铅胁迫下接种AM真菌对龙葵根际土壤微生物群落代谢特征的影响

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韩娟,
张向前,
赵金莉^,
河北大学生命科学学院保定 071002
基金项目: 河北省自然科学基金项目C2017201044
河北大学大学生创新训练项目2017126

详细信息

作者简介:韩娟, 主要从事菌根生物技术方面的研究。E-mail:junhan_hbu@126.com

通讯作者:赵金莉, 主要从事土壤生态学方面的研究。E-mail：plant@hbu.edu.cn

中图分类号:S154.3

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出版历程

收稿日期:2018-11-29
录用日期:2018-12-05
刊出日期:2019-04-01

Effect of arbuscular mycorrhizal fungi on metabolic characteristics of microbial community in Solanum nigrum rhizosphere soil with lead stress

HAN Juan,
ZHANG Xiangqian,
ZHAO Jinli^,
College of Life Sciences, Hebei University, Baoding 071002, China
Funds: the Natural Science Foundation of Hebei ProvinceC2017201044
the Student Innovation Training Project of Hebei University2017126

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Corresponding author:ZHAO Jinli, E-mail: plant@hbu.edu.cn

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摘要
摘要:为从微生态角度探索接种AM真菌对铅污染根际土壤微生物群落代谢特征的影响，以摩西管柄囊霉（Funneliformis mosseae）和幼套近明囊霉（Claroideoglomus etunicatum）为接种菌剂，在温室盆栽条件下以Pb⁴⁺含量为0 mg·kg^-1、200 mg·kg^-1、400 mg·kg^-1和800 mg·kg^-1土壤种植龙葵（Solanum nigrum）10周后采集根际土壤，采用Biolog微平板法测定龙葵根际土壤微生物群落的代谢变化。结果表明：1）微生物平均代谢活性（AWCD）随铅浓度增加呈降—升—降趋势；接种AM真菌显著提高了铅胁迫下根际土壤微生物的AWCD值，仅中浓度（400 mg·kg^-1）下未达显著差异。2）中浓度铅处理能显著提高根际土壤微生物对糖类及其衍生物、氨基酸类、脂肪酸和脂类及代谢产物类四大类碳源底物利用能力；接种AM真菌，高浓度（800 mg·kg^-1）铅处理显著提高了根际土壤微生物对氨基酸类底物的利用能力。3）铅胁迫下接种AM真菌提高了根际土壤微生物多样性指数，在中浓度下丰富度指数、Shannon-Wiener多样性指数、Simpson优势度指数均达显著水平。4）主成分分析显示，代谢产物类在PC1和PC2中种类最多，分别为6种和4种；糖类及其衍生物在PC3中种类最多（5种）。5）在铅胁迫和接种AM真菌共同作用下，微生物碳源利用主要受铅浓度调节，并且二者对微生物碳源利用具有显著交互效应。综上可知，接种AM真菌能够提高铅胁迫下龙葵根际土壤微生物多样性指数，增强根际土壤微生物对碳源底物的利用能力。该研究为进一步探究AM真菌强化植物联合修复技术提供了依据。
Abstract:Pot experiments were conducted to explore the effect of arbuscular mycorrhiza (AM) fungi on the characteristics and differences in rhizosphere soils of Solanum nigrum under different levels of lead stress[0 mg·kg^-1 (CK), 200 mg·kg^-1, 400 mg·kg^-1, 800 mg·kg^-1). To this end, S. nigrum was inoculated with Funneliformis mosseae and Claroideoglomus etunicatum, and the resulting rhizosphere soils collected after 10 weeks of growth under 16 h/8 h, 28℃/20℃ with 12 000 Lux light intensity in a greenhouse. The characteristics and differences in carbon metabolic profiles of microbes were evaluated using the Biolog-ECO micro-plate method. The results showed that:1) the average metabolic activity of microorganisms, described by average well color development (AWCD), decreased-increased-decreased with increasing lead stress. Inoculation with AM fungi improved AWCD significantly under lead stresses, except for 400 mg·kg^-1 Pb⁴⁺. 2) The ability of soil microbes to utilize the four types of carbon substrates (carbohydrate and derivatives, fatty acid and lipids, amino acids, and metabolites) was higher under 400 mg·kg^-1 Pb⁴⁺ than under low (200 mg·kg^-1) and high (800 mg·kg^-1) stresses of Pb⁴⁺. Inoculation with AM fungi significantly improved the ability of soil microbes to utilize amino acid substrates under high lead concentration. 3) Lead stress reduced McIntosh evenness index of rhizosphere soil microbial community, but had no significant impact on richness index, Shannon-Wiener diversity index and Simpson index. Inoculation with AM fungi increased microbial diversity index under lead treatment, and had significant effects on Species richness index, Shannon-Wiener diversity index and Simpson dominance index at medium stress. 4) Under the same Pb⁴⁺ stress, inoculation of AM fungi enhanced metabolic capacity of soil microorganisms for the four major carbon sources, but only had significant effect on amino acids. Principal component analysis showed that metabolites were the most abundant in PC1 and PC2, with respective values of 6 and 4. Sugar was the most abundant in PC3. 5) Under combined effects of lead stress and AM fungi, microbial carbon source utilization was mainly regulated by lead concentration, both had significant interaction effects on microbial carbon source utilization. In conclusion, inoculation with AM fungi increased microbial diversity index of rhizosphere soils of S. nigrum under lead stress, and enhanced utilization of carbon source substrate by rhizosphere soil microbes. This study provided theoretical basis for the application of AM fungi which could strengthen the use of phytoremediation technology in soil remediation for heavy metal pollution.

