青藏高原禾草混播对土壤微生物多样性的影响

doi:10.17521/cjpe.2020.0330

摘要/Abstract

摘要：

土壤微生物多样性的形成、维持和变化机理是生态学研究的核心内容, 已有大量研究表明土壤微生物群落构建不仅受到土壤环境的深刻影响, 也与植物群落物种多样性密切相关。由于自然群落中土壤环境和植物多样性协同影响土壤微生物, 难以区分和厘清植物多样性和土壤环境对土壤微生物多样性构建的各自影响。该研究基于在青藏高原高寒草地构建的人工草地群落, 比较分析了3种优势禾本科牧草单播和混播及施肥处理13年后, 土壤细菌和真菌物种多样性及其与植物群落和土壤理化因子的关系。主要结果: 1)与各单播处理相比, 3种牧草两两混播一致显著降低了土壤细菌群落的丰富度和多样性, 其中变形菌门和放线菌门相对丰度显著增加, 而酸杆菌门、拟杆菌门和浮霉菌门相对丰度显著减小; 牧草混播对土壤真菌多样性没有显著影响。2)牧草混播显著降低了土壤pH和土壤全氮含量, 增加了土壤全磷含量; 施肥显著降低土壤pH, 增加了土壤速效磷含量; 但这些土壤理化因子的变化不足以解释土壤细菌和真菌多样性在处理间的差异。3)施肥显著提高了植物群落地上生物量, 降低了植物物种丰富度, 土壤细菌多样性随植物物种丰富度增加而减小, 而与植物生物量变化无关。该研究在野外条件下, 通过长期控制实验揭示了高寒草地禾草混播并不增加土壤微生物多样性, 为高寒地区牧草混播人工草地实践提供了科学依据。

关键词: 植物多样性, 土壤微生物多样性, 混播, 多样性促进多样性

Abstract:

Aims How soil microbial diversity assembly, maintain and change is a key topic of ecology. A large number of studies show that soil microbial biodiversity is controlled not only by soil environment but also by plant species. However, due to strong covariation between the two factors in the field, it remains a challenge to isolate and clarify the role of plant diversity in regulating soil microbial biodiversity. Hence, here, we aim to clarify how plant diversity affects soil microbial diversity in environment-consistent artificial communities.
Methods In this study, we examined differences in species diversity of soil bacteria and fungi among plots subjected single- and mixed-sowing of three grass species with fertilization treatments after 13 years’ experiment on the eastern Qingzang (Tibetan) Plateau. We also analyzed the relationships between soil microbial diversity and edaphic factors as well as plant community attributes.
Important findings (1) The species richness and diversity of soil bacteria, not including soil fungi, significantly and consistently decreased in mixed-sowing plots relative to single-sowing plots, with higher relative abundances in proteobacteria and actinobacteria but lower in acidobacteria, bacteroidetes and planctomycetes in the mixed- sowing plots. (2) Soil pH and total nitrogen content significantly decreased while soil total phosphorus content increased in mixed-sowing plots relative to single-sowing plots. Fertilization significantly increased soil available phosphorus while decreased soil pH and soil humidity. However, variations in these edaphic factors contributed little in variation of soil microbial diversity. (3) Fertilization significantly increased plant aboveground biomass while decreasing richness of present plant species, which was also negatively associated with soil bacterial diversity. In short, this long-term field experiment clearly showed that mixed-sowing of common grass species did not promote diversity of soil microbes. This study provides new insight into management of grasses mixed-sowing artificial grasslands.

Key words: plant diversity, soil microbial diversity, mixed-sowing, diversity begets diversity

姜鑫, 牛克昌. 青藏高原禾草混播对土壤微生物多样性的影响. 植物生态学报, 2021, 45(5): 539-551. DOI: 10.17521/cjpe.2020.0330

JIANG Xin, NIU Ke-Chang. Effects of grass mixed-sowing on soil microbial diversity on the Qingzang (Tibetan) Plateau. Chinese Journal of Plant Ecology, 2021, 45(5): 539-551. DOI: 10.17521/cjpe.2020.0330

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2020.0330

https://www.plant-ecology.com/CN/Y2021/V45/I5/539

图/表 7

表1 广义线性混合模型检验混播和施肥对土壤微生物多样性的影响

Table 1 Summary of the effect of mix-sowing and fertilization on variation in soil microbial diversity tested by generalized linear mixed effect model

