Microorganisms maintain C:N stoichiometric balance by regulating the priming effect in long-term fertilized soils
Graphical abstract
Introduction
Microorganisms are key components in regulating organic matter decomposition, soil carbon (C) sequestration, and nutrient (re)cycling (Mooshammer et al., 2014b; Hartman et al., 2017). The microbial decomposition of fresh plant residues and soil organic matter (SOM) liberates C and nutrients for microbial biomass synthesis and extracellular enzyme production (Allison and Vitousek, 2005; Wei et al., 2019). The amount of nutrients released into the soil during decomposition depends on the stoichiometry of C to nutrient ratios (hereafter, C:nutrients) in plant residues or SOM and the demand of both microbial C and nutrient stoichiometry (Sinsabaugh and Follstad-Shah, 2012; Nannipieri et al., 2018). However, the mechanism by which soil microorganisms regulate the decomposition of organic inputs to maintain the stoichiometric balance of microbial biomass remains poorly understood.
The nutrient stoichiometry of soil microbial biomass is more stable (in range and variance) than that of organic inputs, indicating that microorganisms are largely homeostatic in terms of their biomass carbon:nitrogen:phosphorus (C:N:P) ratio (Cleveland and Liptzin, 2007; Wei et al., 2020). Microbial decomposers can adjust their biomass C:nutrient ratios to adapt to the C:nutrient ratio of a resource. This phenomenon is achieved by altering the structure, composition, or rate of metabolic function of microbial communities (Sinsabaugh and Follstad-Shah, 2012; Mooshammer et al., 2014b; Fang et al., 2018). Under nutrient-limited conditions, fast-growing microorganisms (copiotrophs or r-strategists) have lower biomass C:N and C:P ratios than slow-growing organisms (oligotrophs or K-strategists) (Elser et al., 2003). Furthermore, microorganisms regulate extracellular enzyme production and stoichiometric ratios, which, in turn, control nutrient release to meet their stoichiometric requirements (Allison and Vitousek, 2005; Wei et al., 2019). Therefore, the stoichiometric demand for nutrients by microbes is a key regulator of soil C cycling.
In terrestrial ecosystems, resources (i.e., substrates) available to soil microorganisms have considerably wider and more variable C:nutrient ratios than those of soil microorganisms (Manzoni et al., 2010; Ge et al., 2017). Soil microorganisms are able to adjust their organic C and nutrient metabolism strategies, leading to the convergence of microbial biomass and substrate stoichiometry (Hartman et al., 2017; Fang et al., 2018). Soil microorganisms catabolize organic C via overflow respiration under C-rich conditions, but mostly anabolize organic C under C-limited conditions (Li et al., 2018; Zhu et al., 2018b). Furthermore, organic C input alters the microbial decomposition of SOM, which is known as the priming effect (PE) (Kuzyakov et al., 2000). Nutrients released during SOM decomposition that meet microbial demand potentially generate balanced microbial C:N ratios. For instance, in soils where inputs of labile C increase C:nutrient ratios, the growth and activity of K-strategists is stimulated, promoting microbial N mining (i.e., a positive PE) (Fang et al., 2018; Peduruhewa et al., 2020). In contrast, adding substrates with low C:nutrient ratios to soil could result in a negative PE (Liu et al., 2017; Yu et al., 2018). Therefore, the C:N stoichiometry of soil resources strongly influences both microbial growth and PE (Chen et al., 2018).
Paddy fields cover approximately 165 million ha worldwide, with rice crops being grown two or three times every year (Lal, 2004; H.Y. Liu et al., 2019; Y. Liu et al., 2019). Rice yield, fertility, the physicochemical properties of soil (Atere et al., 2020; Mbuthia et al., 2015), and microbial community composition change in response to long-term fertilization practices in paddy soils (Li et al., 2021a, Li et al., 2021b; Luo et al., 2019). Consequently, these changes influence soil C and nutrient turnover and rebalance C:nutrient stoichiometry between microbial biomass and substrates (Ge et al., 2020; Mooshammer et al., 2014b; Zhu et al., 2018a). Thus, the dynamics of organic matter input mineralization and nutrient mining from SOM depend on long-term fertilization regimes. It is, therefore, necessary to clarify the effects of labile C input on soil resource stoichiometry and microbial activity to deepen our understanding on PE mechanisms in paddy fields.
Here, we aimed to investigate: (1) how labile C (as 13C-labeled glucose) addition affects microbial C:N stoichiometry and PE dynamics in long-term fertilized paddy soils, and (2) how microorganisms regulate their C and N balance and enzyme activity to maintain stoichiometric homeostasis by nutrient mining. We hypothesized that (i) microbial N mining from SOM would be increased by positive PE, contributing to a notable increase in the dissolved organic C (DOC):ammonium (NH4+) ratio, which would induce microbial N limitation after glucose addition; and (ii) soil microorganisms would increase N- and C-hydrolase production under a high DOC:NH4+ ratio and labile C exhaustion, respectively, maintaining the C:N stoichiometric balance between microbial biomass and substrates available in soil.
Section snippets
Site description and fertilization strategies
Soil was sampled from a long-term field experiment in Ningxiang County, Hunan Province, China (28°07′N, 112°18′E), in April 2017. The soil is classified as Hydragric Anthrosol developed from red granite parental material (Driessen et al., 2000), and has a sand loamy texture (based on the United States Department of Agriculture soil taxonomy). The study site is a milk vetch–rice–rice rotation field with a history of long-term fertilization (since 1986). The region is characterized by a
Glucose mineralization and PE
Cumulative glucose mineralization was 38%–59% of the 13C added at day 60. The highest cumulative glucose mineralization rate (59%) was recorded in NPKS-fertilized soil, followed by NPK-fertilized soil, non-fertilized soil, and NPKM-fertilized soil (38%) (Fig. 1a). The cumulative SOC mineralization increased linearly in long-term fertilized soils without glucose addition. Approximately 2.5% SOC was mineralized after day 60. The highest mineralization was recorded in NPK-fertilized soil. Glucose
Effects of glucose addition on the microbial C:N stoichiometric imbalance
Microbial communities inhabiting various environments are exposed to resources that contain varied content and ratios of elements (Hessen et al., 2013). In general, the C:N ratios of the resources available to microorganisms are considerably higher than those of either bulk soil or microbial biomass (Mooshammer et al., 2014b). Similarly, in our study, DOC contents and DOC:NH4+ ratios increased with glucose addition, intensifying the imbalance of microbial C:N [(DOC: NH4+):(MBC:MBN)] by 24- to
Conclusions
Labile C input initially increased the C:N ratio of available resource, which induced microbial stoichiometric imbalance. Thus, soil microorganisms coped with the relative N limitation by increasing N-hydrolase production and nutrient mining to obtain the necessary N resources, which led to positive priming effect. However, with the rapid utilization of labile C, microorganisms shifted to C limitation. This resulted in decrease of microbial growth and N-hydrolase production, and led to much
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 study was supported by the National Natural Science Foundation of China (41877104 and 41771337); the National Key Research and Development Program (2016YFD0300902); Natural Science Foundation of Hunan Province (2019JJ30028 and 2019JJ10003); the Youth Innovation Promotion Association of the Chinese Academy of Sciences (2019357); and the State Scholarship Fund of China Scholarship Council (CSC) to Zhu ZK and the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese
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