Influences of continuous monoculture of alfalfa and rotation of annual crops on soil fungal communities in the semi-arid Loess Plateau
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摘要: 为研究半干旱区种植制度对土壤真菌群落和功能的影响, 本研究依托布设于黄土高原雨养农业区的长期定位试验, 采集长期种植苜蓿(LC)、苜蓿-休耕(LF)、苜蓿-休耕-玉米(LFC)、苜蓿-马铃薯(LP)、苜蓿-谷子(LMi)5个处理的耕层(0~30 cm)土壤样品, 基于真菌ITS区高通量测序技术, 分析比较长期种植苜蓿和一年生作物对土壤真菌多样性和群落特征的影响, 并采用FUNGuild平台分析预测不同处理土壤真菌的生态功能。结果表明, 本研究共检测到真菌7门25纲77目169科347属, 其中以子囊菌门(Ascomycota, 69.17%~88.22%)为最优势菌门, 且远远大于次优势菌门——接合菌门(Zygomycota, 6.72%~19.88%)和担子菌门(Basidiomycota, 1.64%~9.01%); 属水平下各处理优势菌群存在差异, 其中LC处理优势属为Phaeomycocentrospora, LF、LP和LMi的优势属均为赤霉菌属(Gibberella), LFC处理优势属为被孢霉属(Mortierella)。冗余分析(RDA)发现, 土壤有效磷(P=0.002)是影响土壤真菌群落结构的主要环境因子。真菌FUNGuild功能预测结果表明, 本试验黄绵土主要以病理营养型真菌(pathotroph)为主(25.44%~39.27%), 速效磷和硝态氮是影响土壤真菌营养类型变化的主要环境因子, 与长期种植苜蓿相比种植一年生大田作物显著增加了土壤腐生-共生营养型、病原体-腐生-共生营养型和病理-腐生-共生营养型等过渡型真菌类群相对丰度, 说明合理的种植制度有利于改善农田土壤真菌群落结构, 促进区域土壤生态系统的稳定。Abstract: Lucerne (Medicago sativa) is widely planted in the Loess Plateau of western China and can accumulate soil carbon and nitrogen nutrients. However, continuous cropping of lucerne has consumed soil water and phosphorus for many years leading to a decrease in soil quality and alfalfa productivity. Therefore, after lucerne is planted for a certain period, it is necessary to plant the stubble and rotate annual crops to promote sustainable land use. Choosing suitable crops can improve the stability of the soil ecosystem. In this study, we analyzed the effects of long-term continuous cropping of alfalfa and rotation with annual crops on the structure and diversity of soil fungal communities in semi-arid areas based on a long-term localization experiment in the rainfed agricultural area of the Loess Plateau using the FUNGuild platform to predict the ecological functions of fungi in different treatments. The cropping systems included monocropping for 16 years of lucerne (LC), field fallow for 7 years after monocropping for 9 years of lucerne (rotation of lucerne-fallow, LF), field fallow for 2 years after monocropping for 9 years of lucerne and then planting corn (Zea mays) for 5 years (rotation of lucerne-fallow-corn, LFC), planting potato (Solanum tuberosum) for 7 years after monocropping for 9 years of lucerne (rotation of lucerne-potato, LP), and planting millet (Panicum miliaceum) for 7 years after monocropping for 9 years of lucerne (rotation of lucerne-millet, LMi). A total of 7 phyla, 25 classes, 77 orders, 169 families, and 347 genera of fungi were identified. The fungi were mainly Ascomycota, Zygomycota, and Basidiomycota at the phylum level. Ascomycota was the first dominant phylum in different treatments, and its relative abundance ranged from 69.17% to 88.22%, which was much greater than that of the subdominant phyla Zygomycota (6.72%–19.88%) and Basidiomycota (1.64%–9.01%). The dominant genera varied in different treatments, with Phaeomycocentrospora in LC treatment, Gibberella in LF, LP, and LMi treatments, and Mortierella in LFC treatment. Redundancy analysis revealed that soil available phosphorus (P=0.002) was the main factor influencing the soil fungal community structure. The alpha diversity results showed that crop type had no significant impact on the diversity and richness of the soil fungal communities. However, the Shannon index was significantly negatively correlated with the soil nitrate-nitrogen content (r=−0.553, P<0.05) and the Simpson index was significantly positively correlated with the soil nitrate-nitrogen content (r=0.515, P<0.05). Functional prediction with FUNGuild showed that pathotrophs (25.44%–39.27%) was the dominant fungal functional group of loessal soil in this study. After lucerne rotation with annual crops, the relative abundance of transitional fungal groups, such as soil saprotrophs-symbiotrophs, pathogens-saprotrophs-symbiotrophs, and pathotrophs-saprotrophs-symbiotrophs, changed, whereas the relative abundance of pathotrophs-saprotrophs decreased. Available phosphorus (P=0.002) and nitrate-nitrogen (P=0.02) were the main environmental factors affecting the changes in soil fungal functional groups. In conclusion, rational cropping systems are conducive in enriching the structure of soil microbial communities and promoting the stability of the soil ecosystems in the region. The results of this study can provide reference and data support for the prediction of soil fungal communities and their functions in different planting systems.
