Scientia Agricultura Sinica ›› 2018, Vol. 51 ›› Issue (10): 1982-1994.doi: 10.3864/j.issn.0578-1752.2018.10.017

• FOOD SCIENCE AND ENGINEERING • Previous Articles     Next Articles

The Solid-State Fermentation Process of Rhodotorula Mucilaginosa for Producing Carotenoids

JiaJing SUN(), Mao LI, ZhiHong SUN(), ZhiRu TANG, XiangXin ZHANG, JinChao CHEN   

  1. College of Animal Science and Technology/Laboratory for Bio-Feed and Animal Nutrition, Southwest University, Chongqing 400715
  • Received:2017-10-09 Accepted:2018-03-05 Online:2018-05-16 Published:2018-05-16

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Abstract:

【Objective】 This study was performed to enhance carotenoid yield, to improve nutritional value of fermentation product, and to reduce the production cost of carotenoids through optimizing solid-state fermentation substrate and fermentation conditions of Rhodotorula mucilaginosa.【Method】 In this study, Rhodotorula mucilaginosa TZR2014 was used as a inoculant. First, the Mixture-Design of Design-Expert software was used to design the fermentation substrate, and the contents of ingredients as followed: 50%-80% wheat bran, 6%-20% soybean meal, 3%-15% maize flour, 2%-14% rice bran, 2%-10% maize syrup, 0.4%-2.5% ammonium sulfate, 0.05%-0.5% monopotassium phosphate, and 0.03%-0.3% magnesium sulfate. Then the optimal ratio of ingredients in substrate was determined according to the carotenoid yield. Based on this result, an L16(45) orthogonal design was used to optimize the fermentation conditions, including inoculum (5.0%-12.5%), fermentation time (60.0-96.0 h), fermentation temperature (26-32℃), and fermentation pH (60.0%-75.0%). Finally, the number of Rhodotorula mucilaginosa and contents of carotenoids, crude fiber, crude protein, water, crude fat, ash, calcium, phosphorus, and amino acids in fermentation product were determined to evaluate the effects of the optimized fermentation process on the nutritional values of fermentation product. 【Result】 The results showed that there was a positive correlation between maize starch content in substrate and carotenoid content in fermentation product (r=0.344, P=0.040) or between rice bran content in fermentation substrate and carotenoid content in fermentation product (r=0.329, P=0.050). There was a significantly negative correlation between carotenoid yield and the content of wheat bran in solid-state fermentation substrate (r=-0.336, P=0.045). There was a positive correlation between the number of live bacteria of Rhodotorula mucilaginosa in fermentation product and the content of soybean meal in fermentation substrate (r=0.510, P=0.001). Inoculum, fermentation temperature, pH, and moisture had extremely significant impacts on the number of Rhodotorula mucilaginosa (P<0.01), thereinto, fermentation temperature had the greatest effect on the number of Rhodotorula mucilaginosa, followed by moisture, inoculum, and pH. Fermentation time, fermentation temperature, and pH had extremely significant influences on the carotenoid content in the fermentention product (P<0.01), and fermentation temperature had the greatest influence on the carotenoid content in the fermented product, followed by pH and fermentation time. After the optimization of the fermentation process, the carotenoid yield by Rhodotorula mucilaginosa TZR2014 was increased to 4 535 μg·kg-1; the bacteria number was increased to 3.79×109 CFU/kg; the contents of crude fiber, crude protein, ash, threonine, glutamate, and proline in fermentation product were significantly increased (P<0.05), meanwhile, the contents of histidine, water, and crude fat was significantly decreased (P<0.05). 【Conclusion】 The optimal ratio of solid-state fermentation substrate for Rhodotorula mucilaginosa was as followed: 52.5% wheat bran, 20.0% soybean meal, 3.0% maize flour, 14.0% rice bran, 10.0% maize syrup, 0.4% ammonium sulfate, 0.05% monopotassium phosphate, and 0.04% magnesium sulfate. The optimal fermentation conditions were as followed: inoculum 5.0%, fermentation time 72 h, fermentation temperature 28.0℃, pH 6.0, and moisture 60.0%. The results suggested that the optimized fermentation process of Rhodotorula mucilaginosa enhanced the yield of carotenoids and improved the nutritional value of fermentation product.

