Land-use change from cropland to plantations affects the abundance of nitrogen cycle-related microorganisms and genes in the Loess Plateau of China

https://doi.org/10.1016/j.apsoil.2020.103873Get rights and content

Highlights

  • Land-use change affects the abundance of nitrogen-cycling genes and microorganisms.

  • The effect is mainly related to changes in soil properties.

  • The potential of nitrification and denitrification is high in cropland soil.

  • The potential of assimilatory nitrogen reduction is high in cropland soil.

Abstract

The “Grain for Green” project has been considered an effective avenue to control soil erosion, improve vegetation coverage and prevent ecosystem degradation in the Loess Plateau of China. However, the effect of the project on the underlying microbial mechanism of soil nitrogen cycling is not well understood. In the present study, the effect of land-use change from cropland to plantations on soil microbial community and functional genes involved in the nitrogen cycle was investigated via metagenomic sequencing analyses. The abundance rather than the composition of functional genes for nitrification, denitrification, assimilatory and dissimilatory nitrogen reduction significantly changed during the conversion of cropland to plantations. The abundance rather than the composition of microorganisms involved in the nitrogen cycle also changed significantly. The effect on the abundance of functional genes and microorganisms was mainly related to changes in soil properties, such as organic matter, total nitrogen, available phosphorus, available potassium and pH. The observed changes likely decrease the potential of nitrification, denitrification and assimilatory nitrogen reduction in the soil of plantations. Our results demonstrate that land-use change from cropland to plantations significantly affects soil nitrogen cycling in the Loess Plateau of China.

Introduction

The nitrogen cycle is one of the basic material cycles in the biosphere and plays an important role in the transformation of different forms of nitrogen (Thamdrup, 2012). It not only affects the productivity and sustainable development of soil but also affects global environmental change (Canfield et al., 2010). Microorganisms are the main drivers of nitrogen cycling and play important roles in different nitrogen transforming processes, such as assimilation, ammonification, nitrification, denitrification, anaerobic ammonium oxidation (anammox) and nitrogen fixation (Kuypers et al., 2018). Different microbial communities and their functional genes (for example, nifH for nitrogen fixation, amoA for nitrification, and narG, nirS, and nosZ for denitrification) participate in different nitrogen transforming processes (Qin et al., 2016; Blaud et al., 2018). It is, therefore, useful to understand these functional genes and their differential abundances to elucidate the mechanism of nitrogen cycling in the biosphere.

Land-use change refers to the conversion of land use and management via anthropogenic activity (Broch et al., 2013). It has received widespread scientific attention due to its significant impact on natural landscapes, ecosystem functioning and climate change (Mitsuda and Ito, 2011; Broch et al., 2013). In the process of land use change, vegetation composition and soil properties change in varying degrees, which influences the composition and diversity of the soil microbial community (Moon et al., 2016; Ma et al., 2019). As an important component of soil microorganisms, the abundance and composition of the microbial community and functional genes related to the nitrogen cycle are also affected (Wu et al., 2017; Sun and Badgley, 2019; Xu et al., 2019a). Land-use change is, therefore, generally considered to be an important factor affecting the nitrogen cycle (van Lent et al., 2015).

