Elsevier

Applied Soil Ecology

Volume 169, January 2022, 104222
Applied Soil Ecology

Rhizosphere soil metabolites mediated microbial community changes of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert

https://doi.org/10.1016/j.apsoil.2021.104222Get rights and content

Highlights

  • Pinus sylvestris var. mongolica can release rhizosphere metabolites with certain ecological functions.

  • Fatty acids, monoacylglycerides, and diterpenes significantly affected the rhizosphere microbial diversity.

  • The bioactive metabolites were the primary driving factors in the variation of the rhizosphere microbial community.

Abstract

Soil metabolites strongly affect microbial community structure and function. Yet the response of soil microbial communities to plant rhizosphere metabolism and their interaction mechanism is poorly understood. In this study, we aimed to explore the influence of Pinus sylvestris var. mongolica (P. sylvestris) rhizosphere metabolites on microbial diversity, and clarify the dominant factors driving the variation in the rhizosphere microbial community along chronosequence. Gas chromatography–mass spectrometry (GC–MS) and high-throughput sequencing were used to determine the rhizosphere metabolites and microbial community composition, respectively. The results showed that P. sylvestris can release a variety of rhizosphere metabolites (such as fatty acids, monoacylglycerides, and diterpenes) with certain ecological functions, and these metabolites significantly affected the rhizosphere microbial alpha diversity and community composition. Simultaneously, the edaphic factors, such as pH, soil moisture, organic carbon, total phosphorus, NO3-N, NH4+-N, and available phosphorus concentrations, also significantly affected the rhizosphere microbial community. However, partial Mantel test and variation partitioning analysis confirmed the rhizosphere metabolites had a stronger relationship with the variation of rhizosphere bacterial and fungal communities than edaphic factors. Overall, our study highlights the regulatory role of the rhizosphere metabolites of P. sylvestris in shaping microbial community, and provides an insight into the rhizosphere microecological during vegetation restoration process in the Mu Us Desert.

Introduction

Rhizosphere soil metabolites include root exudates and small molecules produced by the metabolism of rhizosphere soil microorganisms (Hu et al., 2018). Due to the production of root exudates, a special microdomain called the “rhizosphere” is formed within a few millimeters of the root system, which is a special microecological environment different from the bulk soil (Chaparro et al., 2014). Rhizosphere metabolites play an important role in the process of plant-microbe interaction. Among rhizosphere metabolites, sugars, amino acids, and vitamins provide nutrition for the growth and reproduction of rhizosphere microorganisms (Badri and Vivanco, 2009). Certain bioactive metabolites may affect the rhizosphere microbial community structure. Hu et al. (2018) reported that some defensive secondary metabolites such as benzoxazinoids in the rhizosphere of wheat and maize altered the rhizosphere bacterial and fungal community composition. Huang et al. (2014) pointed out that some specific rhizosphere metabolites can directly promote or inhibit pathogenic microorganisms. In general, the effects of metabolites on rhizosphere microorganisms are loose and non-specific (Shen et al., 2020).

Soil microbial communities maintain multiple ecosystem functions in terrestrial ecosystems (Goldfarb et al., 2011). At present, the differences in microbial community diversity at the regional scale with climate condition, vegetation type, and soil texture, and the impact of natural vegetation restoration on soil microbial communities have been widely reported (Wang et al., 2018; Zhang et al., 2016). The composition and activity of soil microbial communities are affected by the substrates properties, especially pH and organic carbon content (Delgado-Baquerizo et al., 2016). Plants can influence soil pH releasing organic acids into the rhizosphere, and increase the available substrates of rhizosphere microorganisms through releasing carbohydrates. Thus, rhizosphere metabolites not only directly affect the rhizosphere microbial community structure and activity, but also indirectly regulate the rhizosphere microbes by affecting the rhizosphere microenvironment (Morrien et al., 2017). In addition, soil moisture also have a profound impact on the microbial community. In arid and semi-arid regions, changes in soil moisture caused by vegetation restoration strongly affect the rhizosphere microbial community composition, especially those microbial taxa that are adapted to drought (Ochoa-Hueso et al., 2018). Therefore, exploring the variation of the microbial community mediated by rhizosphere metabolites will enhance our mechanistic understanding of plant-microbe-soil interactions.

