Effects of plant functional groups removal on soil fungal community structure and diversity in an alpine meadow on the Qinghai-Tibet Plateau
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摘要:
为研究植物多样性丧失对土壤真菌群落的影响，本研究在青藏高原高寒草甸进行了为期3年的植物功能群移除实验，实验共设置5个处理：不移除任何植物功能群（CK）、移除豆科和杂类草而保留禾状草、移除禾状草和杂类草而保留豆科、移除禾状草和豆科而保留杂类草以及移除所有功能群。本研究分析了高寒草甸不同植物功能群移除对根系性质、土壤理化性质的影响，并利用高通量基因测序技术分析了不同处理对土壤真菌群落结构和多样性的影响。结果显示，不同处理下均以子囊菌门、被孢霉门、担子菌门为优势类群，占土壤真菌群落的90%以上。土壤真菌群落结构和多样性在不同植物移除处理下变化不显著。球囊菌门的相对丰度在保留杂类草、保留豆科的处理中显著高于对照。捕虫霉门的相对丰度在保留豆科处理中显著高于其他处理。不同处理下土壤真菌优势功能类群为土壤腐生营养型。丛枝菌根真菌相对丰度在保留禾状草、保留豆科处理中显著高于对照。地衣寄生菌/腐生菌的相对丰度在保留杂类草处理中显著高于移除所有植物功能群处理。利用Mantel test检验，未发现土壤真菌群落结构和功能与环境因子具有显著相关性。土壤真菌丰富度与根系生物量、根系碳氮比、可溶性有机碳含量呈负相关关系。研究结果说明，青藏高原高寒草甸植物移除3年后，土壤真菌群落结构发生改变，但并未对真菌群落多样性指数产生显著影响。
Abstract:To investigate the effect of plant diversity on soil fungal communities, we conducted a three-year experiment in an alpine meadows on the Qinghai-Tibet Plateau. The experiment included five treatments: no removal, legume and forb removal, graminoid and forb removal, graminoid and legume removal, and all removal. We analyzed soil fungal abundance and diversity using high-throughput sequencing, and measured root and soil properties. Results showed that Ascomycota, Mortierellomycota, and Basidiomycota were the dominant fungal phyla in the different treatments, accounting for more than 90%. There were no significant differences in composition and alpha diversity indices of the fungal communities under different treatments. The relative abundance of Glomeromycota was increased under graminoid and forb removal and graminoid and legume removal. Compared to the other treatments, the removal of graminoids and forbs increased the relative abundance of Zoopagomycota. The dominant fungal functional group was soil saprotroph fungi in all treatments. The relative abundance of arbuscular mycorrhizal fungi was increased under legume and forb removal and graminoid and forb removal. Compared with the removal of all, the removal of graminoids and legumes increased the relative abundance of lichen parasites/saprotroph fungi. The Mantel test showed no clear correlation between soil fungal community composition and function and environmental factors. Soil fungal richness indices were negatively affected by the increase in root biomass, root carbon:nitrogen (C:N), and dissolved organic carbon. Overall, our results indicate that the removal of plant functional groups in alpine meadows on the Qinghai-Tibet Plateau has a significant effect on soil fungal community structure but not on fungal community diversity.
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Keywords:
- Alpine meadow /
- Plant functional group removal /
- Soil fungi /
- Plant-soil interaction
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图 2 不同植物功能群移除下土壤真菌群落结构组成
A：不同处理土壤真菌OTUs的Venn图；B：不同样品的门水平土壤真菌群落结构组成；C：不同处理下门水平的土壤真菌群落NMDS图。CK：不移除；Forbs：移除禾状草和豆科而保留杂类草；Graminoids：移除豆科和杂类草而保留禾状草；Legumes：移除禾状草和杂类草而保留豆科；None：移除所有植物功能群。
Figure 2. Soil fungal community composition under removal of different plant functional groups
A: Venn diagram of soil fungal OTUs in different treatments; B: Phylum-level soil fungal community composition in different samples; C: NMDS diagram of phylum-level soil fungal community in different treatments. CK: No removals; Forbs: Removal of graminoids and legumes; Graminoids: Removal of legumes and forbs; Legumes: Removal of graminoids and forbs; None: Removal of all.
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图 3 环境因子对土壤真菌群落结构和功能的影响（Mantel test）
SWC：土壤含水率；TC：总碳；TN：总氮；C:N：碳氮比；SOC：土壤有机碳；DOC：可溶性有机碳；NH+4-N：铵态氮；NO−3-N：硝态氮；Root TC：根总碳；Root TN：根总氮；Root C:N：根系碳氮比；Root biomass：根系生物量。下同。
Figure 3. Effects of environmental factors on soil fungal community composition and function
SWC: Soil water content; TC: Total carbon; TN: Total nitrogen; C:N: Carbon-to-nitrogen ratio; SOC: Soil organic carbon; DOC: Dissolved organic carbon; NH+4-N: Ammonium nitrogen; NO−3-N: Nitrate nitrogen. Root TC: Root total carbon; Root TN: Root total nitrogen; Root C:N: Root carbon-to-nitrogen ratio. Same below.
