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Journal of Arid Land
Journal of Arid Land  2022, Vol. 14 Issue (5): 561-575    DOI: 10.1007/s40333-022-0064-2     CSTR: 32276.14.s40333-022-0064-2
Research article     
Changes in diversity, composition and assembly processes of soil microbial communities during Robinia pseudoacacia L. restoration on the Loess Plateau, China
WANG Kun1, WANG Xiaoxia1, FEI Hongyan1, WAN Chuanyu1, HAN Fengpeng1,2,*()
1State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, College of Natural Resources and Environment, Northwest A & F University, Yangling 712100, China
2Research Center on Soil & Water Conservation, Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling 712100, China
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Abstract  

Robinia pseudoacacia L. (RP) restoration has increased vegetation cover in semi-arid regions on the Loess Plateau of China, but ecological problems have also occurred due to RP restoration, such as reduced soil moisture. Further, it is still uncertain how microbial diversity, composition and assembly processes change with RP restoration in semi-arid regions. Therefore, amplicon sequencing of small subunit ribosomal ribonucleic acid (16S rRNA) and internal transcribed spacer (ITS) genes was performed to study soil bacterial and fungal diversity, composition and assembly processes at four study sites with different stand ages of RP plantations (Y10, RP plantation with stand ages less than 10 a; Y15, RP plantation with stand ages approximately 15 a; Y25, RP plantation with stand ages approximately 25 a; and Y40, RP plantation with stand ages approximately 40 a) along a 40-a chronosequence on the Loess Plateau. The diversity of soil bacteria and fungi increased significantly during the restoration period from 10 to 15 a (P<0.05). However, compared with Y15, bacterial diversity was lower at Y25 and Y40, and fungal diversity remained stable during the restoration period between 25 and 40 a. The relative abundances of Proteobacteria and Ascomycota increased during the restoration period from 10 to 15 a. Conversely, after 15 a of restoration, they both decreased, whereas the relative abundances of Actinomycetes, Acidobacteria and Basidiomycota gradually increased. The variations in soil bacterial communities were mainly related to changes in soil total nitrogen, nitrate nitrogen and moisture contents, while soil fungal communities were mainly shaped by soil organic carbon and nitrate nitrogen contents. Bacterial communities were structured by the heterogeneous selection and stochastic process, while fungal communities were structured primarily by the stochastic process. The RP restoration induced an increase in the relative importance of heterogeneous selection on bacterial communities. Overall, this study reveals the changes in microbial diversity, community composition and assembly processes with RP restoration on the Loess Plateau and provides a new perspective on the effects of vegetation restoration on soil microbial communities in semi-arid regions.

Key words： Robinia pseudoacacia      microbial diversity      community structure      community assembly      restoration      semi-arid regions     
Received: 27 December 2021      Published: 31 May 2022
Corresponding Authors: *: HAN Fengpeng (E-mail: hanxiangzi007@163.com)
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WANG Kun, WANG Xiaoxia, FEI Hongyan, WAN Chuanyu, HAN Fengpeng. Changes in diversity, composition and assembly processes of soil microbial communities during Robinia pseudoacacia L. restoration on the Loess Plateau, China. Journal of Arid Land, 2022, 14(5): 561-575.

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http://jal.xjegi.com/10.1007/s40333-022-0064-2     OR     http://jal.xjegi.com/Y2022/V14/I5/561

