Increasing plant species diversity enhances microbial respiration but does not alter its temperature sensitivity in a subtropical karst forest

Abstract

Temperature sensitivity of soil microbial respiration (or soil organic carbon decomposition) is crucial in determining the dynamics of soil organic carbon or carbon cycle-climate feedback under global warming. Though increasing plant species diversity (PSD) has been found to stimulate soil organic carbon accumulation during ecological restoration or afforestation, whether this carbon sink can persist under global warming largely depends on the responses of temperature sensitivity of microbial respiration to PSD. Nevertheless, the latter remains unknown so far. Here, soil microbial respiration and its temperature sensitivity were investigated based on an incubation experiment with soils collected in 43 plots covering a natural gradient of PSD as indexed by Shannon-Weiner index ranging from 0.15 to 3.53 in a subtropical forest with calcareous soil. Increasing PSD stimulated soil microbial respiration by increasing soil water content and microbial biomass but decreasing fungal/bacterial biomass ratio. Nevertheless, PSD had no significant effect on the temperature sensitivity of microbial respiration due to the contrasting effects of soil biotic and abiotic variables. Increasing PSD stimulated temperature sensitivity by enhancing soil pH, or suppressed temperature sensitivity via decreasing fungal/bacterial biomass ratio. These findings suggest that increasing PSD would stimulate microbial respiration along with soil organic carbon accumulation, but not alter the carbon cycle-climate feedback when implementing ecological restoration or afforestation. Additionally, this study, for the first time, provides the mechanism underlying the response of temperature sensitivity of microbial respiration to PSD, which should be considered when assessing the impacts of PSD on soil organic carbon dynamics under climate change.

Graphical abstract

Keywords

plant species diversity / soil microbial respiration / soil organic carbon / subtropical forest / karst region / temperature sensitivity

1 Introduction

Forest ecosystems play a key role in global carbon storage by responsible for a total amount of 861 ± 66 Pg C, of which 44% is stored as soil organic carbon (SOC) (Pan et al., 2011). Therefore, small changes in forest SOC pool may lead to a substantial fluctuation in atmospheric carbon dioxide (CO₂) concentration, and subsequently affect global climate. Soil microbes use SOC as a source of energy and convert a fraction of carbon (C) into atmosphere as CO₂, a process known as soil organic carbon decomposition or microbial respiration (Rm) (Karhu et al., 2014). Global warming may promote Rm and reduce the ability of forest soil to act as a carbon sink, leading to a positive C cycle-climate feedback (Bradford et al., 2016). As a key parameter in assessing the response of Rm to global warming, temperature sensitivity (or Q₁₀ hereafter) of Rm represents a factor by which Rm increases in response to a temperature increase of 10°C (Walker et al., 2018). Therefore, a better understanding of the controls on Rm and Q₁₀ is undoubtedly crucial for improving the representative of C cycle-climate feedbacks in Earth system models under global warming (Niu et al., 2021). Increasing plant species diversity (PSD) benefits SOC accumulation (Chen et al., 2023; Qian et al., 2023), and has been identified as an effective strategy for maintaining or increasing forest SOC pool under global changes (Ontl et al., 2020). Though increasing PSD has been found to stimulate Rm, and vice versa (Chen and Chen, 2019), whether and how PSD is related to Q₁₀ remain unknown.

Both Rm and Q₁₀ are affected by a variety of biotic and abiotic factors, including microbial community abundance and composition, C quantity and quality, SOC protection via mineral association or aggregation (Qin et al., 2019), but their main controls may be divergent (Chen et al., 2022). For instance, Wang et al. (2016) observed that microbial properties strongly affected Rm while Q₁₀ was controlled by substrate quality. Rm is an important process during soil microbial catabolism, so that factors that affect microbial activity would subsequently impact Rm. Soil temperature and water content directly or indirectly affect Rm through impacting microbial activities or changing substrate availability (Ma et al., 2019). Soil pH (Wong et al., 2008) and substrate availability (He et al., 2023) also exert significant effects on Rm by influencing microbial abundance, activity or community composition. Q₁₀ may be affected by multiple factors including substrate quality, mineral protection of SOC and microbial properties (Dash et al., 2019). According to the C quality-temperature hypothesis, substrate quality is considered as one of the major drivers in regulating Q₁₀ (Liu et al., 2021). The decomposition of low-quality C substrates requires high activation energy, so that is more sensitive to changes in temperature (Lefèvre et al., 2014). Although many findings are consistent with C quality-temperature hypothesis, cumulative evidence shows that mineral protection would attenuate Q₁₀ by limiting substrate availability (Gentsch et al., 2018). On one hand, minerals promote the formation of soil aggregates, which weaken Q₁₀ through limiting the accessibility of substrates to microorganisms or extracellular enzymes (Qin et al., 2019). On the other hand, SOC can be absorbed to mineral surface by covalent bonding or electrostatic bonding, so that its decomposition and in turn Q₁₀ would decline (Porras et al., 2017). Microbial physiologic characteristics, community structure and composition also affect Q₁₀ (Walker et al., 2018). For example, the Q₁₀ values increased with a higher proportion of K-selected microbial communities (Li et al., 2021), while microbial diversity was found to negatively impact Q₁₀ (Qin et al., 2021).

