It is well-established that soil nutrients, microorganisms and enzymes are important components of soil ecosystems (Na et al., 2021; Li Y. et al., 2023). In soil ecosystems, the rhizosphere is closely related to plants and interacts with them throughout their life cycle (Liu et al., 2019). An increasing body of evidence suggests that the diversity of rhizosphere soil microorganisms and the presence of specific genera can ensure proper soil function and promote plant health (Chen et al., 2019; Zhang et al., 2019). Soil enzymes act as biocatalysts, and their activity level reflects soil biological activity and fertility (Gregorich et al., 1994; Mi et al., 2018). Changes in soil microbial and enzyme activities are important indicators of the effectiveness of soil nutrient fertility utilization and respond rapidly to changes in soil environmental conditions, providing an early indication of changes in soil health (Li J. et al., 2023).

The arid and semi-arid areas of north-west China have a poor natural resource endowment and a fragile ecological environment, and are subject to serious soil erosion, accounting for their poor economic status. The past few years have witnessed a burgeoning interest in restoring the natural habitat of this region. Gravel mulching which began in the early Kangxi period of the Qing Dynasty (1,644 to 1911) dating back to about 300 years ago, is a unique form of drought-resistant farming in arid and semi-arid areas of northwest China (Zhao et al., 2017). Gravel mulching involves spreading a mixture of sand and gravel washed down from alluvial fans to form a 10 to 20 cm thick surface layer on farmland (Zhao et al., 2016, 2020). This method can effectively inhibit evaporation, and improve water storage and moisture conservation. Gravel-mulched land in China is mainly distributed in the arid and semi-arid climate transition zone of Gansu and Ningxia provinces. The vegetation types are mostly desert or desert steppe in this region. Vegetation degradation and land desertification have seriously affected the socio-economic development of the region. Since 2004, the Chinese government has widely promoted this technology by means of subsidies and encouraged planting watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai) on gravel-mulched fields. Because of the long sunshine hours and the large temperature difference between day and night during the growth period, the watermelon grown from the stone crevices is crisp., fleshy and high in sugar (Ren et al., 2023). At the same time, it absorbs the trace element selenium in the sand and gravel, and is actively sought after in the market, which in turn has given birth to a unique selenium sand melon industry. However, long-term watermelon continuous cropping leads to drastic shifts in soil bacterial community composition (Gu et al., 2022), soil mineral deficiencies, and the ecological environment was severely negatively impacted. Watermelon production has declined (Wu et al., 2022), and people began to look for other crops to grow.

L. japonica commonly known as “Ren Dong,” has been widely used in traditional medicine in East Asian countries for thousands of years. Its dry flower buds, leaves, and stems are rich in flavonoids, polysaccharides and other components, which have a broad spectrum of antioxidant, anti-carcinogenic, anti-inflammatory, and anti- bacterial effects (Yang et al., 2017; Tang et al., 2021). L. japonica extract is widely used in cosmetics, pharmacological preparations, food, and animal husbandry (Li et al., 2020; Zhang X. et al., 2022; Yang et al., 2023). L. japonica has strong adaptability (Thanabhorn et al., 2006; Yan et al., 2016), is tolerant of severe cold and drought, and does not require high soil nutrient conditions. Cultivation of L. japonica can effectively improve soil nutrients, prevent soil erosion, and fertilize the soil, and has great potential for improvement of the ecological environment and economic development of the gravel-mulched land (Thanabhorn et al., 2006; Yang et al., 2017). Because of its good economic benefits and the emergence of obstacles associated with continuous watermelon production, local enterprises began planting 33.3 ha of L. japonica in 2017, and the sales amounted to more than 960,000 yuan in 2018, reaching a gratifying achievement of one-year investment recovery; in 2019, the planting area was expanded to 66.7 ha. The local government began to encourage the people living locally to plant L. japonica. By 2023, the cropped area of L. japonica was 2000 ha, with a yield of more than 600 kg•ha⁻¹ of high-quality dried flowers, a total output value of nearly 192 million yuan. L. japonica has truly become the ‘rich flower’ of the masses in Zhongwei City, Ningxia, China.

Currently, research on gravel-mulched land has primarily centered on the effects of soil water infiltration and evaporation (Xie et al., 2006), soil nutrients (Qiu et al., 2015), fertilization (Bao et al., 2022) and sand mulching (Qiu et al., 2023) on crops. Our hypothesis was that planting L. japonica will lead to longer-term positive effect on soil microbes, soil enzyme activity and nutrient cycling. To test this hypothesis, a field experiment was conducted in a typical gravel-mulched land to compare growing L. japonica for 1 year, 2 years and 4 years with a control with natural shrub vegetation. The specific objectives of the current study were to determine the effects of different years of growing L. japonica on (i) the soil properties, and (ii) the composition of the bacterial community of L. japonica rhizosphere soil in a gravel-mulched land.

Our study found that planting L. japonica significantly increased SOC, AN, AP, AK and enzyme activity (Table 1). The improved soil quality parameters might be related to improved soil conditions resulting from greater input of plant residues, especially roots (Abbott et al., 2018; Upadhyay et al., 2022). The accumulation of these nutrients activated soil urease, phosphatase and catalase, boosting microbial activity, metabolism, and activity after planting L. japonica in the gravel-mulched land, with faster cycling and transformation of soil nutrients. Planting L. japonica increased the plant biomass and subsequent accumulation of the SOC, which could have affected pH (Table 1). It is well-known that soils rich in SOC have a better buffer capacity to adjust the soil pH (Ma et al., 2022). Moreover, the soil quality can be improved relatively quickly, alleviating the problems related to aeolian sandy soil and crop production in the region (Scheibe et al., 2015). There were little to no statistically significant differences in any of those measured soil properties between plots planted 1, 2 or 4 years ago.