Soil property RP plantation
Y10 Y15 Y25 Y40
pH 8.76±0.05a 8.59±0.13b 8.53±0.09bc 8.48±0.12c
SM (%) 10.79±0.55b 14.20±0.99a 9.65±0.34c 9.57±0.46c
SOC (mg/g) 5.94±0.42d 6.89±0.21c 13.86±0.31b 15.89±0.67a
TN (mg/g) 0.66±0.05d 0.76±0.03c 1.49±0.04b 1.66±0.06a
NO3--N (μg/g) 1.95±0.15a 1.79±0.31a 1.12±0.34b 1.60±0.77ab
NH4+-N (μg/g) 0.46±0.04c 0.40±0.05c 0.71±0.15b 0.92±0.09a
AP (μg/g) 2.64±0.47c 1.90±0.36c 3.94±1.17b 5.09±0.75a
Table 1 Soil properties of Robinia pseudoacacia (RP) plantations with different stand ages
Fig. 1 Diversity indices of soil bacterial and fungal communities at four Robinia pseudoacacia (RP) plantations with different stand ages.
(a), Shannon index of bacterial communities; (b) Chao index of bacterial communities; (c) Shannon index of fungal communities; (d) Chao index of fungal communities. Y10, Y15, Y25 and Y40 indicate RP plantations with stand ages of 10, 15, 25 and 40 a, respectively. Different lowercase letters indicate significant differences (P<0.05) among RP plantations with different stand ages. The box plot conveys the distribution of data values, including the median, the approximate quartiles, and the lowest and highest data (Williamson et al., 1989). The points in the box plot represent outliers.
Fig. 2 Relative abundance of dominant bacteria
(a) and fungi (b) at the phylum level at four RP plantations with different stand ages. The relative abundance level less than 1% and undefined phyla were defined as "Others". The error bars within the different colour blocks represent the standard variance of the species relative abundance (n=5).
Fig. 3 Dissimilarities of soil microbial communities and the relationships between soil microbial communities and soil properties at four RP plantations with different stand ages.
(a), principal coordinate analysis (PCoA) based on the bacterial community Bray-Curtis dissimilarities between samples; (b), PCoA based on the fungal community Bray-Curtis dissimilarities between samples; (c), redundancy analysis (RDA) between bacterial communities and soil properties; (d), RDA between bacterial communities and soil properties. SM, soil moisture; SOC, soil organic carbon; TN, total nitrogen; NO3--N, nitrate nitrogen; NH4+-N, ammonium nitrogen; AP, available phosphorous.
Fig. 4 Distribution of the microbial beta nearest taxon index (βNTI) at four RP plantations with different stand ages. The box plot conveys the distribution of βNTI values, including the median, the approximate quartiles, and the lowest and highest of values (Williamson et al., 1989). In addition, βNTI values for all samples (points in box plot) are shown. An absolute value of βNTI larger than 2 (|βNIT|>2) indicates that deterministic process strongly drives the microbial community assembly, while the microbial community assembly is considered to result from stochastic process if |βNTI|<2.
RP plantation Location Altitude (m) ATH (m) Slope
gradient (°)		 DBH
(cm)		 Trees density (numbers/hm2) Litter biomass (g/m2)
Y10 109°28′E, 36°27′N 1276.4 6.92±0.24 20 6.40±0.42 1600 190.05±7.92
Y15 109°33′E, 36°27′N 1338.1 7.33±0.15 18 7.00±0.34 2800 418.39±11.58
Y25 109°29′E, 36°24′N 1351.6 9.87±1.21 16 15.30±1.27 1500 505.61±12.34
Y40 110°22′E, 38°47′N 1342.4 10.72±0.69 18 17.30±1.56 1300 556.88±17.60
Table S1 Geographical characteristics of Robinia pseudoacacia L. (RP) plantations with different stand ages
Soil property Bacterial α diversity Fungal α diversity
Shannon Chao Shannon Chao
pH 0.435 -0.016 -0.823** -0.858**
Moisture 0.728** 0.556* -0.233 -0.201
SOC -0.754** -0.269 0.762** 0.846**
TN -0.760** -0.255 0.765** 0.852**
NO3--N 0.516 -0.084 -0.255 -0.256
NH4+-N -0.640** -0.265 0.630** 0.698**
AP -0.658** -0.382 0.518* 0.545*
C:N -0.421 -0.378 0.330 0.379
Table S2 Relationships between soil properties and microbial α diversity indices
df Sums of square Mean of square F P
Group factor 1 0.682 0.682 8.429 0.011
Residual 8 0.647 0.081
Total 9 1.330
Table S3 Significance tests of the variations of fungal communities between Y10 and Y15 using the Adonis test
Microbe Soil property Explanation (%) Contribution (%) F P
Bacteria TN# 21.5 39.2 4.9 0.002
NO3--N# 10.0 18.2 2.5 0.002
SM# 9.1 16.6 2.5 0.002
pH 4.0 7.3 1.1 0.346
SOC 3.8 6.9 1.0 0.408
AP 3.3 6.1 0.9 0.654
NH4+-N 3.1 5.7 0.8 0.718
Fungi SOC# 28.9 43.2 7.3 0.002
NO3--N# 17.6 18.8 3.7 0.002
SM 5.1 7.2 1.8 0.059
pH 4.4 6.6 1.5 0.078
TN 5.8 8.6 2.1 0.014
AP 2.7 4.0 1.0 0.462
NH4+-N 2.4 3.6 0.9 0.632
Table S4 Forward selection results of the redundancy analysis (RDA) for microbial communities and soil properties
Fig. S1 Principal component analysis (PCA) of soil properties at four Robinia pseudoacacia (RP) plantations with different stand ages. PCA and visualization were performed using CANOCO v5.0. SM, soil moisture; SOC, soil organic carbon; TN, total nitrogen; NO3--N, nitrate nitrogen; NH4+-N, ammonium nitrogen; AP, available phosphorous.
Fig. S2 Venn analyses of the operational taxonomic units (OTUs) of soil bacterial (a) and fungal (b) communities at four RP plantations with different stand ages. Venn analyses and visualization were performed using the ''VennDiagram'' package in R 3.4.1.
Fig. S3 Time-decay relationships of fungal and bacterial communities at RP plantations with 40 a of restoration. The slope means the temporal turnover rate of microbial communities across restoration time.
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