PSD significantly affects a range of soil biotic and abiotic factors (Luo et al., 2019) (See Supplementary Materials, Fig. S1). Many studies have shown that SOC and Rm would be enhanced by increasing PSD, since high PSD promotes detritus inputs via stimulating aboveground and underground plant productivity (Lange et al., 2015; Chen et al., 2019a). Meanwhile, PSD directly or indirectly affects soil microbial properties and Rm by altering the chemical properties of plant detritus inputs (Cotrufo et al., 2015). Since the detritus composition and quality differ among plant species, they would subsequently change the level and stability of SOC and microbial features (Jewell et al., 2017) (Fig. S1). More nutrients are needed to satisfy plant nutrient demand owing to stimulated plant productivity under higher PSD, so that plant would invest more resources to enhance root biomass to acquire more nutrients including calcium (Ca) and magnesium (Mg) from deeper soil with the nutrients eventually returning to top soil layer through litter inputs (Furey and Tilman, 2021). Meanwhile, greater root biomass would be accompanied by more organic acid release, so that increase soil calcium and other minerals via promoting bedrock weathering (Beugnon et al., 2021). Minerals such as iron (Fe), aluminum (Al), Ca or Mg can absorb SOC and form mineral-organic associations, which may contribute to SOC stabilization and in turn restrain Rm and Q₁₀ (McGrath et al., 2022) (Fig. S1). The alteration in soil minerals by PSD may affect soil moisture and pH that are crucial factors affecting Rm and Q₁₀ (Wu et al., 2020) (Fig. S1). However, though quite a few studies have determined the effects of PSD on Rm (Chen and Chen, 2019), relatively few studies have explored the effect of PSD on Q₁₀ (Luan et al., 2018). Luan et al. (2018) reported that increasing PSD suppressed Q₁₀ in temperate forests, but the underlying mechanisms were not explored. Considering that increasing PSD is an effective way to enhance SOC accumulation during vegetation restoration or afforestation, knowledge about how increasing PSD alters the temperature sensitivity of SOC decomposition is urgently needed under the background of climate change.

Natural PSD gradients in mature forests have often been used to explore the impacts of increasing PSD on ecosystem function and process (Qian et al., 2023; Zhu et al., 2023). In the current study, 43 plots covering a natural gradient of PSD were selected in a subtropical karst forest in south-west China (Qian et al., 2023; Zhu et al., 2023) to explore the effects of increasing PSD on Rm and Q₁₀. The major objectives were to address: 1) how Rm and Q₁₀ respond to increasing PSD; 2) what mechanisms underline the effects of PSD on Rm and Q₁₀.

2 Materials and methods

2.1 Experimental design and sample collection

This study was carried out in Mulun National Nature Reserve (25°06′09″−25°12′25″ N, 107°53′29″−108°05′45″ E), southwest China. The region is located in the subtropical monsoon climate zone with a mean annual temperature of 19°C and mean annual precipitation of 1389 mm (Zhu et al., 2023). The selected forest is a subtropical karst evergreen and deciduous broad-leafed forest with the underlain bedrock being a mixture of limestone and dolomite. The soil is calcareous with soil types being Cambisols, Luvisols, or Leptosols depending on topographic positions (Zhu et al., 2023). Forty-five plots with an area of 20 m × 20 m each were established in the valley and lower slope with the elevation ranging from 446 m to 521 m (See Supplementary Materials, Fig. S2) and soil type being Luvisols (Zhu et al., 2023). The interval between any two adjacent plots is 40 m. All the plants with a diameter at the breast height greater than 1 cm in each plot were measured, labeled and recorded. Shannon-Weiner index was calculated to represent PSD, which ranged from 0.15 to 3.53. Detailed information of the dominant plant species in each plot is presented in Supplementary Data 1.

