Effects of rotation and Bacillus on the changes of continuous cropping soil fungal communities in American ginseng

World Journal of Microbiology and Biotechnology https://doi.org/10.1007/s11274-023-03807-w (2023) 39:354 RESEARCH Effects of rotation and Bacillus on the changes of continuous cropping soil fungal communities in American ginseng Fengan Jia1 · Fan Chang1 · Min Guan3 · Qingan Jia4 · Yan Sun2 · Zhi Li2 Received: 3 August 2023 / Accepted: 13 October 2023 © The Author(s) 2023 Abstract The continuous cropping obstacle is the main factor in leading to difficulty in American ginseng replanting. The dormant microbiota in the soil may be the cause of American ginseng disease and eventually caused continuous cropping obstacles, but there are few studies on the dynamic changes of soil microenvironment after American ginseng planting. In this study, we tracked short-term variation in physicochemical properties, enzyme activities, and fungal communities over time-series in soils with continuous cropping obstacle under crop rotation and probiotic Bacillus treatments. Furthermore, we examined the relationships between the important fungal compositions and the soil properties. The results showed that sucrase, cellulase, urease and acid phosphatase activities were significantly increased, while catalase and dehydrogenase were decreased with treatments time. Rotation treatment significantly affected the diversity, dissimilarity degree and species distribution of soil fungal community with continuous cropping obstacle over a short-term. Moreover, beneficial fungal biomarkers such as Cladorrhinum, Oidiodendron, and Mariannaea were accumulated at 48 h under rotation treatments. Almost all fungal biomarkers were negatively correlated with hydrolases and positively correlated with oxidoreductases and acid phosphatase under crop rotation treatments. This study suggested that compared to probiotic Bacillus, crop rotation can significantly affect soil fungal community structure, especially the enrichment of specific potentially beneficial fungal species. Our findings provide a scientific basis for understanding the dynamic changes of fungal communities and soil properties with continuous cropping obstacle of American ginseng in initial stage of soil improvement. Keywords American ginseng · Fungal community · Dynamic changes · Continuous cropping obstacle · Crop rotation Introduction The cropping obstacle, characterized by reduced crop yield and quality resulting from prolonged monoculture continuous cropping, has been observed in both annual and perennial crops (Tan et al. 2021). After harvest, replanting of traditional Chinese medicine will also cause soil continuous cropping obstacles, resulting in slow growth, Zhi Li 1 Shaanxi Institute of Microbiology, Xi’an 710043, China 2 College of Life Science, Shaanxi Normal University, Xi’an 710062, China 3 Shaanxi Agricultural Machinery Research Institute, Xianyang 712000, China 4 Institute of Medical Research, Northwestern Polytechnical University, Xi’an 710072, China increased incidence of soil-borne diseases, and decreased yields (Tagele et al. 2023; Wang et al. 2023b). The continuous cropping obstacle of traditional Chinese medicine has always been a bottleneck problem in the development of traditional Chinese medicine, especially in the cultivation of American ginseng (Panax quinquefolius L.) (Xiao et al. 2016). Due to its slow growth, American ginseng usually requires 4 years of growth to achieve optimal biomass and active component content (Zhang et al. 2023b). However, the soil cultivated the American ginseng for one season can lead to a decline in both yield and quality on the same land for 10 years or more (Li et al. 2020). Although American ginseng has adopted “two-year land-changing planting” transplanting mode in northwest China, soil continuous cropping obstacle is still unavoidable and seriously restricts the local American ginseng cultivation (Chang et al. 2022). The cropping obstacle may include numerous biotic and abiotic factors, e.g., changes in soil physicochemical properties and enzyme activities (Chung et al. 2017; Wei et al. 13 354 Page 2 of 11 2018; Zhang et al. 2020a). enriched soil-borne pathogenic microorganisms (Liu et al. 2021), and allelopathic effects of plants (Zhang et al. 2023c). Among them, soil microbiota are the main driving factor for soil nutrient cycling and transformation (Jiao et al. 2019a). The establishment of the soil microbiota is a dynamic process. In particular, the initial microbial community can become more specific by selection for plant growth or different treatments (Bulgarelli et al. 2013; Tkacz and Poole 2015). In the studies of Panax ginseng, the increase of in cultivation years significantly changed the diversity of soil microbial communities and led to the accumulation of soil pathogenic fungi (Tong et al. 2021). Crop rotation could significantly affect the structure and composition of American ginseng continuous cropping soil microbial community, which were influenced by the alteration of soil properties (Liu et al. 2021). Our previous research also found the microbiota in soil and rhizosphere microhabitat had a tendency of gradual differentiation and specific enrichment during the growth process, especially in the first year of American ginseng cultivation (Chang et al. 2022). Fungal community is an essential component of soil microbiome which play an important role in material circulation, energy transfer, as well as inhibition or prevalence of soil-borne diseases (Li et al. 2022). Some studies have shown that the dynamic shifts of the fungal community with the cropping process of American ginseng could potentially change the soil composition, and the enrichment of potential pathogenic fungi may change the rhizosphere secretions, collectively impacting the soil environment and leading to the occurrence of continuous cropping obstacles (Bi et al. 2023; Zhang et al. 2023b). However, these studies only focused on specific time points during the growth of American ginseng or alterations in soil and plants pre- and post-intervention. Crop rotation and Bacillus amyloliquefaciens biocontrol agent have been demonstrated to effectively mitigate the replanting difficulties and soil diseases development caused by soil continuous cropping obstacles (Li et al. 2022; Wang et al. 2023a). However, the reasons for the sustained alleviation of soil continuous cropping obstacles after initial intervention have not been fully explained. We hypothesized that the continuous cropping obstacles might be related to the dormant fungal community in the soil, and different soil improvement methods could regulate the structure and composition of the fungal community in the initial stage. Time series analysis has proven to be an effective strategy for exploring the dynamics in the structure and composition of soil microbiota and has been widely adopted in rice and Arabidopsis studies (Lundberg et al. 2012; Edwards et al. 2018). In this study, time-series trials were performed to track the dynamic sh (...truncated)