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Received: 1 July 2016    Revised: 25 September 2016    Accepted: 2 October 2016

DOI: 10.1002/fsn3.441

ORIGINAL RESEARCH

Value-­added probiotic development by high-­solid fermentation
of sweet potato with Saccharomyces boulardii

Carmen Campbell | Ananda K. Nanjundaswamy | Victor Njiti | Qun Xia | 
Franklin Chukwuma

Department of Agriculture, School of
Agriculture, Research, Extension and Applied Abstract
Sciences, Alcorn State University, Lorman, Controlled fermentation of Sweet potato (Ipomoea batatas) var. Beauregard by yeast,
MS, USA
Saccharomyces boulardii (MAY 796) to enhance the nutritional value of sweet potato
Correspondence was investigated. An average 8.00 × 1010 Colony Forming Units (CFU)/g of viable cells
Ananda K. Nanjundaswamy, Department of
Agriculture, School of Agriculture, Research, were obtained over 5-­day high-­solid fermentation. Yeast cell viability did not change
Extension and Applied Sciences, Alcorn significantly over time at 4°C whereas the number of viable yeast cells reduced signifi-
State University, Lorman, MS, USA.
Email: ananda@alcorn.edu cantly at room temperature (25°C), which was approximately 40% in 12 months.
Overall, the controlled fermentation of sweet potato by MAY 796 enhanced protein,
Funding information
USDA (US Department of Agriculture) crude fiber, neutral detergent fiber, acid detergent fiber, amino acid, and fatty acid
levels. Development of value-­added sweet potato has a great potential in animal feed
and human nutrition. S. boulardii-­ fermented sweet potato has great potential as
probiotic-­enriched animal feed and/or functional food for human nutrition.

KEYWORDS
amino acid, CFU, fatty acid, fermented, Ipomoea batatas, neutral detergent fiber, viable cell

1 |  INTRODUCTION sweet potato is known to contain about 80% starch and a potential
feedstock for bioethanol production (Santa-­Maria, Yencho, Haigler, &
Sweet Potato (Ipomoea batatas (L.) Lam) is an important crop of south- Sosinski, 2011).
ern United States due to the ideal long frost-­free growing season. Fermentation of vegetable products with beneficial microbes
Globally, sweet potato is ranked at the seventh position next to rice, such as Lactobacillus (LA), Sacchromyces, Bacillus, etc. have been car-
wheat, corn, and cassava consumption. This is primarily due to the ried out for preservation and nutritional enhancement (Karovičova,
versatile adaptation of the crop to diverse environmental and climatic Grief, Kohajdova, & Hybenova, 2001). Salt-­incorporated fermenta-
conditions. Sweet potato is considered as a vegetable crop and has tion of cabbage, cucumber, and olives are commercially available
various food and feed applications. According to the USDA-­NASS which not only provide preservation but also enhance the nutritional
(2015), the U.S. production topped 29 million hundredweight (cwt). quality (Maifreni, Marino, & Conte, 2004). Some of the Asian LA-­
Southern states dominated in production with North Carolina and fermented vegetables such as radish, mustard, and cauliflowers are
California ranking top states followed by Texas and Mississippi. Sweet known to enhance flavor and preserve some biochemicals such as
potatoes are rich in wide range of nutrients which include dietary fiber, carotenes and phenolics (Shivashankara, Isobe, Al-­Haq, Takenaka,
vitamins, phenolic compounds, and carotenes (Ray & Tomlins, 2010). & Shiina, 2004). Because of the starch-­rich nature of sweet potato
Sweet potato has been used as animal feed in poultry, pigs, and in live- and its co-­products from processing industry, various fermenta-
stock (Chittaranjan, 2007; Lebot, 2009; Woolfe, 1992). On dry basis, tion routes have been used to develop value-­added products (Ray

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provided the original work is properly cited.