Key words: Rhodotorula mucilaginosa, solid-state fermentation, carotenoids, fermentation substrates, fermentation conditions

Table 1

The optimized design of the substrates for the solid-state fermentation of Rhodotorula mucilaginosa (%)"

序号
Order
number		 麸皮
Wheat
bran		 豆粕
Soybean meal		 玉米
Maize		 米糠
Rice bran		 玉米浆
Maize syrup		 硫酸铵
Ammonium sulphate		 磷酸二氢钾
Monopotassium phosphate		 硫酸镁
Magnesium sulphate
1 73.4 9.51 5.00 6.64 2.43 2.50 0.33 0.17
2 77.7 6.00 3.00 8.10 4.16 0.74 0.08 0.19
3 79.8 7.93 3.00 2.00 6.59 0.46 0.05 0.18
4 59.5 19.3 4.44 10.2 4.45 1.89 0.05 0.08
5 71.4 7.89 15.0 2.00 2.04 1.30 0.18 0.22
6 67.7 10.0 4.60 14.0 2.00 1.27 0.23 0.24
7 63.4 14.4 13.6 3.70 2.44 1.57 0.50 0.28
8 52.3 19.8 13.6 10.6 2.00 1.57 0.15 0.03
9 77.0 7.53 9.97 2.98 2.05 0.40 0.05 0.03
10 58.1 15.5 9.15 12.2 4.03 0.40 0.50 0.06
11 58.1 18.2 12.9 5.01 3.10 2.50 0.11 0.15
12 53.8 16.6 7.79 11.3 8.59 1.16 0.50 0.28
13 62.1 13.3 8.73 8.05 6.00 1.53 0.28 0.09
14 69.4 6.37 3.00 11.9 6.39 2.44 0.25 0.30
15 56.0 18.3 5.81 7.81 10.0 1.74 0.13 0.26
16 76.1 8.99 3.00 4.93 4.38 2.48 0.06 0.03
17 59.5 19.3 4.44 10.2 4.45 1.89 0.05 0.08
18 62.3 16.4 10.1 7.38 2.94 0.61 0.05 0.22
19 57.7 15.6 6.41 10.9 8.82 0.40 0.19 0.03
20 56.4 17.7 14.0 3.66 7.32 0.85 0.10 0.04
21 70.2 20.0 3.06 3.21 2.63 0.68 0.21 0.05
22 62.1 13.3 8.73 8.05 6.00 1.53 0.28 0.09
23 77.7 6.00 3.00 8.10 4.16 0.74 0.08 0.19
24 65.9 7.38 13.8 7.01 4.86 0.40 0.42 0.27
25 57.6 12.2 13.8 4.76 8.84 2.35 0.20 0.30
26 63.6 6.00 14.0 4.73 9.90 1.54 0.12 0.10
27 73.4 9.51 5.00 6.64 2.43 2.50 0.33 0.17
28 77.7 6.00 3.00 8.10 4.16 0.74 0.08 0.19
29 79.8 7.93 3.00 2.00 6.59 0.46 0.05 0.18
30 79.8 7.93 3.00 2.00 6.59 0.46 0.05 0.18
31 59.5 19.3 4.44 10.2 4.45 1.89 0.05 0.08
32 67.7 10.0 4.60 14.0 2.00 1.27 0.23 0.24
33 62.1 13.3 8.73 8.05 6.00 1.53 0.28 0.09
34 69.4 6.37 3.00 11.9 6.39 2.44 0.25 0.30
35 76.1 8.99 3.00 4.93 4.38 2.48 0.06 0.03
36 62.3 16.4 10.1 7.38 2.94 0.61 0.05 0.22