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图1菌剂接种及播种方式
Figure1.Method of inoculation and seeding

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图2接种AM真菌对铅胁迫下龙葵根际土壤微生物平均颜色变化率(AWCD)的影响
CK:未接种AM真菌, Pb⁴⁺为0 mg·kg^-1; AM:接种AM真菌; Pb1: Pb⁴⁺浓度为200 mg·kg^-1(低浓度); Pb2: Pb⁴⁺浓度为400 mg·kg^-1(中浓度); Pb3: Pb⁴⁺浓度为800 mg·kg^-1(高浓度)。*和**分别表示在P < 0.05和P < 0.01水平差异显著。
Figure2.Effect of AM fungi inoculation on the average well color development (AWCD) of microbia in rhizosphere soil of Solanum nigrum under lead stress
CK: no AM with 0 mg·kg^-1 Pb⁴⁺; AM: inoculation of AM; Pb1: low Pb⁴⁺ concentration (200 mg·kg^-1); Pb2: medium Pb⁴⁺ concentration (400 mg·kg^-1); Pb3: high Pb⁴⁺ concentration (800 mg·kg^-1). * and ** mean significant difference at P < 0.05 and P < 0.01 levels, respectively.

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图3接种AM真菌和铅胁迫下龙葵根际土壤微生物群落碳源代谢特征的主成分分析
CK:未接种AM真菌, Pb⁴⁺为0 mg·kg^-1; AM:接种AM真菌; Pb1: Pb⁴⁺浓度为200 mg·kg^-1(低浓度); Pb2: Pb⁴⁺浓度为400 mg·kg^-1(中浓度); Pb3: Pb⁴⁺浓度为800 mg·kg^-1(高浓度)。
Figure3.Principal component analysis for carbon source utilization of soil microbes in Solanum nigrum rhizosphere under inoculation of AM and lead stress
CK: no AM with 0 mg·kg^-1 Pb⁴⁺; AM: inoculation AM; Pb1: low Pb⁴⁺ concentration (200 mg·kg^-1); Pb2: medium Pb⁴⁺ concentration (400 mg·kg^-1); Pb3: high Pb⁴⁺ concentration (800 mg·kg^-1).