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Key words:
- Medicago sativa /
- Annual crops /
- High throughput sequencing /
- Fungal community structure /
- FUNGulid
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图 1 不同种植制度土壤真菌群落Alpha多样性
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。
Figure 1. Alpha diversity of soil fungal communities in different cropping systems
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively.
图 2 不同种植制度土壤真菌群落PCoA分析
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。
Figure 2. PCoA analysis of soil fungal communities in different cropping systems
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively.
图 3 不同种植制度土壤真菌门水平相对丰度
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。*表示不同处理间差异显著(P<0.05)。
Figure 3. Relative abundances of soil fungal communities at phylum levels in different cropping systems
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively. * means significant differences among treatments (P<0.05).
图 4 不同种植制度土壤真菌属水平相对丰度
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。
Figure 4. Relative abundance of soil fungal communities at the level of genus in different cropping systems
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively.
图 5 土壤真菌属与理化因子RDA分析
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。Gibberella: 赤霉菌属; Mortierella: 被孢霉属; Metarhizium: 绿僵菌属; Fusarium: 镰刀菌属; Humicola: 腐质霉属; Cryptococcus: 隐球菌属; Mycosphaerella: 球腔菌属; Beauveria: 白僵菌属; BD: 容重; SOC: 有机碳: TN: 全氮; NO3−-N: 硝态氮; AP: 有效磷; AK: 速效钾。
Figure 5. RDA analysis of soil fungi genus and physicochemical factors
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively. BD, SOC, TN, NO3−-N, AP and AK represent soil bulk density, organic carbon, total nitrogen, nitrate nitrogen, available phosphorus and available potassium, respectively.
图 6 不同种植制度土壤真菌营养型及相对丰度
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。*表示不同处理间差异显著(P<0.05)。
Figure 6. Relative abundance of soil fungal nutrient types in different cropping systems
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respetively. * means significant differences among treatments (P<0.05).
图 7 土壤真菌功能类群与理化因子RDA分析
LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。图中红色箭头代表土壤环境因子, 蓝色箭头代表土壤真菌营养类型; BD、SOC、TN、NO3−-N、AP和AK分别代表土壤容重、有机碳、全氮、硝态氮、有效磷和速效钾; Saprotroph: 腐生营养型; Symbiotroph: 共生营养型; Pathotroph: 病理营养型; Pathotroph-Saprotroph: 病理-腐生营养型; Pathotroph-Symbiotroph: 病理-共生营养型; Saprotroph-Symbiotroph: 腐生-共生营养型; Pathogen-Saprotroph-Symbiotroph: 病原体-腐生-共生营养型; Pathotroph-Saprotroph-Symbiotroph: 病理-腐生-共生营养型。
Figure 7. RDA analysis of soil fungal functional groups and physicochemical factors
LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively. The red arrow in the figure represents soil physicochemical factors and the blue arrows represent soil fungal functional groups. BD, SOC, TN, NO3−-N, AP and AK represent soil bulk density, organic carbon, total nitrogen, nitrate nitrogen, available phosphorus and available potassium.
表 1 试验处理
Table 1. Experimental treatment
处理
Treatment代码
Treatment code田间操作管理
Field operation and management紫花苜蓿连作
Lucerne continuous cropingLC 于2003年建植紫花苜蓿, 并连续种植至2018年Lucerne established in 2003 and continuously cropped to 2018 紫花苜蓿-休耕
Rotation of lucerne-fallowLF 于2003年建植紫花苜蓿, 2012年3月挖除紫花苜蓿后一直保持休耕Lucerne established in 2003 and removed in March 2012, field fallowed until 2018 紫花苜蓿-休耕-玉米
Rotation of lucerne-fallow-cornLFC 于2003年建植紫花苜蓿, 2012年3月挖除紫花苜蓿后保持休耕, 之后于次年春季种植玉米, 2014—2018年种植玉米Lucerne was established in 2003 and removed in March 2012, field fallowed until maize was sown in the spring of 2013, and maize was continuously cropped in 2014−2018 紫花苜蓿-马铃薯