Field sampling was carried out between July 28 and August 1, 2020. In each plot, 16 mineral soil samples were randomly collected with a soil corer (5 cm in inner diameter) to a depth of 10 cm after removing the surface organic matter. The soil samples in each plot were thoroughly mixed into one composite sample and sieved to 2 mm with stones and plant residues removed. Each composite sample was divided into three parts. One part was stored at 4°C for the determination of Rm, Q₁₀, dissolved organic C (DOC). The second part was stored at −40°C for measuring microbial properties. The third part was air-dried to analyze physicochemical variables, including soil pH, texture, SOC, exchangeable Ca, exchangeable Mg exchangeable Fe, exchangeable Al. It should be noted that only 43 plots were included due to soil missing in the current study.

2.2 Determination of soil microbial respiration and its temperature sensitivity

Fresh soil samples of 12 g each (dry weight equivalent) were weighted into 125 mL glass jars with two replicates per sample. The incubation was conducted in a biochemical incubator (LRH-150F, Shanghai Daohan Industry Co., Ltd, Shanghai, China) with the temperature being adjusted manually. Each jar was covered with Parafilm^® to prevent evaporation after the soil moisture was adjusted to 60% water holding capacity (WHC), and the soils were pre-incubated at 25°C under dark conditions for 7 days. A scheme of changing temperatures was adopted to determine soil microbial respiration and its temperature sensitivity (Liu et al., 2017; Liu et al., 2019; Liu et al., 2021). The incubation temperature was changed from 15°C to 35°C and then down to 15°C with a changing step of 5°C, i.e., 15°C – 20°C – 25°C – 30°C – 35°C – 30°C – 25°C – 20°C – 15°C. When reaching a new temperature, an equilibration period of 3 h was applied to allow soil microbes to adapt to the new temperature (Ding et al., 2016). Soil moisture was regularly checked and adjusted if necessary, during the incubation period. During the equilibration period of 3 h, each jar was covered with Parafilm^® to let air exchange between the headspace and the ambient atmosphere but reduce evaporation. Upon the end of equilibration period, each jar was sealed with an air-tight lid with a rubber septum for the collection of headspace gas. Twenty ml of laboratory air was immediately injected to the headspace of each jar and mixed well using a 60-mL syringe, followed by 20 mL headspace air being collected and stored in a 12-mL vacuumed vial (839W, Labco, England). A second headspace gas sample was collected from each jar after 18 h, 12 h, 8 h, 3 h, and 1 h following the collection of the first sample for the incubation temperature of 15°C, 20°C, 25°C, 30°C, and 35°C, respectively. The air-tight lid was replaced by the Parafilm^® after the second headspace gas collection, followed by a new equilibration period under another incubation temperature. The experiment only lasted for one round of incubation with changing temperature (~5 days). The sealed incubation period was determined based on a preliminary experiment to avoid the CO₂ concentration in the jar from exceeding 0.3% (Jewell et al., 2017). The lips were replaced by Parafilm^® again after each Rm determination. CO₂ concentrations were analyzed using an Agilent 7890A gas chromatograph equipped with a thermal conductivity detector (Agilent Technologies, Santa Clara, CA, USA). The soil microbial respiration (Rm, μg C·g⁻¹ soil·h⁻¹) was calculated using Eq. (1):

(1)R{m}_{}=\frac{M}{22.4}\frac{P}{P_0}\frac{T_0}{T}\frac{\mathrm{\Delta }C}{\mathrm{\Delta }t}\frac{V}{m},

where M is the molar mass of C (g·mol⁻¹); 22.4 is the molar mass of gas in the standard conditions (273 K, 1013 hPa); T₀ and P₀ are the air temperature (K) and pressure (hPa) under standard conditions, respectively; T and P are the determined air temperature (K) and pressure (hPa), respectively; ΔC and Δt are the changes of CO₂ concentrations (ppm) and time (h), respectively, between the two sampling time points for each Rm determination; V is the headspace volume of jar (L); and m is the mass of dry soil (g). Since soil microbial respiration has been found to increase up to a threshold of ~25°C across all non-desert biomes (Carey et al., 2016), microbial respiration under 25°C was used to assess the impact of increasing PSD on Rm. Similarly, the respiration under 20°C or 25°C from incubation with changing temperatures has been used to assess Rm variation or response to environmental change (Wang et al., 2016).

