Population turnover promotes fungal stability in a semi-arid grassland under precipitation shifts

doi:10.1093/jpe/rtaa038

J Plant Ecol ›› 2020, Vol. 13 ›› Issue (4): 499-509 .DOI: 10.1093/jpe/rtaa038

• Research Articles • Previous Articles

Population turnover promotes fungal stability in a semi-arid grassland under precipitation shifts

Nannan Wang^1,2,3 , Lei Li^1,3 , Bingwei Zhang⁴, , Shiping Chen¹ , Wei Sun⁵ , Yukun Luo⁶ , Kuanhu Dong⁶ , Xingguo Han^1,3 , Jianhui Huang^1,3,
*, Xiaofeng Xu² and Changhui Wang^1,
*

¹ State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China,²Biology Department, San Diego State University, San Diego, CA 92182, USA, ³ University of Chinese Academy of Sciences, Beijing 100049, China,⁴ Department of Ecology, State Key Laboratory of Biocontrol and School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China, ⁵ Key Laboratory of Vegetation Ecology, Ministry of Education, Institute of Grassland Science, Northeast Normal University, Changchun, Jilin 130024, China,⁶ College of Grassland Science, Shanxi Agricultural University, Taigu, Shanxi 030801, China

^*Corresponding author. E-mail: jhhuang@ibcas.ac.cn (J.H.); E-mail: wangch@ibcas.ac.cn (C.W.)

Received:2020-02-07 Revised:2020-05-31 Accepted:2020-07-16 Online:2020-07-14 Published:2020-08-01

Abstract

Abstract:

Aims

Bacteria and fungi are two primary groups of soil microbes, and their stability determines the persistence of microbial functions in response to a changing environment. Recent studies reported higher fungal than bacterial stability under precipitation alteration, the underlying mechanisms, however, remain elusive.

Methods

A 3-year precipitation manipulation experiment in a semi-arid grassland was used to compare the bacterial and fungal diversities, including alpha diversity, beta diversity and microbial community composition turnover, in response to precipitation manipulations. A framework is proposed to understand the stability properties of bacteria and fungi under precipitation alteration. We conceived a diagrammatic valley to illustrate microbial stability with the depth representing resistance and the width ecological resilience.

Important Findings

We found that ±60% in precipitation significantly reduced the richness and increased the evenness of bacteria but had trivial impacts on fungi. Precipitation alteration yielded stronger impacts on the variation in alpha diversity of bacteria than fungi, suggesting that the bacterial community is more sensitive to water stress than the fungal community. Moreover, fungi had wider composition turnover than that of bacteria, indicating higher composition variation of fungi than bacteria. The population turnover of fungi, reflected by composition variation, coefficient variation of diversity index and composition turnover, was larger than that of bacteria at both temporal and spatial scales, indicating the population turnover promotes fungal stability. The higher stability of fungal community in tolerating water stress is analogous to a ball in a wide valley that swing substantially but remain close to its steady state; while the lower stability of bacteria community is analogous to a ball that swings slightly but stay far away from its steady state. Our finding that the fungal community had higher stability than bacterial community in a semi-arid grassland might be applicable to other biomes.

Key words: bacteria, diversity, fungi, resistance, ecological resilience

摘要：
土壤中细菌和真菌的稳定性在维持土壤生态系统功能方面起着重要作用，环境条件的改变直接影响细菌和真菌的组成与结构。已有研究表明，土壤真菌群落稳定性对降水变化响应的敏感性比细菌低,但其内在机制还不清楚。在内蒙古典型草原建立3年的增减降雨实验平台，设置5个降水梯度，包括分别增加和减少30%和60%的降水量以及对照，比较控制不同的降水水平对土壤细菌和真菌多样性的影响，包括α多样性，β多样性和细菌/真菌群落组成的变化。本研究开发了一个概念模型来反映不同降水条件下土壤细菌和真菌的稳定性特征，其中模型山谷的深度表示微生物抵抗力(Resistance)，谷的宽度代表生态弹性(Ecological Resilience)。结果表明，增加和减少60%的降水量均显著降低了细菌的丰富度，同时显著增加了细菌均匀度，但对真菌的丰富度和均匀度没有显著的影响。降水对细菌α多样性的影响高于真菌，说明细菌对水分胁迫的敏感性大于真菌。而真菌群落的周转比细菌快，包括组成变化(Composition Variation)，多样性指数和变异系数(Coefficient Variation)，反映了真菌群落具有较高的群落可变性,使得降水变化对真菌群落的影响较小。概念模型中两种相反的情景表示细菌和真菌对降水变化不同的响应模式：真菌群落对水分胁迫响应不敏感，可以用宽谷中的一个球来表示，球虽然在较大范围内往复摆动，但仍接近稳定状态；而细菌群落对水分响应敏感，即稳定性低，可以表示为一个球在较窄的谷里远离平衡态的位置摆动。基于本研究结果，半干旱草原真菌群落比细菌群落具有更高的稳定性,该结论对于量化群落稳定性特征具有重要意义。

关键词: 细菌, 多样性, 真菌, 抵抗力, 生态恢复力

Nannan Wang, Lei Li, Bingwei Zhang, Shiping Chen, Wei Sun, Yukun Luo, Kuanhu Dong, Xingguo Han, Jianhui Huang, Xiaofeng Xu and Changhui Wang. Population turnover promotes fungal stability in a semi-arid grassland under precipitation shifts[J]. J Plant Ecol, 2020, 13(4): 499-509.

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Population turnover promotes fungal stability in a semi-arid grassland under precipitation shifts

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