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表1接种AM真菌和铅胁迫对各测定指标影响的方差分析
Table1.ANOVA analysis results of effects of AM inoculation and lead stress on the investigated indexes of the experiment

指标 Index	变异来源Source of variation
	AM接种(AM) AM inoculation		铅处理(Pb) Pb treatment		AMxPb
	F	P	F	P	F	P
平均颜色变化率Average well color development (AWCD)	11.456	**	5.851	**	3.793	*
物种多样性指数Shannon-Wiener diversity index (H')	24.750	***	1.031	NS	0.269	NS
优势度指数Simpson dominance index (D)	30.727	***	0.438	NS	0.511	NS
丰富度指数Species richness index (S)	19.678	***	2.444	NS	0.611	NS
McIntosh均匀度指数McIntosh evenness index (U)	5.270	*	5.232	**	3.428	*
糖类及其衍生物Carbohydrate and its derivates	0.030	NS	22.922	***	23.623	***
氨基酸类Amino acid	0.268	NS	4.380	*	3.951	*
脂肪酸及脂类Fatty acid and lipid	0.072	NS	7.814	**	10.344	***
代谢产物Metabolites	5.709	*	6.952	**	6.538	**
NS:不显著; :显著水平为P < 0.05; :显著水平为P < 0.01; *:显著水平为P < 0.001。NS: no significant difference; : significant difference at P < 0.05; : significant difference at P < 0.01; *: significant difference at P < 0.001.

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表2接种AM真菌对铅胁迫下龙葵根际土壤微生物功能多样性指数的影响
Table2.Effect of AM fungi inoculation on soil microbial function diversity indexes of Solanum nigrum rhizosphere soil under lead stress

处理 Treatment	丰富度指数 Species richness index	Shannon-Wiener多样性指数 Shannon-Wiener diversity index	Simpson优势度指数 Simpson dominance index	McIntosh均匀度指数 McIntosh evenness index
CK	24.67±1.33aA	3.175 4±0.002 9aA	0.951 5±0.000 4aA	3.760 4±0.045 0aA
Pb1	22.67±0.88bA	3.079 0±0.054 5aA	0.945 6±0.003 9aA	3.494 7±0.320 1aA
Pb2	24.67±2.03aA	3.128 1±0.085 8aA	0.950 0±0.004 7aA	3.037 3±0.654 4bA
Pb3	24.00±1.15aA	3.139 0±0.022 3aA	0.948 9±0.001 2aA	3.593 7±0.337 7aA
AM+CK	29.67±0.33aB	3.303 7±0.024 3aA	0.960 0±0.001 4aB	5.774 5±0.154 0aB
AM+Pb1	26.00±1.15bA	3.263 7±0.008 5aB	0.957 4±0.000 7aB	4.225 0±0.248 8bA
AM+Pb2	29.00±0.58aB	3.277 4±0.027 1aB	0.957 9±0.001 6aB	4.771 1±0.345 4abA
AM+Pb3	26.33±0.33bA	3.238 4±0.009 1aA	0.955 8±0.000 5aA	4.212 7±0.337 4bA
CK:未接种AM真菌, Pb⁴⁺为0 mg·kg^-1; AM:接种AM真菌; Pb1: Pb⁴⁺浓度为200 mg·kg^-1(低浓度); Pb2: Pb⁴⁺浓度为400 mg·kg^-1(中浓度); Pb3: Pb⁴⁺浓度为800 mg·kg^-1(高浓度)。同列不同小写字母分别表示接种AM真菌或未接种AM真菌处理下不同Pb⁴⁺浓度间差异显著(P < 0.05);同列不同大写字母表示同一Pb⁴⁺浓度下接种AM和不接种AM处理间差异显著(P < 0.05)。CK: no AM with 0 mg·kg^-1 Pb⁴⁺; AM: inoculation of AM; Pb1: low Pb⁴⁺ concentration (200 mg·kg^-1); Pb2: medium Pb⁴⁺ concentration (400 mg·kg^-1); Pb3: high Pb⁴⁺ concentration (800 mg·kg^-1). Different lowercase letters in the same column indicate significant differences among different concentrations of Pb⁴⁺ at P < 0.05. Different capital letters in the same column indicate significant differences between AM inoculation and no inoculation under the same Pb⁴⁺ concentration at P < 0.05.