The exponential function was used to fit the correlation of Rm with temperature (R² > 0.95), and Q₁₀ was calculated using Eqs. (2) and (3):

(2)R{m}_{}=B{e}^{k^T},

(3)Q_{10}={\mathit{e}}^{10k},

where T is temperature (°C); and B and k are model parameters.

2.3 Measurements of auxiliary variables

Litter, root and soil physicochemical properties were determined using methods described in companion studies (Duan et al., 2023; Zhu et al., 2023) (See Supplementary Materials, Table S1). To investigate the relationship between Rm or Q₁₀ and mineral protection, we calculated the clay to SOC content ratio (Clay/SOC) to evaluate how clay particles contribute to SOC protection (Fang et al., 2021; Duan et al., 2023).

The functional group composition of SOC was determined using a Fourier transform infrared spectrometer (Nicolet is50, Thermo Fisher, USA). Samples were first dried under 60°C until completely dry, then ground to a fine power. Spectra were recorded by averaging 40 scans at 4 cm⁻¹ resolution over the range of 4000 to 400 cm⁻¹. Specifically, polysaccharides (Poly), phenolic and aliphatic (Ali), and aromatics and aromatic or aliphatic carboxylates (Aro) were represented by the absorption bands at 950–1170 cm⁻¹ (1033 cm⁻¹), 1420 cm⁻¹ and 1630 cm⁻¹, respectively. The relative peak ratios of 1630/1033 (Aro/Poly) and 1420/1033 (Ali/Poly) were used as recalcitrance indices of SOC (Wang et al., 2016; Qin et al., 2021), with greater ratios implying higher recalcitrance.

Microbial abundance and community composition were assessed by phospholipid fatty acids (PLFAs). Details of PLFAs assay are presented in a companion study (Li et al., 2023). The F/B ratio represent fungal-to-bacterial biomass ratio.

2.4 Statistical analysis

The normality of the data was checked using Shapiro-Wilk test, and logarithmical transformation was applied if necessary. Correlation analyses were conducted to examine the relationships of Rm (the respiration at 25°C) or Q₁₀ with the measured biotic and abiotic variables. Random forest analysis was then conducted to identify the major variables affecting Rm and Q₁₀. To clarify the direct and indirect drivers of Rm or Q₁₀, the partial least squares path model (PLS-PM) was utilized. Prior to PLS-PM, all selected variables were standardized. To reduce collinearity among the predictor variables, principal component analysis (PCA) was conducted for substrate properties, mineral protection and microbial traits with the first component (PC1) was used for PLS-PM (See Supplementary Materials, Table S2). All the possible models based on the priori model (Fig. S1) were tested with the non-significant pathways removed. The statistical analyses were implemented in R software 4.2.2.

3 Results

Soil microbial respiration ranged from 0.12−0.59 μg C·g⁻¹ soil·h⁻¹, with an average of 0.30 ± 0.11 μg C·g⁻¹ soil·h⁻¹ (Fig. 1(a)). Q₁₀ ranged from 3.30 to 7.16, with a mean value of 4.87 ± 0.97 (Fig. 1(b)). Rm was significantly and positively correlated with PSD (P < 0.01) (Fig. 1(c)), but no significant correlation was found between Q₁₀ and PSD (Fig. 1(d)).

Pearson correlation analysis demonstrated that Rm was significantly and positively correlated with plant properties (litter C/P, litter N/P and fine root biomass), soil water content (SWC), substrate properties (SOC, DOC, Aro/Poly) and microbial biomass (total PLFAs, bacterial PLFAs and fungal PLFAs). In contrast, Rm exhibited negative correlations with Clay/SOC and F/B (Fig. 2(a)). Q₁₀ was positively correlated with pH, Ali/Poly, (Ca + Mg)_exe and microbial biomass (total PLFAs, bacterial PLFAs, and fungal PLFAs), but negatively correlated with (Fe + Al_)o (Fig. 2(b)). Random forest analysis revealed that Clay/SOC, F/B, SWC, SOC and total PLFAs were identified as the strong explanatory factors for Rm, with the total explanation being 48.59% (Fig. 3(a)). For Q₁₀, pH, F/B, fine root biomass, SOC were selected as the strong explanatory factors, with the total explanation being 25.02% (Fig. 3(b)).