Rotation of lucerne-potatoLP 于2003年建植紫花苜蓿, 2012年3月挖除紫花苜蓿, 并于当年5月种植马铃薯, 2013—2018年种植马铃薯Lucerne was established in 2003 and removed in March 2012, potato was sown in May 2012 and continuously cropped in 2013−2018 紫花苜蓿-谷子
Rotation of lucerne-milletLMi 于2003年建植紫花苜蓿, 2012年3月挖除紫花苜蓿, 并于当年4月种植谷子, 2013−2018年种植谷子Lucerne was established in 2003 and removed in March 2012, millet was sown in April 2012 and continuously cropped in 2013−2018 
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表 2 不同种植制度的土壤理化性质
Table 2. Soil physicochemical properties of different cropping systems
处理
Treatment容重Bulk density
(g·cm−3)有机碳Organic carbon
(g·kg−1)全氮Total nitrogen
(g·kg−1)硝态氮Nitrate nitrogen
(mg·kg−1)有效磷Available phosphorus
(mg·kg−1)速效钾Available potassium
(mg·kg−1)pH LC 1.31±0.01a 9.40±0.14a 1.04±0.07a 12.97±0.72b 0.98±0.16d 200.77±20.01b 8.45±0.05a LF 1.27±0.02a 8.34±0.17c 0.91±0.01b 20.72±0.75b 5.54±0.01c 241.91±11.93a 8.32±0.08a LFC 1.25±0.02a 8.95±0.13b 0.94±0.01ab 39.17±4.16a 9.50±0.82b 223.67±0.53ab 8.27±0.06a LP 1.20±0.04a 8.97±0.04b 1.04±0.03a 37.36±3.54a 4.15±0.48c 206.91±0.71ab 8.28±0.07a LMi 1.23±0.03a 9.27±0.06ab 1.01±0.01ab 31.92±0.65a 11.33±0.53a 187.34±8.00b 8.33±0.04a LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。表中数值表示均值±标准误(n=3), 同列不同小写字母表示处理间差异显著(P<0.05)。LC, LF, LFC, LP and LMi indicate lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively. Values in the table are mean ± SD (n=3). Different lowercase letters represent significant differences among treatments (P<0.05).
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表 3 不同种植制度土壤相对丰度前10的真菌属
Table 3. Top 10 genera of relative abundance of soil fungi in different cropping systems
真菌属
Fungal genus相对丰度 Relative abundance (%) LC LF LFC LP LMi 赤霉菌属 Gibberella 7.23±2.47c 19.95±4.55ab 6.20±2.26c 14.18±0.80bc 27.80±4.17a 被孢霉属 Mortierella 6.68±0.27b 13.17±1.25ab 19.73±4.27a 10.05±0.89b 7.83±1.68b 绿僵菌属 Metarhizium 5.17±3.80a 4.66±1.88a 13.64±6.75a 4.15±0.26a 8.36±2.10a 镰刀菌属 Fusarium 3.16±0.56a 2.41±0.31a 3.76±0.28a 2.13±0.16a 9.77±5.79a Phaeomycocentrospora 9.44±3.03a 2.97±2.41b 0.70±0.58b 2.10±1.75b 0.73±0.32b Lectera 4.01±1.38b 2.23±0.58ab 0.13±0.11c 7.66±1.43a 0.61±0.38c 腐质霉属 Humicola 0.64±0.18a 0.83±0.21a 11.59±6.73a 0.72±0.05a 0.42±0.14a 隐球菌属 Cryptococcus 1.84±0.38a 4.35±0.83a 3.86±1.17a 1.71±0.52a 1.85±0.34a 球腔菌属 Mycosphaerella 1.31±0.45a 9.35±7.68a 0.06±0.02a 0.19±0.03a 0.23±0.05a 白僵菌属 Beauveria 6.17±2.39a 0.12±0.03a 4.11±3.92a 0.18±0.06a 0.07±0.01a LC、LF、LFC、LP和LMi分别表示紫花苜蓿连作、紫花苜蓿-休耕、紫花苜蓿-休耕-玉米、紫花苜蓿-马铃薯、紫花苜蓿-谷子。表中数值表示均值±标准误(n=3), 同行不同小写字母代表处理间具有显著性差异(P<0.05)。LC, LF, LFC, LP and LMi indicate the treatments of lucerne continuous cropping, rotation of lucerne-fallow, rotation of lucerne-fallow-corn, rotation of lucerne-potato, and rotation of lucerne-millet, respectively. Values in the table are mean ± SD (n=3). Different lowercase letters in the same line represent significant differences among treatments (P<0.05).
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表 4 土壤真菌Alpha多样性与理化因子Pearson相关分析
Table 4. Pearson correlation analysis between alpha diversity of soil fungi and physiochemical factors
多样性指数
Diversity index容重
Bulk density有机碳
Organic carbon全氮
Total nitrogen硝态氮
Nitrate nitrogen有效磷
Available phosphorus速效钾
Available potassiumpH Sobs 指数 Sobs index −0.048 0.143 −0.097 −0.134 −0.188 −0.066 0.459 Chao1 指数 Chao1 index −0.360 0.187 0.054 0.045 0.128 −0.314 0.276 Shannon 指数 Shannon index 0.275 0.082 −0.014 −0.553* −0.434 −0.040 0.481 Simpson 指数 Simpson index −0.220 −0.103 −0.129 0.515* 0.466 0.148 −0.393 *和**分别表示相关性为显著(P<0.05)和极显著(P<0.01)。* and ** mean significant correlations at P<0.05 and P<0.01, respectively.
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