Responses of soil microbial community composition and enzyme activities to long-term organic amendments in a continuous tobacco cropping system
Introduction
Tobacco is one of the most important economic crops with a long history of cultivation worldwide (World Health Organization, 2015). China grows approximately 32% of the world's tobacco, accounting for ~10% of the national tax income (FAO, 2019; Hu et al., 2016). Tobacco is typically grown without interruption in the same land year after year (continuous cropping) due to limitations in cultivated lands and requirement for yield maximization; however, this can lead to soil degradation and consequently low yield and quality, and poor seedling growth (Chen et al., 2018; Zou et al., 2018). Tobacco selectively absorbs some soil nutrients in continuous tobacco cropping systems, resulting in decreases in soil mineral nitrogen (NH4+-N + NO3−-N), Olsen-P, organic carbon (SOC), total nitrogen (TN), and pH value, as well as in an imbalance in soil nutrients (Chen et al., 2018; Zhang et al., 2016; Zou et al., 2018). Tobacco root exudates have been reported to enrich multiplication of detrimental bacteria (e.g., Ralstonia solanacearum) and reduce the beneficial bacteria abundances (e.g., Arthrobacter and Lysobacter) (Santhanam et al., 2015; She et al., 2017). The decreased soil beneficial bacterial and fungal abundances might induce the decreases of soil urease, invertase, phosphatase, and catalase activities in continuous-cropping tobacco fields (Chen et al., 2018; Wang et al., 2017). Moreover, tobacco has been shown to generate allelopathic substances (e.g., phenolic acids) more easily than other plants (Deng et al., 2017; Ren et al., 2015). Therefore, practical approaches for mitigating soil degradation and increasing agricultural sustainability and production are needed for tobacco production (Liu et al., 2020; Zhang et al., 2021; Zou et al., 2018).
Microorganisms are involved in many critical processes for improving and maintaining soil fertility and are considered as efficient biological indicators of soil health (Beckers et al., 2017; Lehmann et al., 2020). Previous studies have shown that organic amendments had a positive effect on microbial abundance and changed the community composition of soil microorganisms in field experiments (Luo et al., 2019; Peng et al., 2016; Ye et al., 2021). For example, Ye et al. (2021) found that manure application suppressed plant pathogens and parasites in a long-term continuous peanut cropping system, probably because the allele chemicals and beneficial microorganisms were increased by the manure amendments. Likewise, a 7-year field experiment by Peng et al. (2016) showed that rice straw application increased arbuscular mycorrhizal fungi (AMF) abundance in a rapeseed-rice rotation system, which can improve soil nutrient turnover and provide various nutrients for plant growth in return for photosynthetically-derived carbohydrates (Smith and Read, 2008). Glomalin-related soil protein (GRSP) is a wall protein of the AMF mycelium, accounting for approximately 5% of soil C content and known to protect labile SOC by forming soil aggregates (Treseder and Turner, 2007). In a 5-year field experiment, Liang et al. (2018) observed that straw application increased soil GRSP content in a wheat-maize rotation system, which might be probably caused by the increases in soil NH4+-N and NO3−-N content (Liang et al., 2015, Liang et al., 2019). As reported by Luo et al. (2019) based on a meta-analysis of 599 measurements, organic amendments could increase phosphomonoesterase-harboring microbial abundance, which can mineralize organic phosphorus (P) and was correlated with the increased SOC, TN, Olsen-P, and microbial biomass carbon (MBC) and nitrogen (MBN) content.
Soil enzymes, which are mainly produced by the cellular metabolism of soil microorganisms have been reported to directly mediate soil carbon (C), nitrogen (N), and P cycling (Sinsabaugh et al., 2008). Ecoenzymatic stoichiometry has been used as an indicator of the relative limitations of microbial resources because enzymatic activities can determine the relationships between the metabolic and nutrient requirements of microbial assemblages and nutrient availability (Moorhead et al., 2016; Sinsabaugh et al., 2008). Generally, microbial processes are known to have a competitive advantage over plants in the acquisition of soil nutrients (Lipson et al., 1999; Hodge et al., 2000). Thus, if microorganisms are limited by a nutrient, plants should also be limited by that nutrient. Organic amendments have the potential to increase soil enzymatic activities and alleviate microbial nutrient limitations by providing available nutrients for microbial growth and metabolism (Cai et al., 2019; Ling et al., 2014; Liang et al., 2021; Zhang et al., 2019b). In a 13-year field experiment, Ling et al. (2014) reported that application of manure increased the activities of soil β-1,4-glucosidase (BG) and β-1,4-N-acetylglucosaminidase (NAG) in a continuous maize cropping system, mainly due to the increased SOC. Likewise, Liang et al. (2021) reported that the activities of soil BG and NAG, as well as soil fertility and crop yields were increased by straw application in 5-year field experiments, and there were significant correlations between the soil fertility properties and enzymatic activities. Based on a 26-year field experiment, Zhang et al. (2019b) found that the long-term application of manure increased TN, SOC, total phosphorus (TP), and hydrolytic enzymes activities, and alleviated microbial C and P limitations in a corn-corn-soybean rotation system.