According to the partial least squares path model, increasing PSD stimulated Rm via promoting SWC and total PLFAs but suppressing F/B, owing to increased substrate level caused by improved fine root biomass but lowered Clay/SOC (Fig. 4(a)). The total effects of PSD, fine root biomass, Clay/SOC, substrate properties, SWC and microbial traits were 0.43, 0.15, −0.48, 0.64, 0.46, and 0.38, respectively (Fig. 4(b)). Increasing PSD had neutral effect on Q₁₀ because of the contrasting effects of soil biotic and abiotic variables. On one hand, increasing PSD suppressed Q₁₀ via decreasing F/B owing to increased subtrate level caused by promoted fine root biomass and mineral protection (Fig. 4(c)). On the other hand, increasing PSD stimulated Q₁₀ by enhancing soil pH through elevating (Ca + Mg)_exe (Fig. 4(c)). The total effects of PSD, fine root biomass, mineral protection, substrate properties, pH and F/B were 0.15, −0.04, 0.28, −0.10, 0.58 and −0.23, respectively (Fig. 4(d)). The partial least squares path models explained 58% and 37% of the variance in Rm and Q₁₀, respectively (Figs. 4(b) and 4(d)).

4 Discussion

4.1 Increasing plant species diversity stimulates soil microbial respiration

The current study shows that increasing PSD significantly stimulated Rm. Consistently, Rm was found to increase as PSD increased (Chen et al., 2019a), but decrease when PSD lost (Chen and Chen, 2019). Rm is usually influenced by soil microbiome, substrate quantity and quality, mineral protection and environmental factors (Sáez-Sandino et al., 2023). These are applicable to the present study. The stimulated input of plant residues or root exudates under higher PSD leads to greater levels of substrate quantity (Chen et al., 2019b; Fang et al., 2024). Though plant residue inputs were not determined in the current study, they were most likely stimulated as suggested by the increased fine root biomass under higher PSD. Higher substrate availability would benefit microbial growth and activity, and in turn stimulate microbial biomass and respiration (Prommer et al., 2020). This is corroborated by the current study. Additionally, the soils under higher PSD would have greater water holding capacity, which is positively correlated with soil organic matter (Li et al., 2007), and hence would have higher SWC. Relatively high SWC is necessary for maintaining microbial activity and Rm (Schimel, 2018). Consistently, both SWC and Rm were stimulated as PSD increased in the current study.

Soil microbiomes represent the ultimate actors in the decomposition of SOC with higher microbial biomass usually accompanied by great Rm under similar conditions (Sáez-Sandino et al., 2023). Additionally, carbon use strategies differ between fungi and bacteria, with fungi having a lower respiration quotient and a higher carbon use efficiency than bacteria (Soares and Rousk, 2019; Zhang et al., 2020). For example, Zhang et al. (2020) observed a negative correlation between F/B ratio and Rm in forest ecosystems. Some studies show that F/B ratio increases with PSD (Beugnon et al., 2021; Chen et al., 2019b). In contrast, F/B ratio decreased as PSD increased in the current study, likely owing to the increase of labile organic C (e.g., DOC), which favors the growth of bacteria (Huang et al., 2021). Therefore, the increase of microbial biomass and decrease of F/B can partly explain the stimulated Rm under higher PSD in the current study.