变量 Variable	变异度 Variability (%) \| F		混播 Mixed- Sowing	施肥 Fertilized
变量 Variable	单播/混播 Single-sowing/Mixed-sowing (df = 1)	施肥/不施肥 Fertilized/Unfertilized (df = 2)	混播 Mixed- Sowing	单播 Single-sowing	混播 Mixed-sowing
土壤微生物多样性 Soil microbial diversity
细菌丰富度(Chao1) Bacterial richness (Chao1)	38.33 \| 37.87^*	2.72 \| 0.69	-96.92^*	-30.44	-13.61
细菌Shannon多样性 Bacterial Shannon diversity	44.35 \| 41.51^*	0.15 \| 0.04	-0.60^*	-0.02	-0.05
真菌丰富度(Chao1) Fungal richness (Chao1)	16.03 \| 3.10	2.18 \| 0.50	-28.22	19.30	-12.65
真菌Shannon多样性 Fungal Shannon diversity	8.16 \| 3.36	7.14 \| 1.33	-0.15	-0.04	-0.50
土壤理化因子 Soil edaphic factor
土壤pH Soil pH	18.17 \| 55.48^*	27.47 \| 7.25^*	-0.22^*	-0.24^*	-0.12^*
土壤湿度 Soil humidity	10.95 \| 3.49	9.01 \| 1.87	0.02	-0.01	-0.02
土壤全氮含量 Soil total nitrogen content	68.81 \| 51.36^*	2.46 \| 1.47	-0.21^*	0.06	0.00
土壤全磷含量 Soil total phosphorus content	41.15 \| 16.46^*	5.23 \| 1.68	1.23^*	0.18	0.46
土壤有效氮含量 Soil available nitrogen content	0.38 \| 0.77	0.80 \| 0.12	-0.00	-0.18	0.00
土壤速效磷含量 Soil available phosphorus content	8.25 \| 4.43	31.78 \| 8.47^*	0.04	0.08^*	0.05^*
土壤有机碳含量 Soil organic carbon content	0.52 \| 0.26	9.07 \| 1.54	1.20	3.01	-0.42
植物群落 Plant community
植物地上生物量 Plant aboveground biomass	1.45 \| 0.44	27.98 \| 6.83^*	-11.20	14.36	26.93^*
植物物种丰富度 Plant species richness	0.84 \| 1.01	34.08 \| 7.69^*	1.33	-1.11	-4.89^*

图1 混播和施肥对土壤细菌和真菌多样性的影响(平均值±标准误)。A, 细菌丰富度(Chao 1)。B, 细菌Shannon多样性。C, 真菌丰富度(Chao 1)。D, 真菌Shannon多样性。En, 垂穗披碱草; Fo, 羊茅; Fs, 中华羊茅。

Fig. 1 Effect of mixed-sowing and fertilization on variation in soil bacterial and fungal diversities relative to single-sowing and unfertilized treatment (mean ± SE). A, bacterial richness (Chao 1). B, bacterial Shannon diversity. C, fungal richness (Chao 1). D, fungal Shannon diversity. En, Elymus nutans; Fo, Festuca ovina; Fs, F. sinensis.

图2 单播和混播处理中, 土壤细菌和真菌各门水平优势菌群相对丰度比较。A, 细菌门水平优势类群相对丰度。B, 真菌门水平优势类群相对丰度。En, 垂穗披碱草; Fo, 羊茅; Fs, 中华羊茅。图中*表示与单播与混播处理间该菌群相对丰度的差异显著(p < 0.05)。其他细菌包括装甲菌门、衣原体门、绿弯菌门、蓝藻门、迷踪菌门、厚壁菌门、芽单胞菌门、硝化螺旋菌门等16个细菌门类; 其他真菌包括壶菌门、球囊菌门以及3种未知真菌门共5个真菌门类。

Fig. 2 Relative abundance of dominant phyla of soil bacteria and fungi in single- and mixed-sowing plots, with significant difference between them (p < 0.05) indicated by *. A, Dominant phyla of bacteria. B, Dominant phyla of fungi. En, Elymus nutans; Fo, Festuca ovina; Fs, F. sinensis. Others of bacteria include Armatimonadetes, BRC1, Candidatus_Saccharibacteria, Chlamydiae, Chloroflexi, Cyanobacteria, Elusimicrobia, Firmicutes, Gemmatimonadetes, Ignavibacteriae, Latescibacteria, Nitrospirae, Parcubacteria, Unclassified_Bacteria, candidate_division_WPS-1 and candidate_division_WPS-2. Others of fungi include Chytridiomycota, Glomeromycota and three uclassified fungi phyla.

表2 广义线性混合模型检验混播和施肥对土壤微生物优势菌群(门水平)的影响

Table 2 Summary of the effect of mix-sowing and fertilization on variation in dominant phyla of soil microbes tested by generalized linear mixed effect model