Long-term field experiments are the only practical way to assess the sustainability and productivity of different treatments with organic fertilizers in agroecological systems (Johnston and Poulton, 2018). Some studies have showed that organic amendments alleviated soil degradation by improving soil microbial community and enzymes in long-term (>10 years) continuous peanut and maize cropping systems (Ling et al., 2014; Ye et al., 2021). However, there are obvious differences in soil and plant properties (e.g., nutrient limitations, microbial communities, and allelopathic substances) between the continuous tobacco cropping system and other continuous cropping systems (Chen et al., 2018; Deng et al., 2017; Fiorini et al., 2020; Liu et al., 2015). In addition, the chemical composition of organic materials affects soil microbial community, enzymatic activity, and nutrient limitation by changing the properties of soil (Li et al., 2019; Luo et al., 2018). There are significant differences in the content and ratios of nutrient elements and chemical components among the straw, oilseed residues, and manure (Doshi et al., 2014; Xu et al., 2017; Yu et al., 2020; Zhang et al., 2010). For example, C:N ratio of straw was obviously higher than that of oilseed residues and manure, and the lignin content decreased in the following order of straw > oilseed residues > manure (Doshi et al., 2014; Xu et al., 2017; Yu et al., 2020; Zhang et al., 2010). Therefore, less is still known on the soil microbial communities and microbial nutrient status affected by long-term (>10 years) organic amendments (e.g., straw, oilseed residues, and manure) in a continuous tobacco cropping system.
In the current study, we hypothesized that the application of corn straw, oilseed residues, and composted pig manure would mitigate soil degradation by improving soil physiochemical properties, microbial community, and enzymatic activities, and by decreasing microbial nutrient limitations in a continuous tobacco cropping system. Moreover, there are significant differences in soil microbial community, enzymatic activity, and nutrient limitation among the measures of corn straw, oilseed residues, and composted pig manure application. To test this, we investigated the long-term effects of the application of corn straw, oilseed residues, and composted pig manure on plant and soil physicochemical properties, microbial community, enzymatic activities, microbial resource limitations, and GRSP content in a tobacco monoculture field.
Section snippets
Experimental site
The long-term field experiment was carried out over 11 years from 2007 to 2018 in a typical tobacco field (approximately 20 years old), located at the Yunnan Tobacco Agronomy Research Center's Yanhe Research Farm, Yunnan Province, China (24°14′N, 102°30′E, elevation of 1,680 m). The study area has a subtropical monsoon climate, with an annual average precipitation of 1,160 mm and air temperature of 15.9 °C. The soil is classed as red soil in Chinese soil taxonomy (Gong et al., 2007) or Typic
Tobacco yield
We found that, on average, the 5-y tobacco yields under treatment with CF, CFS, CFO, and CFM treatments were 1735, 1675, 1921, and 1952 kg ha−1, and were significantly higher, by 98%, 91%, 119%, and 123%, respectively, compared with the CK (p < 0.05; Fig. 1). The average tobacco yields from the CFO and CFM were significantly increased by 11% and 15%, respectively (CFO); 13% and 17%, respectively (CFM), compared to the CF and CFS (p < 0.05). Relative to the CK, tobacco yields for the CF, CFS,
Effects of organic amendments on soil microbial community
In our field experiment, we found that organic amendments significantly affected soil microbial community composition after 11 years of treatment implementation (p < 0.05; Fig. 3a). To the best of our knowledge, few studies have reported the long-term impacts of straw, oilseed residues, and pig manure amendments on soil microbial community in tobacco fields (>10 years). The organic amendments treatments strongly increased soil G+ and G− PLFAs, bacteria, fungi, total PLFAs, and MBC in the
Conclusion
Our long-term field study demonstrated that the application of organic fertilizers stimulated microbial growth by improving soil properties. Organic amendments increased fungi/bacteria ratios but decreased G+/G− ratios. Soil enzymatic activities were also increased, except that there were no obvious differences in the activities of NAG + LAP and PPO between treatments with CF and CFO. Straw addition treatment had the lowest SOC content among organic amendments treatments, which might be due to
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 National Natural Science Foundation of China (41771337, 41807097), Yunnan Science and Technology Key Research Project (2018BB019, 202001AU070006), Tobacco Monopoly Bureau China (2019530000241011), and Guangxi Natural Science Foundation (2019GXNSFBA245096, 202010593090).
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