Soil properties are among the most important factors shaping microbial communities (Xi et al., 2022). Rhizosphere microbial populations are constantly exposed to both low and high molecular weight organic compounds exuded from roots, which may be affected by specific physical, chemical, and biological conditions and microbial activities (Xie et al., 2019). Current evidence suggests that soil physical and chemical variables have a substantial impact on the microbial abundance and community diversity during land degradation (Li J. et al., 2023). Research on red soil in southern China showed that pH, AP and AN significantly affected soil bacterial community structure (Muneer et al., 2022). Moreover, in the alpine plateau of northern Tibet, variations in soil pH and SOC significantly affected composition of arbuscular mycorrhizal fungal communities (Chen et al., 2022; Zhou et al., 2022; Zhang M. et al., 2022). These studies overlap in their assertion that the change in soil microbial diversity composition and structure may be caused by change in soil characteristics. In the present study, soil nutrients and enzyme activities accounted for 93.63% of the changes in soil bacterial communities, among which available nitrogen, potassium, urease and catalase were significantly affected.

In this study, the most dominant bacterial phyla observed were Firmicutes, Proteobacteria and Bacteroidetes (Figure 3). There is a growing consensus that Bacteroidetes, as R-strategy flora, occupy a dominant position in the early stage of microbial community succession, and with the gradual maturity of microbial community succession, the relative abundance of K-strategy flora such as Acidobacteria gradually increases (Chen et al., 2016). L. japonica treatment resulted in a significant improvement in the relative abundance of Acidobacteria, and resulted in a reduction in Bacteroidetes and Fusobacteria (Figure 3). In this respect, our study revealed that after L. japonica planting, the bacterial community transitioned from a rapidly growing copiotrophic group to a slowly growing oligotrophic group. After the cultivation of L. japonica in the gravel-mulched field, more plant residues are produced, and a large amount of cellulose is decomposed, creating a favorable environment for the Acidobacteria that can use cellulose. Acidobacteria have been shown to be closely related to soil pH regulation and the degradation of plant residue polymers (Xu et al., 2020). This finding also accounts for the decrease in pH value to a certain extent (Xi et al., 2022). In addition, L. japonica planting in the previous year significantly decreased the relative abundance of Firmicute. This finding indicates that L. japonica planting for a short-term would reduce the pathogenic bacteria belonging to Firmicute (Ehrich et al., 1995).

After L. japonica planting, some bacteria at the genus level with relative abundance greater than 1.0% decreased, and those with less than 1.0% abundance increased significantly, which may be related to the significant improvement of soil physicochemical properties and increased bacterial abundance (Urbanová et al., 2015). Growing crops could provide more C and N to the soil for bacterial utilization through residual roots and litter, increase the number of microorganisms, change the bacterial community structure, and promote a change in the soil bacterial community composition.

Soil microbial diversity is a commonly used index to describe the stability of the microbial community, and is informative to fully reflect the significance of the soil environment on the microbial community and assess the health of terrestrial ecosystem (Coyte et al., 2015). Our study showed that L. japonica planting increased the number of bacterial OTU (Figure 2) and diversity index (Table 4) in the rhizosphere soil. This occurrence might be ascribed to the fact that rhizosphere soil bacteria can use the nutrients secreted by roots to grow and reproduce in the short term, and the diversity and richness of abundant communities gradually increase after long-term continuous cropping (Zhang H. et al., 2022).

The effect observed in the soils might be mediated primarily via a change in the composition and structure of the vegetation present on both planted and non-planted plots (due to L. japonica becoming dominant) (in ‘t Zandt et al., 2023). After planting L. japonica, the nutrient substrates such as C, N and P in the soil were affected by roots and litter, and increased significantly (Table 1), promoting bacterial growth in symbiotic groups. As a result of the impact of changes in land use on soil structure and nutrient availability, the configuration of the soil microbial community undergoes alterations (Gschwend et al., 2021; Xi et al., 2022; Labouyrie et al., 2023). A study by Jiang et al. (2022) on the rhizosphere soil of Torreya grandis cv. Merrillii showed that the effects of pH, organic matter, water-soluble SOC and AN and AP were significant on the dominant soil bacteria.

Overall, L. japonica planting significantly changed the soil microbial structure and diversity of the gravel-mulched land by affecting the soil characteristics and contributing significantly in shaping the diversity of microbial communities.

We found that growing L. japonica decreased soil pH, and increased SOC, AN and other nutrients and enzyme activities, with the highest levels observed after 4 years. The improved soil environments gave rise to an increased soil bacterial community diversity. The main dominant phyla of soil bacteria were Firmicutes, Proteobacteria and Bacteroidetes. The relative abundance of Acidobacteria increased after planting L. japonica, and Firmicutes, Bacteroidetes and Fusobacteria decreased. Collectively, the planting L. japonica in the short term could be a low-cost strategy to improve soil nutrients availability and soil bacterial community diversity, and effectively restore degraded land while promoting the local economy in the gravel-mulched area.

The authors acknowledge that the data presented in this study must be deposited and made publicly available in an acceptable repository, prior to publication. The names of the repository/repositories and accession number(s) can be found at: NCBI – PRJNA1044469.

XW and BM developed the concept of this study and are main contributors to writing the manuscript, data analysis, and preparing figures. HL and YB performed all experiments. ML, NM, and LG contributed to the manuscript edit and review. All authors contributed to the article and approved the submitted version.