4.2 Increasing plant species diversity does not alter temperature sensitivity of microbial respiration

The current study demonstrates that increasing PSD had no significant effect on Q₁₀ due to the contrasting effects of soil biotic and abiotic variables. On one hand, increasing PSD stimulated Q₁₀ by enhancing soil pH through increasing exchangeable Ca and Mg. Two possible mechanisms exist for the increase of exchangeable Ca and Mg under higher PSD. First, increasing PSD stimulates the root investment to obtain nutrients including Ca and Mg from deep soil, and the nutrients would be returned to the top soil layer via detritus inputs (Furey and Tilman, 2021). In the current study, fine root biomass was significantly stimulated under higher PSD as reported by a companion study (Zhu et al., 2023). Second, the increase of fine root biomass usually stimulates release of low-molecular-weight organic acids, which subsequently participate in the weathering of primary minerals or bedrocks (a mixture of limestone and dolomite in the current study), so that increase the release of dissolve Ca and Mg (Qin et al., 2019; Beugnon et al., 2021). High concentrations of exchangeable Ca may contribute to the stabilization of SOC through inner or outer sphere interactions and benefit SOC accumulation (Rowley et al., 2018). As exchangeable Ca and Mg accumulate, the poorly crystalline Fe and Al minerals would be transformed to more crystalline phases and their reactivity accordingly decreases (Goldberg, 2014). As basic cations, the increase of soil exchangeable Ca and Mg would increase soil pH (Leiva Soto et al., 2023). The increased pH subsequently stimulated Q₁₀ in the current study, consistent with some previous researches (Ding et al., 2016; Liu et al., 2017). Although the direct linkage between soil pH and Q₁₀ has not be well explored, it is well known that microbial activity and community structure are regulated by soil pH (Rousk et al., 2010; Meyer et al., 2018). For example, some studies show that soil pH is the dominant and direct control on Q₁₀ probably owing to its effect on microbial activity and community structure (Min et al., 2014; Meyer et al., 2018). Nevertheless, both positive (Min et al., 2014; Ding et al., 2016; Liu et al., 2017; Komarova et al., 2022) and negative (Min et al., 2014; Meyer et al., 2018) effects of soil pH on Q₁₀ have been observed likely caused by the differential effects of soil pH on microbial activity and structure under different soil conditions. The mechanism underlying the positive effect of soil pH on Q₁₀ deserve further investigation.

On the other hand, we find that PSD suppressed Q₁₀ via decreasing F/B ratio and increasing SOC quantity and recalcitrance. According to the C quality-temperature hypothesis, Q₁₀ should increase with substrate recalcitrance (Jewell et al., 2017; Wang et al., 2018). With regard to the current study, SOC recalcitrance may have increased under higher PSD according to the increased ratio of aliphatics/polysaccharides (Wang et al., 2016). Consistent with the C quality-temperature hypothesis, significantly positive correlation was observed between the ratio of aliphatics/polysaccharides and Q₁₀ (Fig. 2(b)). Similarly, Wang et al. (2018) found that Q₁₀ increased with indices of SOC recalcitrance in coniferous forests. Although the recalcitrance increased with PSD, labile C fraction as indexed by DOC also increased with PSD in the current study (See Supplementary Materials, Fig. S3). The increase in labile C availability with PSD could shift microbial community composition toward bacterial dominance, as bacteria preferentially utilize labile substrates, thereby reducing the F/B ratio (Huang et al., 2021). Given that fungi are the primary decomposers of recalcitrant C (Fontaine et al., 2011; Ma et al., 2024), a lower F/B ratio may reduce the microbial capacity to utilize recalcitrant C pools. This shift in decomposition pathways could subsequently lower Q₁₀ of soil organic matter decomposition, as recalcitrant C typically exhibits higher Q₁₀ values due to its greater activation energy requirements for breakdown (Li et al., 2021; Pei et al., 2024). In summary, our study explored the effects of PSD on Rm and its temperature sensitivity in a subtropical karst forest with calcareous soil. Increasing PSD stimulated Rm by increasing substrate quantity, microbial abundance and SWC but decreasing F/B. Nevertheless, increasing PSD had no significant effect on Q₁₀ due to the contrasting effects from soil biotic and abiotic variables, i.e., stimulating Q₁₀ by increasing soil pH, but suppressing Q₁₀ via decreasing F/B. These findings suggest that increasing PSD would stimulate microbial respiration along with soil organic carbon accumulation, but not alter the carbon cycle-climate feedback when implementing ecological restoration or afforestation. Additionally, our study, for the first time, provides the mechanism underlying the response of temperature sensitivity of microbial respiration to PSD, which should be considered when assessing the impacts of PSD on soil organic carbon dynamics under climate change.