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图 4 土壤真菌多样性与环境因子相关性分析
OTUs：操作分类单位；Shannon：香农指数；Pielou：均匀度指数； D：辛普森指数；Chao1：描述样品中所含OTUs数目的指数；Ace：样本中物种组成的丰富度和均匀度。
Figure 4. Correlation of soil fungal diversity and environmental factors
OTUs: Operational taxonomic units; Shannon: Shannon-Wiener index; Pielou: Pielou’s evenness index; D: Simpson index; Chao1: An index describing the number of OTUs contained in a sample; Ace: An index describing the richness and evenness of species composition in a sample.
表 1 不同植物功能群移除下根系性质
Table 1 Root properties under removal of different plant functional groups
指标Index CK Forbs Graminoids Legumes None 根总碳 / g/kg 332.0 ± 6.0a 275.6 ± 7.8a 279.1 ± 31.1a 271.2 ± 29.4a 300.3 ± 27.0a 根总氮 / g/kg 8.91 ± 0.85a 8.63 ± 0.74a 8.14 ± 0.25a 9.04 ± 0.65a 9.43 ± 0.49a 根系碳氮比 34.04 ± 5.44a 32.85 ± 2.76a 34.59 ± 4.35a 30.13 ± 2.81a 31.80 ± 2.13a 根系生物量 / kg/m2 0.68 ± 0.23a 0.85 ± 0.20a 0.77 ± 0.12a 0.72 ± 0.16a 0.54 ± 0.15a 注：同行不同小写字母表示在0.05水平上差异显著。CK：不移除；Forbs：移除禾状草和豆科而保留杂类草；Graminoids：移除豆科和杂类草而保留禾状草；Legumes：移除禾状草和杂类草而保留豆科；None：移除所有植物功能群。下同。 Notes: Different lowercase letters in the same row indicate significant differences at the 0.05 level. CK: No removals; Forbs: Removal of graminoids and legumes; Graminoids: Removal of legumes and forbs; Legumes: Removal of graminoids and forbs; None: Removal of all. Same below. 
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表 2 不同植物功能群移除下土壤理化性质
Table 2 Soil properties under removal of different plant functional groups
指标Index CK Forbs Graminoids Legumes None 土壤含水率 / % 54.72 ± 2.18a 55.10 ± 5.30a 54.91 ± 3.92a 50.80 ± 5.10a 51.86 ± 4.87a 总碳 / g/kg 65.05 ± 3.50a 67.44 ± 5.89a 60.38 ± 4.65a 64.97 ± 6.68a 61.19 ± 5.66a 总氮 / g/kg 5.85 ± 0.25a 6.08 ± 0.45a 5.53 ± 0.36a 5.82 ± 0.48a 5.56 ± 0.43a 碳氮比 11.09 ± 0.14a 11.06 ± 0.16a 10.89 ± 0.19a 11.09 ± 0.24a 10.96 ± 0.18a 土壤有机碳 / g/kg 67.72 ± 3.34a 67.15 ± 5.43a 60.60 ± 4.97a 63.01 ± 5.60a 62.43 ± 5.92a 可溶性有机碳 / mg/kg 309.4 ± 19.8a 309.1 ± 25.4a 263.9 ± 15.0a 286.2 ± 14.5a 269.3 ± 11.3a 铵态氮 / mg/kg 8.79 ± 1.16a 9.33 ± 0.45a 9.80 ± 1.88a 8.45 ± 1.58a 9.55 ± 1.23a 硝态氮 / mg/kg 6.10 ± 0.94a 5.22 ± 0.68a 4.76 ± 0.32a 4.14 ± 0.60a 6.62 ± 0.99a
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表 3 不同植物功能群移除下门水平土壤真菌相对丰度 / %
Table 3 Relative abundance of soil fungi at the phylum level under removal of different plant functional groups / %