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表3接种AM真菌对铅胁迫下龙葵根际土壤微生物碳源利用强度的影响
Table3.Effect of AM fungi inoculation on carbon source utilization of soil microbes in Solanum nigrum rhizosphere under lead stress

处理 Treatment	碳源类型Carbon sources
处理 Treatment	糖类及其衍生物 Carbohydrate and derivatives	氨基酸类 Amino acids	脂肪酸和脂类 Fatty acid and lipids	代谢产物 Metabolites
CK	0.664 4±0.046 9aA	0.573 5±0.028 6aA	0.575 9±0.062 6aA	0.315 5±0.022 9aA
Pb1	0.553 4±0.012 5aA	0.722 7±0.048 2aA	0.507 2±0.071 7aA	0.334 8±0.080 7aA
Pb2	0.914 3±0.062 8bA	0.808 8±0.063 1aA	0.604 0±0.131 2aA	0.503 2±0.105 9bA
Pb3	0.614 3±0.097 0aA	0.554 0±0.054 5aA	0.549 7±0.076 1aA	0.305 7±0.032 6aA
AM+CK	0.981 6±0.041 1aB	1.032 7±0.015 4aB	0.941 2±0.061 8aB	0.774 4±0.018 6aB
AM+Pb1	0.748 5±0.057 0abA	0.744 3±0.036 9bA	0.640 9±0.042 1bA	0.479 0±0.060 4bA
AM+Pb2	0.842 3±0.066 1abA	0.848 2±0.050 9abA	0.687 9±0.024 8bA	0.571 7±0.039 4bA
AM+Pb3	0.683 4±0.032 4bA	0.849 2±0.119 7abB	0.637 5±0.0577 bA	0.444 9±0.070 4bA
CK:未接种AM真菌, Pb⁴⁺为0 mg·kg^-1; AM:接种AM真菌; Pb1: Pb⁴⁺浓度为200 mg·kg^-1(低浓度); Pb2: Pb⁴⁺浓度为400 mg·kg^-1(中浓度); Pb3: Pb⁴⁺浓度为800 mg·kg^-1(高浓度)。同列不同小写字母分别表示接种AM真菌或未接种AM真菌处理下不同Pb⁴⁺浓度间差异显著(P < 0.05);同列不同大写字母表示同一Pb⁴⁺浓度下接种AM和不接种AM处理间差异显著(P < 0.05)。CK: no AM with 0 mg·kg^-1 Pb⁴⁺; AM: inoculation of AM; Pb1: low Pb⁴⁺ concentration (200 mg·kg^-1); Pb2: medium Pb⁴⁺ concentration (400 mg·kg^-1); Pb3: high Pb⁴⁺ concentration (800 mg·kg^-1). Different lowercase letters in the same column indicate significant differences among concentrations of Pb⁴⁺ at P < 0.05. Different capital letters in the same column indicate significant differences between AM inoculation and no inoculation under the same Pb⁴⁺ concentration at P < 0.05.

