culture fermentation. The initialconcentrations of sucrose, glucose and fructose, main sources ofenergy in Chinese sauerkraut fermentation, were about 27.0 g/L,3.4 g/L and 3.5 g/L, respectively. Different fermentations showedvarious metabolic features of substrates.

The final concentration of sucrose in the co-culture fermenta-tion was significantly (p < 0.05) lower than in pure culturefermentation with L.p1121. This result may be desirable. It was re-ported that the low concentration of sucrose in spontaneousfermentation of sauerkraut was in favor of the quality of product,because the secondary fermentation of yeast may be inhibited(Fleming et al., 1985). The utilization of sucrose in L.eu1426fermentation was better than that in the co-culture fermentation,likely due to the disappearance of L.eu1426 which utilized sucrosewell as it had high activities of permeases and/or hydrolyzing en-zymes (Gonzalez& Kunka,1986;Mital, Shallenberger,& Steinkraus,1973). Furthermore, the change of sucrose level in the co-culture

fermentation was similar to that in L.eu1426 fermentation before36 h. These results indicated that sucrose may be mainly used byL.eu1426 at the early stage of the co-culture fermentation.

As shown in Fig.3B, the concentration of glucose increased in thebeginning and then decreased in the three fermentations. The finalconcentration of glucose in the co-culture fermentation wassignificantly (p < 0.05) higher than that in L.p1121 fermentation.Therefore, taking into account that the number of viable cells inL.p1121 fermentation was higher (p < 0.05) than that in the co-culture fermentation while the L.p1121 dominated the fermenta-tion, these results suggested that the utilization of glucose byL.p1121 was not stimulated in the co-culture fermentation. How-ever, it was found computationally that the decrease of glucose byan L.p1121 cell was higher in the co-culture fermentation(1.91�10�6 g) than in the starter fermentation (1.67� 10�7 g) after60 h fermentation when the L.eu1426 can not be detected. Thebetter utilization of glucose by an L.p1121 cell in the co-culturefermentation may benefit from the low concentration of sucrose.

There was no decrease in the concentration of fructose inL.eu1426 and the co-culture fermentation. The final concentrationof fructose in the co-culture fermentation was significantly(p < 0.05) lower than in L.eu1426 fermentation. This differencemayresult from the existence of L.p1121 which can utilize the fructosedistinctly.

Some organic acids, for instance citric acid, malic acid and py-ruvic acid, were available in vegetables. As shown in Fig.3D, muchless citric acid was utilized in L.eu1426 fermentation. The decreaseof citric acid was higher in the co-culture fermentation than in pureculture fermentation with L.p1121. Schmitt, Divi�e, and Cardona(1992) reported that glucose and citrate were simultaneouslymetabolized in LAB culture by an enhancement of ATP productionvia the acetate kinase pathway. Certain amount of malic acid wasutilized in the three fermentations (Fig. 3E). The decrease in thelevel of malic acid by malolactic enzyme in the LAB was beneficialto the microbial stability of product (Malic acid þ NADþ / Pyruvicacid þ CO2 þ NADH) (Ansanay, Dequin, Blondin, & Barre, 1993;Fleming et al., 1985). Unexpectedly, the concentration of pyruvicacid did not decrease during fermentation (Data not shown).

3.4. Change of metabolic products

Lactic acid, acetic acid and ethanol as main fermentation prod-ucts were studied in this study. Moderate amount of acetic acid wasreported to improve the stability and organoleptic quality of food(Oliveira et al., 2012a, 2012b). A low amount of ethanol was foundin L.eu1426 fermentation and the co-culture fermentation. Ourprevious study found that the main flavor compounds in the brinewere from the spice added using high performance liquidchromatography-mass spectrometry (HPLC-MS) (Hao, 2013).