Table 2

The optimized gradients of the conditions for the solid-state fermentation of Rhodotorula mucilaginosa"

梯度
Gradients		 接种量
Inoculum (%)		 发酵时间
Fermentation time (h)		 发酵温度
Fermentation temperature (℃)		 pH 含水量
Moisture content (%)
A 5.0 60.0 26.0 4.0 60.0
B 7.5 72.0 28.0 5.0 65.0
C 10.0 84.0 30.0 6.0 70.0
D 12.5 96.0 32.0 7.0 75.0

Table 3

The optimized design of the conditions for the solid-state fermentation of Rhodotorula mucilaginosa"

序号
Order number		 接种量
Inoculum amount (%)		 发酵时间
Fermentation time (h)		 发酵温度
Fermentation temperature (℃)		 pH 含水量
Moisture content (%)
1 A A A A A
2 A B B B B
3 A C C C C
4 A D D D D
5 B A B C D
6 B B A D C
7 B C D A B
8 B D C B A
9 C A C D B
10 C B D C A
11 C C A B D
12 C D B A C
13 D A D B C
14 D B C A D
15 D C B D A
16 D D A C B

Table 4

Effects of the optimization of the subtrates for the solid-state fermentation of Rhodotorula mucilaginosa on the carotenoid production and the number of bacteria"

序号
Order number		 类胡萝卜素
Carotenoid (μg·kg-1)		 发酵料含菌数
Number of bacteria (109 CFU/g)
1 1 673±28.8 2.22±0.40
2 1 329±81.6 2.42±0.38
3 1 715±125 3.08±0.41
4 1 767±47.2 3.28±0.41
5 1 293±76.6 2.85±0.30
6 1 503±94.2 2.82±0.35
7 1 332±24.2 2.85±0.33
8 1 699±70.4 2.94±0.50
9 1 404±73.9 2.70±0.23
10 1 751±159 2.59±0.29
11 1 673±77.7 2.42±0.23
12 1 767±56.8 2.82±0.27
13 1 757±135 2.61±0.39
14 1 785±64.1 2.42±0.22
15 1 902±22.1 3.43±0.45
16 1 470±38.7 2.45±0.33
17 1 831±79.4 3.52±0.23
18 1 923±109 3.13±0.39
19 1 695±100 2.87±0.26
20 1 383±69.6 2.61±0.33
21 1 296±133 3.27±0.36
22 1 329±78.8 2.80±0.28
23 1 758±49.3 2.77±0.43
24 1 776±182 2.85±0.19
25 1 630±51.9 2.67±0.31
26 1 744±79.3 2.91±0.35
27 1 695±32.3 2.14±0.26
28 1 372±53.0 2.32±0.26
29 1 656±63.1 3.01±0.27
30 1 685±73.9 3.07±0.41
31 1 785±88.5 3.22±0.30
32 1 479±72.4 2.79±0.23
33 1 732±103 2.59±0.23
34 1 787±61.3 2.56±0.27
35 1 502±30.9 2.51±0.23
36 1 848±98.7 2.87±0.25

Table 5

The Adeq Precision and Pred R-Squared of the model"

项目
Items		 类胡萝卜素
Carotenoids		 胶红酵母菌数
Number of Rhodototula mucilaginosa
模型的信噪比
Adeq Precision		 6.23 5.32
R2 预测值
Pred R-Squared		 -0.095 -0.031

Table 6

The correlation between the fermentation substrates of Rhodototula mucilaginosa and the carotenoid yield or number of bacteria"

因素
Factor		 类胡萝卜素
Carotenoids		 P值
P-value		 胶红酵母数
Number of Rhodototula mucilaginosa		 P值
P-value
麦麸 Wheat bran -0.336 0.045 -0.370 0.067
豆粕 Soybean meal 0.200 0.242 0.510 0.001
玉米粉 Maize -0.049 0.777 0.005 0.978
米糠 Rice bran 0.329 0.050 -0.027 0.874
玉米浆 Maize syrup 0.344 0.040 0.183 0.284
硫酸铵 Ammonium sulphate 0.094 0.586 -0.296 0.080
磷酸二氢钾 Monopotassium phosphate -0.009 0.960 -0.276 0.104
硫酸镁 Magnesium sulphate 0.196 0.253 -0.069 0.687