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表4接种AM真菌和铅胁迫下龙葵根际土壤微生物Biolog-ECO板上碳源利用的主成分载荷矩阵
Table4.Principal components loading matrix for soil microbes carbon source utilization of Biolog-ECO in Solanum nigrum rhizosphere under inoculation of AM and lead stress

碳源编号 Code of carbon source	碳源类别 Carbon sources	底物 Substrate	提取的主成分 Principal component of extraction
碳源编号 Code of carbon source	碳源类别 Carbon sources	底物 Substrate	PC1	PC2	PC3	PC4	PC5	PC6
A2	糖类及其衍生物 Saccharides and derivates	-甲基D-葡萄糖β-methyl-D-glucoside	-0.112	0.167	0.072	-0.968	0.021	-0.112
A3		D-半乳糖酸γ内酯D-galactonic acid γ-lactone	0.137	0.286	0.624	-0.060	0.254	0.653
B2		D-木糖D-xylose	0.717	0.452	0.369	-0.186	0.316	0.014
B3		D-半乳糖醛酸D-galacturonic acid	-0.492	0.349	0.292	0.159	-0.113	0.709
C2		i-赤藓糖醇i-erythritol	0.577	0.357	0.225	0.101	0.614	-0.316
D2		D-甘露醇D-mannitol	0.575	0.303	0.751	-0.011	-0.040	0.104
E1		α环状糊精α-cyclodextrin	0.768	0.353	0.206	0.226	0.087	-0.014
E2		N-乙酰基-D-葡萄糖氨N-acetyl-D-glucosamine	0.096	-0.123	0.889	0.168	0.202	0.028
F1		肝糖Glycogen	0.159	0.719	0.559	-0.080	0.276	0.250
F2		D-氨基葡萄糖酸D-glucosaminic acid	0.588	0.277	0.178	0.723	0.131	-0.078
G1		D-纤维二糖D-cellobiose	0.400	0.216	0.845	0.120	0.231	0.107
H1		α-D-乳糖α-D-lactose	0.407	0.177	0.309	0.079	0.804	0.218
A4	氨基酸类 Amino acid	L-精氨酸L-arginine	0.377	0.503	0.200	0.741	0.089	-0.090
B4		L-天冬酰胺L-asparagine	0.206	-0.414	-0.815	0.249	0.178	0.077
C4		L-苯丙氨酸L-phenylalanine	-0.045	0.397	0.774	-0.323	-0.346	0.129
D4		L-丝氨酸L-serine	0.095	0.061	0.833	0.429	0.059	0.309
E4		L-苏氨酸L-threonine	0.795	0.525	0.139	0.080	0.137	-0.098
F4		甘氨酰-L-谷氨酸Glycyl-L-glutamic acid	0.380	0.761	0.109	0.402	0.303	0.099
B1	脂肪酸和脂类 Fatty acids and lipids	丙酮酸甲酯Pyruvic acid methyl ester	0.795	0.258	0.035	0.488	0.150	0.198
C1		吐温40 Tween40	0.367	0.809	0.095	-0.257	0.206	0.299
D1		吐温80 Tween 80	0.325	0.835	0.386	0.131	0.034	0.170
E3		γ-羟基丁酸γ-hydroxybutyric acid	0.737	0.316	-0.095	0.492	0.216	-0.156
F3		衣康酸Itaconic acid	0.193	0.863	0.405	0.004	-0.076	-0.207
C3	代谢产物类 Metabolites	2-羟基苯甲酸2-hydroxy benzoic acid	0.968	-0.100	0.015	0.107	0.161	0.019
D3		4-羟基苯甲酸4-hydroxy benzoic acid	0.554	0.671	0.310	0.377	-0.017	0.024
G2		葡萄糖-1-磷酸盐Glucose-1-phosphate	0.817	0.565	0.031	0.047	-0.072	-0.062
G3		α-丁酮酸α-ketobutyric acid	0.768	0.227	0.134	0.318	0.472	-0.127
G4		苯乙胺Phenylethylamine	0.071	0.302	0.879	0.066	0.345	-0.008
H2		D, L-a-磷酸甘油D, L-α-glycerol phosphate	0.163	0.947	0.016	0.126	0.215	0.146
H3		D-苹果酸D-malic acid	0.577	0.672	0.317	0.184	-0.194	0.182
H4		腐胺Putrescine	0.641	0.209	0.380	0.428	0.248	0.396

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