As shown in Fig.4A, the concentration of lactic acid increased upto the end in L.p1121 fermentation and the co-culture fermentation,whereas the increase of lactic acid concentration in L.eu1426fermentationwas not significant (p > 0.05) after 48 h. The change inlactic acid concentration in the co-culture fermentationwas similarto that in L.eu1426 fermentation at prophase. The final concentra-tion of lactic acid in L.p1121 fermentation was markedly (p < 0.05)higher than that in the co-culture fermentation. Nevertheless,supporting a metabolic behavior of L.eu1426 in the co-culturefermentation similar to that in its pure culture fermentation, theincrease of lactic acid level was higher in the co-culture fermen-tation (46.63 mM) than in L.p1121 fermentation (42.77 mM) from48 h to the end of fermentation.

It is known that the heterofermentative LAB can produce aceticacid and ethanol via 6p-gluconate pathway, and the homo-fermentative LAB use Embden-Meyerhof-Parnas pathway to

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Fig. 3. Changed levels of substrates in sauerkraut fermentations by starter cultures and binary co-culture (n ¼ 4).

T. Xiong et al. / LWT - Food Science and Technology 59 (2014) 713e717716

produce lactic acid. As shown in Fig.4B, although L.eu1426 did notdisappear in the co-culture fermentation from 24 h to 60 h, theconcentration of acetic acid was not notably (p > 0.05) increased.Differently, the concentration of acetic acid increased until 72 h inL.eu1426 fermentation. Although the increase in acetic acid levelwas more rapid in the co-culture than in L.eu1426 fermentation,the final concentration of acetic acid in L.eu1426 fermentation washigher (p < 0.05). Oliveira et al. (2012a, 2012b) reported that theincrease of acetic acid level had a slight inhibition in S. thermophilusand B. lactobacillus co-culture compared with in B. lactobacillusculture in fermented milk. The change profile of ethanol wassimilar to that of acetic acid (Data not shown). Furthermore, thefinal concentration of ethanol was higher in starter fermentation ofL.eu1426 (2.1 mM) than in the co-culture fermentation (1.6 mM).

4. Conclusion

Pure cultures and binary co-cultures with L.eu1426 and L.p1121were investigated for their effects on Chinese sauerkraut

fermentation. The change of pH value in the co-culture fermen-tation combined the characteristics of pH values in two pure cul-tures. Firstly, the pH value in the co-culture fermentationdecreased at a high speed like that in L.eu1426 fermentation, butthen decreased gradually to approximately 3.2. The change of cellcounts in the co-culture fermentation was different from that inpure cultures fermentation. L.eu1426 vanished after the 2.5th dayof the co-culture fermentation and the final enumerations ofL.p1121 were lower in the co-culture fermentation than that inL.p1121 fermentation. In three fermentations, the utilization ofsucrose, glucose and fucose was best in L.eu1426 fermentation, inL.p1121 fermentation and in L.p1121 fermentation, respectively.Obviously, the metabolism of critic acid was stimulated in the co-culture fermentation. Three fermentation showed malic acid canbe utilized and its utilization was best in L.p1121 fermentation.Although the final concentration of lactic acid was lower in the co-culture fermentation than in L.p1121 fermentation, L.p1121showed a strong ability of acid-producing in both fermentations.The lower concentration of acetic acid in the co-culture

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Fig. 4. Changed levels of products in sauerkraut fermentations by starter cultures andbinary co-culture (n ¼ 4).

T. Xiong et al. / LWT - Food Science and Technology 59 (2014) 713e717 717

fermentation than in L.eu1426 fermentation indicated that therecould be a slight inhibition of heterofermentative features ofL.eu1426 in the co-culture fermentation. Theoretically, ethanol is ametabolic product of Leu. mesenteroides via 6p-gluconate pathway.However, we found a little bit of ethanol in this study, potentiallydue to the generation of ethanol was dependent on the oxidation-reduction potential of the system (Johnson & Mccleskey, 1957;Kandler, 1983).

Acknowledgments

The financial supports from the National High TechnologyResearch Development Key Program of China (863 Key Program,2011AA100904), State Key Laboratory of Food Science and Tech-nology, Nanchang University (Project No. SKLF-ZZB-201309 and No.SKLF-ZZA-201303 and No. SKLF-KF-201210) and the National Nat-ural Science Foundation of China (NSFC, Project No. 31060224) aregratefully acknowledged.

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