龙葵提取物对大肠杆菌、粪肠球菌及其生物膜形成的抑制作用

doi:10.13304/j.nykjdb.2022.0121

摘要/Abstract

摘要：

为探究龙葵提取物对大肠杆菌、粪肠球菌的抑菌作用及其对生物膜形成的影响，比较了黑果龙葵、黄果龙葵、红果龙葵果及其茎叶提取物的抑菌能力，并对黑果龙葵果提取工艺进行响应面优化；通过结晶紫染色法测定黑果龙葵果提取物抑制细菌生物膜形成能力，以疏水性、泳动性、自聚集性为指标，评价提取物对生物膜形成的抑制作用。结果表明，3种龙葵中黑果龙葵果提取物抑菌效果最好，抑制大肠杆菌生长最佳提取条件为提取温度28 ℃、乙醇含量44.5%、液料比5.1∶1（mL·g^-1），抑制粪肠球菌生长最佳提取条件为提取温度29.5 ℃，乙醇含量44.7%，液料比5.1∶1（mL·g^-1），此时黑果龙葵果提取物对大肠杆菌、粪肠球菌的抑菌率分别为81.44%±1.78%、90.63%±2.33%，最小抑菌质量浓度均为50 mg·mL^-1。30 mg·mL^-1黑果龙葵果提取物对大肠杆菌、粪肠球菌生物膜形成的抑制率分别为83.52%、85.13%，提取物抑制大肠杆菌生物膜形成与降低疏水性显著相关（P<0.05），抑制粪肠球菌生物膜形成与降低泳动性、自聚集性显著相关（P<0.05）。上述结果可为龙葵抑菌和生物膜抑制提供理论依据，为开发天然植物抗生素替代品提供参考。

关键词: 龙葵提取物, 抑菌, 理化性质, 生物膜

Abstract:

To investigate the antibacterial effect of Solanum nigrum L. on Escherichia coli and Enterococcus faecalis and its effect on biofilm formation， the antibacterial activities of extracts from Solanum nigrum L.， Solanum villosum Miller.， Solanum diphyllum L. fruit and their stems or leaves were compared，and the extracting conditions of Solanum nigrum L. fruit was optimized by response surface methodology. The effect of extracts from Solanum nigrum L. fruit on the formation of bacterial biofilm was determined by crystal violet staining， and the factors affecting the formation of antibiofilm were evaluated by swimming， auto-aggregation， and hydrophobicity. The results showed that the extracts from Solanum nigrum L. fruit had the best inhibition rate. The optimum extraction conditions for inhibiting the Escherichia coli were extraction temperature 28 ℃， ethanol content 44.5%， liquid-solid ratio 5.1∶1 （mL·g^-1）； the optimum extraction conditions for inhibiting the Enterococcus faecalis were extraction temperature 29.5 ℃， ethanol content 44.7%， liquid-solid ratio 5.1∶1 （mL·g^-1）. Under these conditions， the extracts showed the best antibacterial effect on Escherichia coli and Enterococcus faecalis， the inhibition rate were 81.44%±1.78% and 90.63%±2.33%. The minimum inhibitory concentration of Escherichia coli and Enterococcus faecalis was 50 mg·mL^-1. The inhibitory rates of 30 mg·mL^-1Solanum nigrum L. fruit extract on biofilm formation of Escherichia coli and Enterococcus faecalis were 83.52% and 85.13% ， respectively. And the inhibition of Escherichia coli biofilm formation was related to the decrease of hydrophobicity （P<0.05）， and the inhibition of Enterococcus faecalis biofilm formation was related to the decrease of swimming and auto-aggregation （P<0.05）. These results provided a theoretical basis for the bacteria inhibition and biofilm inhibition of Solanum nigrum L.， and a reference for the development of natural plant antibiotic substitutes.

Key words: Solanum nigrum L. extract, antibacterial, physicochemical properties, biofilm

中图分类号:

R285

郭航帆, 王萍, 王颖. 龙葵提取物对大肠杆菌、粪肠球菌及其生物膜形成的抑制作用[J]. 中国农业科技导报, 2023, 25(10): 152-164.

