Priming, stabilization and temperature sensitivity of native SOC is controlled by microbial responses and physicochemical properties of biochar
Introduction
Soil organic carbon (SOC) represents the largest reservoir of terrestrial carbon (C) (1550 Gt) in the biosphere (Lal, 2008). Due to the large global SOC pool, a small change in SOC decomposition could significantly affect SOC stocks and hence atmospheric CO2 (Lehmann and Kleber, 2015). Increasing global SOC stocks (e.g., 4 per mille annually) can effectively compensate for anthropogenic greenhouse gas emissions (Minasny et al., 2017). As a soil amendment, biochar decomposes more slowly than fresh plant residues, hence it can increase SOC sequestration and has been suggested as an important contributor to the mitigation of global warming (Paustian et al., 2016). Yet, the addition of biochar can affect native SOC decomposition, referred to as the “priming effect” (Kuzyakov et al., 2000; Zimmerman et al., 2011). There is, however, a limited understanding of the impact of biochar on responses of native SOC mineralization to warming and the associated microbial community changes.
The direction and magnitude of priming of SOC mineralization can vary due to the difference in biochar's physicochemical properties resulting from feedstock characteristics, pyrolysis type, and temperature (Ippolito et al., 2020). The associated mechanisms include (i) positive priming of SOC by stimulating microorganisms capable of degrading SOC; (ii) negative priming of SOC by the inhibitory effect on C-degrading enzymes (Li et al., 2018); (iii) preferential substrate utilization of labile biochar C (DeCiucies et al., 2018); and (iv) stabilization of SOC within biochar by forming aggregates or organo-mineral protection (Weng et al., 2018). Previous studies have also shown that pyrolysis temperature is one of the main factors that control the priming effect of biochar on SOC mineralization. With increasing pyrolysis temperature, positive priming of SOC generally decreases (Fang et al., 2015; Maestrini et al., 2015). This may be because high-temperature biochars contain lower amounts of labile C (Fang et al., 2015; Yu et al., 2018). Besides, greater sorption of native SOC to the higher temperature biochar with the greater specific surface area and porosity may block microbial extracellular enzymes from accessing SOC, thus lowering positive priming or stabilizing SOC (DeCiucies et al., 2018). Overall, biochars generally result in short-term positive priming on SOC mineralization, but longer-term C stabilization (i.e., negative priming), possibly linking to (i) the depletion of labile C over time and (ii) the decreased microbial accessibility to SOC due to the physicochemical interaction with biochars (Fang et al., 2015; Weng et al., 2017). However, the relations of SOC priming and differing C fractions of biochar need to be further validated.
A positive priming effect (i.e., an increase) of SOC mineralization is commonly observed following exogenous C inputs, which could be a result of increased activity of both r- and K-strategists (Fontaine et al., 2003; Zimmerman et al., 2011). The r-strategists are characterized by a higher specific growth rate, weaker substrate affinity, and preferential use of easily available C; while the K-strategists are characterized by higher substrate utilization efficiency and substrate affinity, and preferential use of recalcitrant C (Creamer et al., 2015; Margesin et al., 2007). The labile C fraction in biochar might stimulate the growth of r-strategists and microbial biomass turnover, leading to the co-metabolism and positive priming effect on SOC mineralization (Fang et al., 2015; Junna et al., 2014; Luo et al., 2011; Maestrini et al., 2015). Biochar addition was also reported to increase fungi and Gram-positive bacteria (usually K-strategists) within the first several days, showing that K-strategists may be involved in the early positive priming of SOC (Farrell et al., 2013; Yu et al., 2018). The complex C in biochar might cause a greater positive priming effect by triggering K-strategists that are capable of degrading more recalcitrant forms of SOC (Fontaine et al., 2003). Previous studies have also suggested that K-strategists are likely responsible for positive priming once the labile C in soil has been depleted (Fang et al., 2018; Pascault et al., 2013). However, further evidence for the role of r- and K-strategists in priming, as affected by the characteristics of biochar C, is needed.
The temperature sensitivity of soil C mineralization (i.e., Q10, defined as the proportional increase in C mineralization rate per 10 °C rise) has resulted in a range of responses after biochar addition to soil. The Q10 of total soil C with biochar addition (cf. control soil) was reported to be either increased (Chen et al., 2019; Wang et al., 2019; Zhao et al., 2019; Zhou et al., 2017), decreased (Chen et al., 2018; He et al., 2016; Pei et al., 2017; Zhang et al., 2019), or have no change (Bamminger et al., 2018; Li et al., 2018; Ventura et al., 2014). The increased Q10 of total soil C following biochar amendment into soil might be due to (i) the decreased soil C quality (or increased biochemical recalcitrance) that requires high activation energy (Ea) to break down the molecules (Davidson and Janssens, 2006; Zhou et al., 2017), and/or (ii) increased microbial abundance and enzyme activities under warming condition (Chen et al., 2019). In contrast, a decrease in Q10 of total soil C by biochar might be attributed to SOC stabilization resulting from biochar–SOC–mineral interactions (Weng et al., 2017, 2018), or decreased soil microbial C turnover (Chen et al., 2018; Zhang et al., 2019). This could be driven by shifts in the microbial community composition towards microbes that degrade recalcitrant C, such as K-strategists (Chen et al., 2018). Apart from the stabilization of native SOC (Fang et al., 2014), it is possible that activation energy (Ea) of SOC mineralization is reduced by co-location of microorganisms and substrate at the biochar-soil interface, thus decreasing Q10 of native SOC (Pei et al., 2017).