微生物类群 Microbes taxon	变异度 Variability (%) \| F		混播 Mixed- Sowing	施肥 Fertilized
微生物类群 Microbes taxon	单播/混播 Single-sowing/Mixed-sowing (df = 1)	施肥/不施肥 Fertilized/Unfertilized (df = 2)	混播 Mixed- Sowing	单播 Single- sowing	混播 Mixed- sowing
细菌门水平优势类群 Dominant phylum of bacteria
酸杆菌门 Acidobacteria	32.84 \| 11.81^*	2.48 \| 0.65	-0.05^*	0.00	0.02
放线菌门 Actinobacteria	12.42 \| 9.13^*	13.84 \| 2.83	0.01^*	0.00	-0.01^*
拟杆菌门 Bacteroidetes	34.68 \| 13.62^*	0.93 \| 0.24	-0.03^*	0.01	0.00
浮霉菌门 Planctomycetes	21.33 \| 5.59	0.73 \| 0.16	-0.02	0.00	0.00
变形菌门 Proteobacteria	32.67 \| 28.11^*	0.47 \| 0.11	0.08^*	-0.01	-0.01
疣微菌门 Verrucomicrobia	0.23 \| 0.04	8.19 \| 1.77	0.00	0.01	0.01
真菌门水平优势菌群 Dominant phylum of fungi
子囊菌门 Ascomycota	1.07 \| 0.85	1.25 \| 0.19	-0.05	0.01	0.05
担子菌门 Basidiomycota	2.03 \| 1.82	1.14 \| 0.18	0.02	-0.04	-0.01
接合菌门 Zygomycota	1.51 \| 0.82	4.47 \| 0.72	0.04	0.04	0.06

图3 单播和混播处理中土壤微生物群落结构。A, 细菌群落。B, 真菌群落。En, 垂穗披碱草; Fo, 羊茅; Fs, 中华羊茅。

Fig. 3 Difference in soil microbial community compositions in single- and mixed-sowing plots. A, Soil bacterial community composition. B, Soil fungal community composition. En, Elymus nutans; Fo, Festuca ovina; Fs, F. sinensis. PAB, plant aboveground biomass; PSR, plant species richness; SAN, soil available nitrogen; SAP, soil available phosphorus; SOC, soil organic carbon; STN, soil total nitrogen; STP, soil total phosphorus.

图4 土壤细菌和真菌多样性与土壤理化因子和植物群落关系的多元相关分析。A, 细菌。B, 真菌。En, 垂穗披碱草; Fo, 羊茅; Fs, 中华羊茅。Wilks’ Lambda多元检验显示单播和混播差异显著(p < 0.05)。

Fig. 4 Generalized canonical discriminant analysis for links among soil bacterial and fungal diversities, edaphic factors and plant community. A, Bacteria. B, Fungal. En, Elymus nutans; Fo, Festuca ovina; Fs, F. sinensis. There are significant difference between single- and mixed-sowing plots tested by a Wilks’ lambda multivariate test. PAB, plant aboveground biomass; PSR, plant species richness; SAN, soil available nitrogen; SAP, soil available phosphorus; SOC, soil organic carbon; STN, soil total nitrogen; STP, soil total phosphorus.

表3 广义线性混合模型检验土壤微生物多样性与各土壤理化因子及植物群落的相关关系(平均值±标准误)

Table 3 Association of soil microbial diversity with edaphic factors and plant community tested by generalized linear mixed effect model (mean ± SE)

固定因子 Fixed factor	细菌丰富度(Chao1) Bacterial richness (Chao1) R² = 0.57^*	细菌Shannon多样性 Bacterial Shannon diversity R² = 0.57^*	真菌丰富度(Chao1) Fungal richness (Chao1) R² = 0.35	真菌Shannon多样性 Fungal Shannon diversity R² = 0.19
土壤理化因子 soil edaphic factor
土壤pH Soil pH	-15.24 ± 13.55	-0.10 ± 0.09	-9.79 ± 12.88	0.05 ± 0.18
土壤湿度 Soil humidity	-25.96 ± 11.78^*	-0.09 ± 0.08	-21.80 ± 11.20	-0.13 ± 0.16
土壤全氮含量 Soil total nitrogen content	5.62 ± 19.72	0.13 ± 0.13	23.13 ± 19.02	0.04 ± 0.27
土壤全磷含量 Soil total phosphorus content	-3.28 ± 13.36	-0.04 ± 0.08	-16.29 ± 12.92	-0.11 ± 0.18
土壤有效氮含量 Soil available nitrogen content	-13.50 ± 9.53	-0.09 ± 0.06	3.67 ± 9.01	0.12 ± 0.13
土壤速效磷含量 Soil available phosphorus content	28.74 ± 11.99^*	0.11 ± 0.08	1.07 ± 11.48	0.03 ± 0.17
土壤有机碳含量 Soil organic carbon content	-0.25 ± 9.82	0.01 ± 0.06	-24.04 ± 9.38^*	-0.05 ± 0.14
植物群落 Plant community
植物地上生物量 Plant aboveground biomass	-4.35 ± 10.83	-0.10 ± 0.07	-14.30 ± 10.47	-0.13 ± 0.15
植物物种丰富度 Plant species richness	-23.85 ± 10.77^*	-0.14 ± 0.07	5.89 ± 10.18	-0.07 ± 0.15
处理影响 Treatment effect
混播 Mixed-sowing	-91.07 ± 38.55^*	-0.47 ± 0.24	13.46 ± 38.35	-0.13 ± 0.53
施肥 Fertilized	-103.52 ± 34.32^*	-0.37 ± 0.22	10.27 ± 32.62	-0.20 ± 0.48

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