Hangfan GUO, Ping WANG, Ying WANG. Inhibitory Effect of Solanum nigrum L. Extracts on Escherichia coli and Enterococcus faecalis and Biofilm Formation[J]. Journal of Agricultural Science and Technology, 2023, 25(10): 152-164.

图/表 15

表1 因素水平编码

Table 1 Factors and levels in the experimental design

因素Factor	水平 Level
因素Factor	-1	0	1
A：提取温度Temperature/℃	20	30	40
B：乙醇含量Ethanol content/%	40	45	50
C：液料比Liquid-solid ratio/（mL·g^-1）	4∶1	5∶1	6∶1

图1 龙葵不同部位提取物对大肠杆菌、粪肠球菌生长的抑制注：不同小写字母表示同一菌种不同处理间差异在P<0.05水平显著。

Fig. 1 Inhibition of extracts from different parts of Solanum nigrum L. on the growth of Escherichia coli and Enterococcus faecalisNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at P<0.05 level.

表2 龙葵提取物活性成分

Table 2 Phytochemical screening of Solanum nigrum L. extract

样品Sample	单宁Tannin	皂苷Saponin	蒽醌Anthraquinone	甾醇 Sterol	黄酮Flavone	萜类Terpenoids	生物碱Alkaloid
样品Sample	单宁Tannin	皂苷Saponin	蒽醌Anthraquinone	甾醇 Sterol	黄酮Flavone	萜类Terpenoids	Wanger’s检测 Wanger’s test	Dragendorff’s检测 Dragendorff’s test
SNF	+	++	-	+	+	++	+	+
SNS	+	+	-	+	+	+	+	+
SDF	+	++	-	+	+	++	+	+
SDS	+	+	-	+	+	+	+	+
SVF	+	++	-	+	+	++	+	+
SVS	+	+	-	+	+	+	+	+

图2 单因素试验结果注：不同小写字母表示同一菌种不同处理间差异在P<0.05水平显著。

Fig. 2 Results of single factor experimentsNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at P<0.05 level.

表3 Box-Behnken设计方案及结果

Table 3 Programs and experiment results of the Box-Behnken design

试验编号 No.	A：提取温度Temperature	B：乙醇含量Ethanol content	C：液料比 Liquid-solid ratio	抑制率Inhibition rate/%
试验编号 No.	A：提取温度Temperature	B：乙醇含量Ethanol content	C：液料比 Liquid-solid ratio	Y₁：大肠杆菌 Escherichia coli	Y₂：粪肠球菌 Enterococcus faecalis
1	1	0	1	76.92±0.58	83.54±0.82
2	0	0	0	80.64±0.53	88.85±0.76
3	1	-1	0	75.16±0.24	82.05±0.57
4	-1	-1	0	75.86±0.60	82.32±0.46
5	0	1	-1	72.10±0.49	78.95±0.58
6	-1	0	1	77.66±0.72	74.22±0.77
7	0	1	1	72.73±0.31	79.53±0.31
8	0	0	0	78.76±0.57	88.75±0.39
9	0	-1	1	74.69±0.45	81.60±0.88
10	-1	1	0	74.06±0.78	81.20±0.93
11	1	0	-1	75.71±1.00	82.39±0.53
12	0	0	0	79.98±0.85	88.71±0.39
13	-1	0	-1	76.14±0.47	82.83±0.82
14	0	0	0	78.84±0.77	89.36±0.31
15	1	1	0	73.63±0.60	81.16±0.42
16	0	-1	-1	73.75±0.48	80.65±0.72
17	0	0	0	79.55±0.79	89.09±0.57

表4 大肠杆菌抑制率回归模型与方差分析

Table 4 ANOVA of the regression equation model of Escherichia coli inhibition rate