The temperature could be a driver of the direction or magnitude of SOC priming (Creamer et al., 2015), through variations in labile substrate quantity and soil decomposer communities (Lyu et al., 2019). The positive SOC priming by litter consistently increased under warming, which was mediated by increased Gram-positive bacteria, a proxy for K-strategists (Creamer et al., 2015). Similarly, the magnitude of positive priming of SOC mineralization following biochar addition increased with increasing temperature from 20 to 40 °C by enhanced enzyme activity and co-metabolism (Fang et al., 2015). However, the temperature has been shown to have no effect on the magnitude of SOC priming following glucose addition to soil (Ghee et al., 2013). Thiessen et al. (2013) also reported that the positive priming of SOC mineralization with the addition of plant residue was similar in the warm and cold environments. Despite the importance of soil microbial community to the temperature dependence of SOC mineralization, the microbial mechanism of priming response to temperature and native SOC Q10 relating to biochar C quality remains largely unknown.
The objective of this study was to investigate the influence of biochar, its labile (i.e., water extractable) fraction, and recalcitrant (i.e., artifically oxidized) fraction on native SOC mineralization and Q10, and to unravel the associations with the changes of the microbial community. The mineralization rates of SOC and biochar fractions were quantified using a stable isotope technique (Singh and Cowie, 2014). Quantitative PCR and high-throughput sequencing of the 16S rRNA were used to assess the microbial community abundance and composition as affected by biochar fractions (Zhu et al., 2019). We hypothesized that:
- i)
With the application of low-temperature rice straw biochar, positive SOC priming will be initially induced due to the presence of labile C in biochar that stimulates r-strategists, and that the positive SOC priming may be maintained over time, due to increased activity of K-strategists over time. High-temperature rice straw biochar will result in the stabilization of native SOC after the depletion of the labile C;
- ii)
The elevated temperature will drive increased positive priming of SOC mineralization by low-temperature biochar and will lessen the stabilization of native SOC via the increased abundance of K-strategists in the soil;
- iii)
Biochar addition will decrease Q10 of native SOC due to the enriched recalcitrant C decomposer (K-strategists) that decreases activation energy and sorptive protection of SOC by biochar.
Section snippets
Soil and biochars
Soil was collected from the 0–15 cm layer from an agricultural field where sugarcane (Saccharum spp.), a C4 plant naturally enriched with 13C, had been grown for over 30 years at South China Agricultural University, Guangzhou, China (23°09′1.3″N, 113°21′21.6″E). The soil is a sandy clay loam containing 54% sand, 29% silt, and 17% clay and is described as an Entisol according to the World Reference Base for Soil Resources (IUSS Working Group WRB, 2006). The soil was air-dried and gravel and
Total C mineralization
The total C mineralization rates in the control and biochar treatments were initially high across all temperatures (3.9–60 mg CO2–C kg−1 soil d−1) and then decreased over time (0.23–8.3 mg CO2–C kg−1 soil d−1) (Fig. S1a). Across different temperatures, the most significant difference between biochar treatments occurred during the first 18 days of incubation. That is, the total C mineralization rates during the first 4 days were significantly higher in the LBC, LBCD, and LBCR than the
Microbial responses and physicochemical properties of biochar control SOC priming
Positive priming of SOC was found following the addition of low temperature (300 °C) rice straw biochar, while higher temperature rice straw biochar (800 °C) resulted in the stabilization of SOC across the incubation thermosequence (Fig. 1). This difference is likely to have been controlled by substrate availability from biochar addition altered the soil microbial abundance and community composition (Fig. 3, Fig. 4), and by the physicochemical properties of biochar that changed microbial
Conclusions
The results from this study suggest that the priming of SOC mineralization was affected by C fractions in biochar that alters the microbial community, and by the physical properties of biochar such as the surface area or surface functional groups that sorb labile C thus restricting microbial access. Rice straw biochar produced at 300 °C and its recalcitrant fraction stimulated K-strategists (e.g., fungi and Actinobacteria) and induced positive priming of SOC via co-metabolism. In the presence
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.
Acknowledgment
This study was supported by a grant from the National Natural Science Foundation of China (No. 41471181).
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