Food Sci Nutr. 2017;5:633–638. www.foodscience-nutrition.com © 2016 The Authors. Food Science & Nutrition  |  633
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potato dextrose agar (PDA) and stored at 4°C for 10 days. Lorman. vival. & Ward. After re- ing gastrointestinal inflammation and other disorders (Hamedi et al. prepared for statistical analysis. 2. & Chatzopoulou. at. 2006. Enterococcus. 1990).9 × 10 6.5 g cell viability. & was stored at room temperature at Alcorn State University Experiment Pothoulakis.5 × 1010 a anti-­oxidant activity with a similar pH. Pagana et al. tannin. ing of the end product (Table 1). using Lactobacillus rhamnosus with yield of 10 g/l of lactic acid 12 7. and 0. was chopped ricultural produce to provide supplemental probiotic for humans as and placed in a drying chamber for 3 days at 28°C. 2015. Propionibacterium. Some of the well-­known 2 | MATERIALS AND METHODS prokaryotic probiotic genera of microorganism are Lactobacillus. and osmotic shocks (Klis. Flasks were inoculated and incubated at 30°C. lardii can induce immune response by increasing the IgA and IgG Inoculum was grown at 30°C on an orbital shaker at 200 rpm for 48 hr. 2010). T A B L E   1   Viable cell counts at different time points oped wine from anthocyanin-­rich sweet potato by fermentation Months 4°C 25°C of Saccharomyces cerevisiae. feed supplement to control gastrointestinal disorders and also have Food-­ and feed-­borne gastroenteritis are common among hu. Orlean. 2014. Vaerman. Duplicate samples were 2013) have been used for fermenting S. They have been extensively studied for their ability in reduc.. Matar et al. Additionally. 0. this study was to develop S. American Type Culture Collection (ATCC. Samples were auto- ml viable cells when stored for a month at 4°C. which are mainly responsible “Beauregard” sweet potato was collected from Mound Bayou. They reported a healthy growth of 7. 2013. Pothoulakis. been used to produce antibiotic such as tetracycline (Yang and Yuan. and S.. Buts.9 × 1010 b production in 72 hr. coli. | 634       CAMPBELL et al. E. (2014) used organic waste from sweet po. raw 10 ml of MAY 796. Rodrigues 2. and incubated at 30°C on an orbital shaker at 300 rpm for 5 days and lardii is known to act by providing receptor sites for binding some stored in a deep freezer at −80°C. bator shaker at 300 rpm for 5 days at 30°C. lated into potato dextrose broth which was sterilized at 121°C for 30 min. With the abun. cultures were inoculated into yeast extract malt extract broth 2013. Manassas. boulardii (MAY 796) were obtained from boulardii are known to exhibit probiotic effect in humans and ani.. Some of the pathogens to blame for these out. boulardii-­fermented sweet potato and breaks are Salmonella. Sweet potato flour well as for animals. Swain. Lesage & Bussey. About one vial (1 ml) from – 80°C storage was thawed and was inocu- & DeGroot.59 × 1010 CFU/ MgSO4. 2011). production of value-­added products provides an opportunity to diversify sweet 2. Wongkhalaung.3 | Media preparation for high solid fermentation et al. VA). 2000). flasks were inoculated with products of food industry such as rice bran (Ryan et al. boulardii proteases are known to inhibit Toxin A and Toxin B of Clostridium difficile. 1998). Bifidobacterium. Bernasconi. Only a few eukary- otic microbes such as Saccharomyces cerevisiae and Saccharomyces Lyophilized cultures of S. Keeping this in mind. These ac- 2. and Sivakumar (2012) devel. Saccharomyces bou. These gastrointestinal disorders can be cured by use of vi- able microorganisms called “probiotics”. boulardii-­enriched fermented product. boulardii. 2016.9 × 10 8. lactic acid and ethanol (Ray & Palaniswami. Riegler.3 × 1010 a 10 a tato processing for canning as raw material for production of lactic 8 7. Hudson et al. 1999). 1990. 2008. Kim et al. MS. The overall objective of mans and animals. For example Fratianni et al. revived on mals. tomato juice (Fratianni et al. Panda. toxins produced by pathogens. low pH.0 × 1010 a 7.2 | Inoculum generation tions are well mediated at different physiological conditions includ- ing anaerobic stress. boulardii. and for diarrhea and colitis (Castagliuolo. Solomakos. (2013) used berry was prepared by milling in an Udy bench top grinder. 4 8. 2001. 2006. sweet potato and its waste has Counts are average of two replicates. About 60 g of juice as a medium to grow yeast and used alginate-­inulin-­xanthan the finely ground sweet potato flour was added to 1000 ml flask with gum microencapsulation for better delivery and enhancement of 300 ml of H2O.5 g MnSO4 and ZnSO4 per liter. Other inorganic salts included were 1 g KH2PO4. 2006). citric acid. Yeast glucans and mannans are also known to play a critical role in the toxin-­binding process.. Many other co-­ claved at 121°C for 30 min. Qamar et al. sweet potato was used a feed- stock for production of S.. 1997) and .. Valenick. bou. Due to the probiotic nature of S. Ray.4 | Fermentation conditions potato uses. and Clostridium butyricum (Gibson. The enriched product can serve as potential probiotic in animal Control flasks without inoculum were also maintained.9 × 1010 b acid.1 | Microbial culture Bacillus. Pexara. oughly with running water to remove any surface debris. application in human health and nutrition. Oenoccoccus..95% 10 a 0 7. 1995). levels (Lauren et al. and phenol profile of grape wine. LaMont. Selected sweet potatoes were washed thor- tempts have been made to ferment various food products and ag.7 × 1010 a 5. and Clostridium difficile to name a few characterize the viable cell counts over time and nutritional profil- major pathogens (Govaris. Boorsma.. This production media was then placed in an incu- wheat (Nguyen & Herve. S. 2012). 2009). Station. 300 rpm for 5 days. & Dive. dant supply of sweet potato in southern United States. The resultant wine showed a 58. Two replicates . MS. Upon cooling.