方差来源 Variance source	平方和 Sum of squares	自由度 Degree of freedom	均方 Mean square	F值 F value	P值 P value	显著性 Significance
模型Model	108.440	9	12.050	31.480	<0.000 1	**
A	0.660	1	0.660	1.730	0.230 1	NS
B	6.020	1	6.020	15.730	0.005 4	**
C	2.310	1	2.310	6.040	0.043 6	*
AB	0.018	1	0.018	0.048	0.833 5	NS
AC	0.024	1	0.024	0.063	0.809 4	NS
BC	0.024	1	0.024	0.063	0.809 4	NS
A²	2.650	1	2.650	6.920	0.033 9	*
B²	70.200	1	70.200	183.410	<0.000 1	**
C²	19.520	1	19.520	51.000	0.000 2	**
残差Residual	2.680	7	0.380
失拟项Lack of fit	0.180	3	0.059	0.095	0.958 8	NS
纯误差Pure error	2.500	4	0.630
总和Total	111.120	16

表5 粪肠球菌抑菌率回归模型与方差分析

Table 5 ANOVA of the regression equation model of Enterococcus faecalis inhibition rate

方差来源 Variance source	平方和 Sum of squares	自由度 Degree of freedom	均方 Mean square	F值 F value	P值 P value	显著性 Significance
模型Model	209.990	9	23.330	197.910	<0.000 1	**
A	0.260	1	0.260	2.170	0.184 4	NS
B	4.030	1	4.030	34.210	0.000 6	**
C	2.170	1	2.170	18.440	0.003 6	**
AB	0.010	1	0.010	0.110	0.747 5	NS
AC	0.010	1	0.010	0.120	0.737 0	NS
BC	0.020	1	0.020	0.150	0.705 9	NS
A²	18.850	1	18.850	159.910	<0.000 1	**
B²	111.830	1	111.830	948.530	<0.000 1	**
C²	54.300	1	54.300	460.550	<0.000 1	**
残差Residual	0.830	7	0.120
失拟项Lack of fit	0.530	3	0.180	2.390	0.209 2	NS
纯误差Pure error	0.300	4	0.070
总和Total	210.810	16

图3 各因素交互作用下大肠杆菌的抑菌率

Fig. 3 Inhibition rate of Escherichia coli underinteraction of various factors

图4 各因素交互作用下粪肠球菌的抑菌率

Fig. 4 Inhibition rate of Enterococcus faecalis under interaction of various factors

图5 黑果龙葵果提取物对细菌生物膜形成的影响注：不同小写字母表示同一时间同一菌种不同处理间差异在P<0.05水平显著。

Fig. 5 Effect of Solanum nigrum L. fruit extracts on bacterial biofilm formationNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at same time at P<0.05 level.

图6 黑果龙葵果提取物对细菌表面疏水性的影响注：不同小写字母表示同一菌种不同处理间差异在P<0.05水平显著。

Fig. 6 Effect of Solanum nigrum L. fruit extracts on hydrophobicityNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at P < 0.05 level.

图7 黑果龙葵果提取物对细菌泳动性的影响注：不同小写字母表示同一菌种不同处理间差异在P<0.05水平显著。

Fig. 7 Effect of Solanum nigrum L. fruit extracts on swimmingNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at P<0.05 level.

图8 黑果龙葵果提取物对细菌自聚集性的影响注：不同小写字母表示同一菌种不同处理间差异在P<0.05水平显著。

Fig. 8 Effect of Solanum nigrum L. fruit extracts on auto-aggregationNote：Different lowercase letters indicate significant differences between different treatments of same bacteria at P<0.05 level.

图9 大肠杆菌生物膜形成能力与细菌理化性质相关性分析注：*表示相关性在P<0.05水平显著。

Fig. 9 Correlation analysis between biofilm formation ability and physicochemical properties of Escherichia coliNote：* indicates significant correlation at P<0.05 level.

图10 粪肠球菌生物膜形成能力与细菌理化性质相关性分析注：*表示相关性在P<0.05水平显著。

Fig. 10 Correlation analysis between biofilm formation ability and physicochemical properties of Enterococcus faecalisNote： * indicates significant correlation at P< 0.05 level.

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