As one of the most vulnerable ecosystems in China, the Loess Plateau is well known for extensive loess distribution, severe soil erosion, desertification and low vegetation coverage (Xu et al., 2019b). To prevent continued degradation, the Chinese government has launched the national “Grain for Green” project (Fu et al., 2017). As described by Lü et al. (2012), a total of 8.69 × 105 ha of cropland was converted to forest in this region between 2000 and 2008. The “Grain for Green” has been considered an effective avenue to increase soil carbon storage (Hu et al., 2017; Yang et al., 2019), and due to the close coupling between the soil carbon and nitrogen cycles (Quan et al., 2014), it is reasonable to believe that the change of carbon content will also affect the nitrogen content. Indeed, it has been reported that conversion to forest increases soil nitrogen storage in conjunction with increasing carbon storage (Zhang et al., 2020). It is, therefore, predicted that the abundance of genes related to the nitrogen cycle within the soil microbial community may decrease after conversion from cropland to plantations. Because nitrogen inputs and outputs are so transitory, nitrogen cycling genes provide a useful indicator of the changed potential for nitrogen inputs or outputs for the Loess Plateau system. At present, numerous studies have focused on the response of the carbon cycle and soil microbial abundance and composition to vegetation restoration in the Loess Plateau region (Liu et al., 2018; Wang et al., 2018; Yang et al., 2020). The response of the nitrogen cycle to vegetation restoration in this region receives much less attention. At present, two studies show that the afforestation affects the microbial community of the nitrogen cycle (Xu et al., 2019a, Xu et al., 2019b), but most of these studies only focus on the microbial community composition in a certain process of the nitrogen cycle (for example, nitrogen fixation, nitrification or denitrification) (Wu et al., 2017; Tao et al., 2018; Meng et al., 2019; Wang et al., 2019). There is still a limited understanding of how the microbial community composition involved in the whole nitrogen cycle is impacted. Moreover, how functional genes involved in the nitrogen cycle respond to afforestation is also unclear.

Metagenomic sequencing can reflect the composition, structure and functional potential of microbial communities in specific environments via direct sequencing of the extracted DNA (Jansson and Hofmockel, 2018). At present, the method has been widely used to analyze soil microbial communities and functional genes and their response to land use change (Castañeda and Barbosa, 2017; Zhong et al., 2018). In the present study, we used metagenomics to analyze characteristics of the soil microbial community and functional genes involved in the nitrogen cycle during the conversion of cropland to plantations in the Loess Plateau. The objectives were to explore the change in microbial community and functional genes involved in the nitrogen cycle and their response to soil properties. It was hypothesized that the abundance of genes related to the nitrogen cycle would change significantly after the land-use conversion and the associated increase of soil carbon storage in the region.

Section snippets

Field site, soil sampling and soil physicochemical properties

The study site, belonging to a hilly area of the Loess Plateau, is in Youyu County, Shanxi Province, China. The region has to a temperate continental monsoon climate with an average annual temperature around 4.2 °C and average annual precipitation around 410 mm. The soil is classified as calcic cambisols according to the FAO-UNESCO soil map of the world (Selcer, 2015).

The two most common land-use types in the region were selected, namely, plantations (Pinus sylvestris var. mongolica Litv.) and

Changes in functional genes involved in the nitrogen cycle during the conversion of cropland to plantations

As shown in Fig. 1, functional genes involved in the nitrogen cycle were studied to investigate changes in their abundance and diversity during the conversion of cropland to plantations. For nitrification, five functional genes (nxrA, nxrB, pmoA-amoA, pmoB-amoB and pmoC-amoC) were detected. Among them, the abundance of nxrA and nxrB significantly decreased during the conversion of cropland to plantations (p < 0.05). Four genes involved in denitrification (narG, narH, napA and nirK) were

Changes in functional genes involved in the nitrogen cycle during the conversion of cropland to plantations

As described by Li et al. (2020), nitrogen cycling contains seven different processes of ammonification, nitrification, denitrification, anammox, assimilatory nitrogen reduction, dissimilatory nitrogen reduction and nitrogen fixation. In the present study, only five processes of ammonification, nitrification, denitrification, assimilatory nitrogen reduction and dissimilatory nitrogen reduction were found. Although the process of denitrification was found, some functional genes, such as norZ and

Conclusion

In this study, the abundance of some functional genes participating in the nitrogen cycle was shown to significantly decrease during the conversion of cropland to plantations. The abundance of some microorganisms involved in the nitrogen cycle also changed significantly. The effect on the abundance of microorganisms and functional genes was mainly related to changes in soil properties, such as organic matter, total nitrogen, available phosphorus, available potassium and pH. All changes likely

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.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 41701108).

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