Table 7

The optimized formulation of the substrates for the solid-state fermentation of Rhodotorula mucilaginosa (%)"

麦麸
Wheat bran		 豆粕
Soybean meal		 玉米粉
Maize		 米糠
Rice bran		 玉米浆
Maize syrup		 硫酸铵
Ammonium sulphate		 磷酸二氢钾
Monopotassium phosphate		 硫酸镁
Magnesium sulphate
52.5 20.0 3.00 14.0 10.0 0.40 0.05 0.04

Table 8

The model predictive values and measured data of the carotenoid production of Rhodotorula mucilaginosa"

指标
Index		 模型预测值
Model predictive value		 实测值
Measured data		 SEM P值
P-value
类胡萝卜素 Carotenoids (μg·kg-1) 1 923 1 937 22.6 0.65
活菌数 Number of bacteria (109 CFU/g) 3.2 3.18 0.38 0.31

Table 9

The orthogonal test results of the optimized conditions for the solid-state fermentation of Rhodotorula mucilaginosa"

序号
Order number		 A B C D E 发酵料含菌数
Number of bacteria in fermented materials (109 CFU/g)		 类胡萝卜素含量
Carotenoid content
(μg·kg-1)
1 1 1 1 1 1 4.03±0.29 1 377±30.5
2 1 2 2 2 2 3.60±0.31 3 149±50.8
3 1 3 3 3 3 2.78±0.40 2 150±93.5
4 1 4 4 4 4 3.53±0.41 2 126±75.6
5 2 1 2 3 4 2.57±0.25 3 150±77.8
6 2 2 1 4 3 3.29±0.23 1 914±65.5
7 2 3 4 1 2 3.64±0.43 1 902±46.2
8 2 4 3 2 1 2.82±0.35 2 378±87.9
9 3 1 3 4 2 2.96±0.26 1 651±55.4
10 3 2 4 3 1 3.49±0.28 3 068±32.5
11 3 3 1 2 4 3.02±0.34 2 012±69.8
12 3 4 2 1 3 3.41±0.39 2 447±103.5
13 4 1 4 2 3 3.27±0.38 2 350±45.6
14 4 2 3 1 4 2.73±0.37 1 752±29.6
15 4 3 2 4 1 3.31±0.26 2 686±56.4
16 4 4 1 3 2 3.29±0.21 2 192±33.8
k1 3.49 3.21 3.41 3.45 3.41 C4E1D1A1B2
RC>RE>RD>RA>RB
k2 3.08 3.28 3.22 3.18 3.37
k3 3.22 3.19 2.82 3.03 3.19
k4 3.15 3.26 3.48 3.27 2.96
R 0.41 0.09 0.66 0.42 0.45
k1 2201 2132 1874 1870 2377
k2 2336 2471 2858 2472 2224 C2D3B2E1A2
RC>RD>RB>RE>RA
k3 2294 2187 1983 2640 2215
k4 2245 2286 2362 2094 2260
R 135 338 984 770 161

Table 10

e optimized scheme of the conditions for the solid-state fermentation of Rhodotorula mucilaginosa"

项目Items 因素水平（由主到次）Factors level (from the main to the second)
细胞数 Cell number C4（32℃） E1（60%） D1（4.0） A1（5.0%） B2（60 h）
类胡萝卜素Carotenoids C2（28℃） D3（6.0） B2（72 h） E1（60%） A2（7.5%）

Table 11

The variance analysis of the effects of fermentation conditions on the number of Rhodototula mucilaginosa"