& Ingledew. 2011).6 | Stability of the viable yeast cells ent metabolic stress. since cell viability is critical for probiotic efficiency of the fermented-­ product. which was about 44%. Magnus. using PROC ANOVA and (Nanjundaswamy & Vadlani. acids. After incubation of plates at 30°C for 4 days.1 | Viable cell count in fermented product 2. 2014. Temperature) and periodically (every 4 months) subjected for deter. Significance was set actively growing yeast can break down proteins into numerous amino at p < . crude fiber. using the ASOS methods as described in Nanjundaswamy and dardii is shown in Figure 1. a serial other studies (Fratianni et al. 2013). total fatty acid profile. dilution method was used and spread plate method of culturing yeast & Mas. Ough.2.. resulting in enhanced total amino acids (Sturley & Young. Analysis of Variance was measured.0 × 1010 CFU/g (Table 1). Torija. 1974. It is plausible that the mination of viability. and decrease in membrane Samples were stored in Zip-­lock bags at 4° and 25°C (Room functionality (Casey. total amino acid content. and ash content compared to the con- % neutral detergent fiber (NDF). next 12 months. 2002).05. A 2. whereas the CFU decrease at room temperature was signif- varied between 50 and 100) were counted and CFU/g of fermented icant (p = . Also storage of the prod- uct at 4°C prevents any loss of viability of the probiotic. ↓%decrease compared to control . Endo-­ and exo-­proteases in the Tukey test was used for pair-­wise comparisons. ethanol production. 1966). Rozès. In brief.CAMPBELL et al. colo. This cell viability count was similar to viable cells per gram of the final fermented samples.8362). This information is very vital. 2.05) in the control than in the fermented sample. % crude fiber. Poblet. Guillamèn. Castellano. & Steinkraus. a co-­product of corn ethanol production 9. *significantly different (p < . Nutrition composition analyses included total amino hanced the % crude protein. When the fermented product was stored at room tem- cells on PDA medium was carried out. Actively growing yeast produced significant protein which contributed to the enhanced levels of total protein. trol. there was a decrease in the CFU over the were carried out.05) treatment from control. using serial dilution technique. Moisture was significantly greater (p ≤ .8 | Statistical analyses similar trend was observed in red yeast fermentation of dry distillers Data were analyzed by Statistical Analysis Software (SAS) version grain with solubles (DDGS). 1984. % crude fat.5 | Determination of viable cells of S. 3. acid profile. % NDF. F I G U R E   1   Nutrition composition. Means and standard errors are provided. boulardii was about Serial dilution technique was used to determine CFU which represents 8. Sample dilutions up to 10−12 perature (25°C) and at 4°C. Samples were freeze dried for 48 h and 3 | RESULTS AND DISCUSSION stored at −80°C until further analyses. Fermentation significantly (p ≤ . The overall nutritional profile of fermented sweet potato by S.0032).05) en- Vadlani (2011). samples was expressed.2 | Overall nutritional profile Agricultural Experiment Station Chemical Laboratories (AESCL) at the University of Missouri-­Columbia for biochemical compositional analy.7 | Nutritional profiling Known quantity of freeze-­dried samples were weighed and sent to the 3. ↑% increase. Nagodawithana. boulardii The end of fermentation viable cell count for S. |       635 per treatment were employed. and % acid detergent fiber (ADF). crude fat and protein. The decrease in the CFU was not significant at 4°C nies from plates with the highest dilutions (where the colony numbers (p = . Some of the earlier yeast cell stability studies conducted in liquid medium showed clear drop in the CFU over time due to the inher- 2. % ADF. boul- ses. removal of water and reducing the water activity has a great impact on long-­term stability of the probiotic product.