The Mu Us Desert is a typical arid area in northern China. Wind erosion is one of the most serious ecological and environmental problems in this region, and effective vegetation restoration has become an important way to reduce wind erosion and conserve soil and water (Wu and Ci, 2002). Pinus sylvestris var. mongolica has been extensively planted in this region for sand control and fixation. P. sylvestris not only affects the rhizosphere microbial community, but also drives changes in the physicochemical properties of the rhizosphere soil through root regeneration and rhizosphere metabolism (Galland et al., 2019). Recent studies on P. sylvestris plantations in sandy land mainly focused on the following aspects: (1) the decline of water level caused by the consumption of soil moisture in P. sylvestris plantation with forest age, and the imbalance of water supply and demand (Nan et al., 2020; Dang et al., 2021); (2) dynamic changes of soil microbial communities or functional microorganisms with forest age (Zhao et al., 2020; Bi et al., 2021); and (3) the impacts of afforestation on soil quality including soil nutrients, microbial biomass and extracellular enzyme activities (Huang et al., 2021; Yao et al., 2020). However, the analysis of a single factor cannot fully reflect the growth (or degradation) status of P. sylvestris, and the microscopic changes of rhizosphere soil caused by afforestation. Studying the response of the microbial community of P. sylvestris to rhizosphere metabolites at different growth stages and with soil biotic and abiotic factors will help us understand the rhizosphere microscopic dynamics mediated by rhizosphere metabolites of P. sylvestris, and evaluate the impact of afforestation on the rhizosphere microbial processes.

To this end, we investigated the variation of rhizosphere metabolites composition, edaphic factors, and microbial community structure along chronosequence by selecting P. sylvestris plantations with five different stand ages, and tried to explore the variation of microbial community and their internal driving mechanisms mediated by the rhizosphere metabolites of P. sylvestris. We aimed to (1) assess the response of the soil microbial community to rhizosphere metabolites and edaphic factors with stand age, and determine the interrelationship among them; (2) clarify the relative importance and contribution of rhizosphere metabolites and edaphic factors to the variation of rhizosphere microbial community with forest age.

Section snippets

Site description and sampling

The study was conducted at the Hongshixia Sandy Botanical Garden, 6 km north of the city of Yulin, Shaanxi Province, China. The region is located in the transition zone between the Mu Us Desert and the Loess Plateau. The study area covers an area of more than 300 hectares (ha) and suffers from severe desertification, wind erosion, and water erosion. The region has a warm temperate and temperate semiarid continental monsoon climate. The average annual temperature is 7.9–11.3 °C, the annual

Identification of rhizosphere metabolites

A total of 39 different metabolites within 12 categories were identified by GC–MS (Tables S2; S3), and total ion chromatograms (TICs) of different samples were shown in Fig. S1. In the rhizosphere soil metabolites of the five stand age groups, sterols and lipids accounted for the greatest proportion; the relative abundance of monopalmitin (10.76–18.32%) was greater than other substances, followed by monostearin (6.52–13.58%), and both of them showed a significant increasing trend with stand age

Rhizosphere metabolites and edaphic factors

Our results suggested significant differences in the composition of rhizosphere metabolites at P. sylvestris with distinct forest ages (Fig. 5A and Table S5). The dynamic changes of rhizosphere soil metabolites reflect their response to environmental changes (Massalha et al., 2017). This study suggested that some fatty acids (hexadecanoic acid, n-pentadecanoic acid, and octadecanoic acid) were observed in the rhizosphere soil of P. sylvestris (Table S2). Fatty acids are an important class of

Conclusions

Our results suggest that P. sylvestris released a variety of rhizosphere metabolites (such as fatty acids, monoacylglycerides, and diterpenes) with certain ecological functions, and these metabolites significantly affected the variation of rhizosphere microbial diversity along chronosequence. These changes were reflected in that (1) microbial alpha diversity and dominant microbial taxa have changed, and (2) the complexity of co-occurrence network gradually weaken. Compared with edaphic factors,

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was supported by the National Key Research and Development Program of China (2016YFA0600801, 2017YFC0504504), the West Light Foundation of the Chinese Academy of Sciences (XAB2016A04) and the National Natural Science Foundation of China (41471437, 41101528, 41571225).

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