变异来源
Sources of variation		 偏差平方和
Sum of squares of deviations		 自由度
Freedom		 方差
Variance		 F值
F value		 Fa
Fa		 显著水平
Significant level
接种量Inoculum amount 0.38 3 0.13 16.9 F0.01（3,6）=9.78 ***
发酵时间Fermentation time 0.02 3 0.01 F0.05（3,6）=4.76
发酵温度Fermentation temperature 1.05 3 0.35 47.0 F0.1（3,6）=3.29 ***
pH 0.37 3 0.12 16.7 F0.25（3,6）=1.78 ***
含水量Moisture content 0.51 3 0.17 22.8 ***
误差Error 0.02 3 0.01
修正误差Corrected error 0.05 6 0.01
总和Sum 2.35

Table 12

The variance analysis of the effects of fermentation conditions on the carotenoid content"

变异来源
Sources of variation		 偏差平方
Sum of squares of deviations		 自由度
Freedom		 方差
Variance		 F值
F value		 Fa
Fa		 显著水平Significant level
接种量 Inoculum amount 41472 3 13 824 F0.01（3,9）=6.99
发酵时间 Fermentation time 265432 3 88 477 5.32 F0.05（3,9）=3.86 **
发酵温度 Fermentation temperature 2374448 3 791 483 47.5 F0.1（3,9）=2.81 ***
pH 1476072 3 492 024 29.6 F0.25（3,9）=1.63 ***
含水量Moisture content 66880 3 22 293
误差Error 41472 3 13 824
修正误差Corrected error 149824 9 16 647
总和Sum 4265776

Table 13

The carotenoid production and Rhodotorula mucilaginosa number under the optimal fermentation process"

指标 Index 试验值 Test values
类胡萝卜素 Carotenoids (μg·kg-1) 4 535±32.5
发酵料含菌数 Number of bacteria of fermentation (109 CFU/g) 3.79±0.29

Table 14

The changes of conventional nutrient composition in substrate for Rhodotorula mucilaginosa after fermentation (%)"

项目 Items 发酵底物Fermentation substrate 发酵产物Fermentation product SEM P 值 P-value
粗纤维 Crude fiber 10.4b 11.6a 0.10 <0.05
粗蛋白质 Crude protein 25.9 b 28.4a 0.13 <0.05
水分 Moisture 12.6a 11.0b 0.24 <0.05
粗脂肪 Crude fat 3.25a 2.73b 0.13 <0.05
粗灰分 Ash 6.87 b 7.83a 0.04 <0.05
磷 Phosphorus 0.51 0.51 0.01 0.116
钙 Calcium 0.55 0.56 0.03 0.712

Table 15

The changes of amino acid content in substrate in substrate for Rhodotorula mucilaginosa after fermentation (g /100 g)"

项目 Items 发酵前 Before fermentation 发酵后 After fermentation SEM P 值 P-value
天门冬氨酸 Aspartic acid 1.65 1.70 0.03 0.29
苏氨酸 Threonine 0.72b 0.86a 0.02 <0.05
丝氨酸 Serine 0.90 0.92 0.01 0.40
谷氨酸Glutamate 3.47b 3.80a 0.04 <0.05
甘氨酸 Glycine 0.99 0.99 0.01 0.99
丙氨酸 Alanine 1.16 1.20 0.01 0.65
半胱氨酸 Cysteine 0.24 0.20 0.09 0.23
缬氨酸 Valine 0.94 0.98 0.04 0.56
蛋氨酸 Methionine 0.19 0.20 0.01 0.10
异亮氨酸 Isoleucine 0.76 0.82 0.05 0.12
亮氨酸 Leucine 1.52 1.60 0.06 0.38
酪氨酸 Tyrosine 0.43 0.50 0.04 0.21
苯丙氨酸 Phenylalanine 0.94 1.08 0.04 0.07
赖氨酸 Lysine 1.03 1.11 0.05 0.29
组氨酸 Histidine 0.60a 0.24b 0.06 <0.05
精氨酸 Arginine 1.30 1.21 0.06 0.33
脯氨酸 Proline 2.22b 2.98a 0.04 <0.05
总量 Total 19.5 20.9 0.51 0.16
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