linolenic acid. Simon. boulardii. ↑% increase. GC-­MS profiling to DDGS (Stein et al. Means and standard errors are provided. | 636       CAMPBELL et al. hydroxylysine. fermented samples had significantly higher (p ≤ . peratures (Torija et al.4 | Fatty acid profile of control and fermented including hemicellulose. stearidonic acid. stearic acid. been reported with respect to fatty acid profile of S. The lysine levels of the fermented sweet potato is comparable edly changed the metabolomic profile for rice bran. treatments were significantly different only for myristci acid. At least 12 fatty acids were detected. of the volatile fatty acid was positively influenced by fermentation. and tryptophan (Figure 2). & Stein.05) levels of myristic acid. F I G U R E   2   Amino acid Content. but not statistically control but not statistically significant. & Fermented rice bran showed elevated levels of secondary metabolites Boersma. Pedersen. Urriola et al. & Stein. Pedersen. Pedersen. significant. and DHA compared to the control. 2009). Fermented samples had 3. (2011) provided insights into the metabolomics of rice bran-­ compared to control. only six fatty acids were higher in content in fermented (p ≤ . Figure 3 represents fatty acid profile of fermented and control sam- ples.3 | Amino acid profile of control and fermented significantly higher (p ≤ . Pahm. A similar fatty acid profile was reported in wine from fer- tent was significantly greater (p ≤ . . 2005.05) Taurine. Hoehler.05. These amino acids are of importance in animal fermented with S. and lignin. 3. 2002). The S. Increased NDF results in sweet potato higher digestible energy. except for glutamic acid which was greater than were greater in control than fermented samples. cellulose. ↓%decrease compared to control F I G U R E   3   Fatty acid profile. For all samples than control. boulardii fermentation undoubt- feed. Means and standard errors are provided. three fatty other amino acids. Ryan tamic acid. leucine. boulardii. but were not statistically significant.05). lino- sweet potato lenic acid.05) in fermented samples than mentation of different species of Saccharomyces under different tem- control. Stein. total amino acid con. Overall. fermented samples had significantly lower fatty acids. and aspartic acid levels were higher in fermented samples et al. *significantly different treatment from control (p < . 2006. ↑% increase. such as ferulic acid. and DHA. At p < . ↓%decrease compared to control Neutral detergent fiber represents the total plant fiber or cell wall. 2006. A very limited metabolic profiling has Some of the important amino acids such as lysine. 2006. and behnoic acid content content than control. glu. Of the remaining nine Compared to the control.05) acids namely palmitic (16:0). stearic acid. Gibson. Pahm...

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