门Phylum CK Forbs Graminoids Legumes None 子囊菌门 55.49 ± 5.04a 51.01 ± 4.37a 55.78 ± 6.89a 55.97 ± 3.79a 56.97 ± 4.11a 被孢霉门 22.98 ± 2.07a 21.58 ± 1.88a 19.53 ± 2.27a 20.97 ± 1.83a 23.17 ± 3.61a 担子菌门 18.67 ± 5.55a 24.84 ± 4.32a 20.27 ± 6.52a 18.51 ± 4.59a 16.38 ± 4.66a 壶菌门 0.39 ± 0.06a 0.24 ± 0.06a 1.54 ± 0.52a 1.35 ± 0.69a 0.78 ± 0.26a 根肿黑粉菌门 0.53 ± 0.28a 0.65 ± 0.23a 0.83 ± 0.40a 1.27 ± 0.37a 0.43 ± 0.07a 罗兹菌门 0.16 ± 0.06a 0.18 ± 0.01a 0.28 ± 0.14a 0.30 ± 0.04a 0.27 ± 0.06a 球囊菌门 0.05 ± 0.02b 0.19 ± 0.04a 0.17 ± 0.02ab 0.18 ± 0.05a 0.11 ± 0.02ab 油壶菌门 0.15 ± 0.05a 0.08 ± 0.02a 0.08 ± 0.02a 0.06 ± 0.01a 0.12 ± 0.02a 毛霉门 0.06 ± 0.01a 0.03 ± 0.01a 0.03 ± 0.01a 0.10 ± 0.04a 0.02 ± 0.00a 捕虫霉门 0.01 ± 0.00b 0.01 ± 0.00b 0.01 ± 0.00b 0.03 ± 0.01a 0.01 ± 0.00b
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表 4 不同植物功能群移除下土壤真菌多样性
Table 4 Soil fungal diversity under removal of different plant functional groups
指数Index CK Forbs Graminoids Legumes None OTUs 585.2 ± 47.2a 633 ± 39.7a 664.8 ± 7.2a 660 ± 11.7a 671.6 ± 6.1a H 4.19 ± 0.20a 4.13 ± 0.11a 4.10 ± 0.12a 4.18 ± 0.10a 4.26 ± 0.07a Pielou 0.66 ± 0.03a 0.64 ± 0.01a 0.63 ± 0.02a 0.64 ± 0.01a 0.66 ± 0.01a D 0.96 ± 0.01a 0.95 ± 0.01a 0.94 ± 0.01a 0.95 ± 0.01a 0.95 ± 0.01a Chao1 617.57 ± 45.20a 672.76 ± 34.79a 699.08 ± 9.69a 698.73 ± 8.42a 699.74 ± 3.97a Ace 613.88 ± 44.54a 661.72 ± 37.37a 697.51 ± 8.34a 693.77 ± 8.52a 696.92 ± 4.74a 注：OTUs，操作分类单位；Ace，样本中物种组成的丰富度和均匀度；Chao1，描述样品中所含OTUs数目的指数；D，辛普森指数；Pielou，均匀度指数； H，香农指数。 Notes: OTUs, operational taxonomic units; Ace index, species composition richness and evenness in a sample; Chao1 index, number of OTUs in a sample; D, Simpson index; Pielou, Pielou’s evenness index; H, Shannon-Wiener index.
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表 5 不同植物功能群移除下土壤真菌功能类群相对丰度 / %
Table 5 Relative abundance of soil fungal functional groups under removal of different plant functional groups / %
功能类群 Functional group CK Forbs Graminoids Legumes None 动物寄生真菌/病原菌 6.75 ± 3.09a 7.97 ± 3.28a 3.19 ± 0.46a 3.48 ± 0.60a 5.73 ± 2.23a 丛枝菌根真菌 0.10 ± 0.03b 0.31 ± 0.07ab 0.32 ± 0.03a 0.33 ± 0.09a 0.22 ± 0.04ab 粪腐生真菌 7.25 ± 1.12a 3.11 ± 1.38a 4.19 ± 1.38a 5.32 ± 4.02a 4.26 ± 0.61a 外生菌根真菌 6.75 ± 5.17a 0.10 ± 0.03a 0.12 ± 0.05a 0.13 ± 0.03a 0.23 ± 0.13a 内生真菌 0.36 ± 0.06a 0.49 ± 0.21a 0.42 ± 0.07a 0.39 ± 0.08a 0.78 ± 0.11a 真菌寄生菌 1.61 ± 0.62a 0.44 ± 0.05a 0.99 ± 0.25a 0.92 ± 0.39a 1.15 ± 0.45a 叶腐生菌 5.15 ± 0.67a 3.44 ± 0.42a 9.50 ± 3.62a 5.72 ± 1.83a 7.00 ± 1.15a 地衣寄生菌/腐生菌 1.15 ± 0.40ab 1.53 ± 0.49a 0.47 ± 0.10ab 0.81 ± 0.24ab 0.28 ± 0.06b 兰花菌根真菌 0.08 ± 0.04a 0.09 ± 0.05a 0.22 ± 0.07a 0.17 ± 0.09a 0.10 ± 0.06a 植物病原菌/腐生菌 8.15 ± 2.10a 5.24 ± 0.48a 5.87 ± 0.74a 9.37 ± 1.65a 8.76 ± 1.80a 土壤腐生菌 35.64 ± 2.13a 36.85 ± 4.02a 44.49 ± 5.56a 41.82 ± 5.81a 37.26 ± 4.39a 木质腐生菌 2.34 ± 0.23a 2.30 ± 0.27a 3.33 ± 0.80a 3.53 ± 0.69a 3.81 ± 0.69a 未定义腐生菌 24.67 ± 4.47a 38.14 ± 5.48a 26.90 ± 8.90a 28.01 ± 5.38a 30.42 ± 6.67a
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