References

[1] Beugnon R, Du J, Cesarz S, Jurburg S D, Pang Z, Singavarapu B, Wubet T, Xue K, Wang Y, Eisenhauer N (2021). Tree diversity and soil chemical properties drive the linkages between soil microbial community and ecosystem functioning.ISME Commun, 1(1): 41

[2] Bradford M A, Wieder W R, Bonan G B, Fierer N, Raymond P A, Crowther T W (2016). Managing uncertainty in soil carbon feedbacks to climate change.Nat Clim Chang, 6(8): 751–758

[3] Carey J C, Tang J, Templer P H, Kroeger K D, Crowther T W, Burton A J, Dukes J S, Emmett B, Frey S D, Heskel M A, Jiang L, Machmuller M B, Mohan J, Panetta A M, Reich P B, Reinsch S, Wang X, Allison S D, Bamminger C, Bridgham S, Collins S L, de Dato G, Eddy W C, Enquist B J, Estiarte M, Harte J, Henderson A, Johnson B R, Larsen K S, Luo Y, Marhan S, Melillo J M, Peñuelas J, Pfeifer-Meister L, Poll C, Rastetter E, Reinmann A B, Reynolds L L, Schmidt I K, Shaver G R, Strong A L, Suseela V, Tietema A (2016). Temperature response of soil respiration largely unaltered with experimental warming.Proc Natl Acad Sci USA, 113(48): 13797–13802

[4] Chen C, Chen H Y H, Chen X, Huang Z (2019a). Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration.Nat Commun, 10(1): 1332

[5] Chen L, Xiang W, Wu H, Ouyang S, Zhou B, Zeng Y, Chen Y, Kuzyakov Y (2019b). Tree species identity surpasses richness in affecting soil microbial richness and community composition in subtropical forests.Soil Biol Biochem, 130: 113–121

[6] Chen S, Zhang M, Zou J, Hu Z (2022). Relationship between basal soil respiration and the temperature sensitivity of soil respiration and their key controlling factors across terrestrial ecosystems.J Soils Sediments, 22(3): 769–781

[7] Chen X, Chen H Y H (2019). Plant diversity loss reduces soil respiration across terrestrial ecosystems.Glob Change Biol, 25(4): 1482–1492

[8] Chen X, Taylor A R, Reich P B, Hisano M, Chen H Y H, Chang S X (2023). Tree diversity increases decadal forest soil carbon and nitrogen accrual.Nature, 618(7963): 94–101

[9] Cotrufo M F, Soong J L, Horton A J, Campbell E E, Haddix M L, Wall D H, Parton W J (2015). Formation of soil organic matter via biochemical and physical pathways of litter mass loss.Nat Geosci, 8(10): 776–779

[10] Dash P K, Bhattacharyya P, Roy K S, Neogi S, Nayak A K (2019). Environmental constraints’ sensitivity of soil organic carbon decomposition to temperature, management practices and climate change.Ecol Indic, 107: 105644

[11] Ding J, Chen L, Zhang B, Liu L, Yang G, Fang K, Chen Y, Li F, Kou D, Ji C, Luo Y, Yang Y (2016). Linking temperature sensitivity of soil CO₂ release to substrate, environmental, and microbial properties across alpine ecosystems.Global Biogeochem Cycles, 30(9): 1310–1323

[12] Duan P, Fu R, Nottingham A T, Domeignoz-Horta L A, Yang X, Du H, Wang K, Li D (2023). Tree species diversity increases soil microbial carbon use efficiency in a subtropical forest.Glob Change Biol, 29(24): 7131–7144

[13] Fang K, Chen L, Qin S, Zhang Q, Liu X, Chen P, Yang Y (2021). Mineral and climatic controls over soil organic matter stability across the Tibetan alpine permafrost region.Global Biogeochemical Cycles, 35(12): e2021GB007118

[14] Fang Y, He X, Gao K, Zhu Z, Wang K, Li D (2024). Increasing plant species diversity suppresses free-living N₂ fixation in litter and soil of a subtropical karst forest.Funct Ecol, 38(2): 391–402

[15] Fontaine S, Henault C, Aamor A, Bdioui N, Bloor J M G, Maire V, Mary B, Revaillot S, Maron P A (2011). Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect.Soil Biol Biochem, 43(1): 86–96

[16] Furey G N, Tilman D (2021). Plant biodiversity and the regeneration of soil fertility.Proc Natl Acad Sci USA, 118(49): e2111321118

[17] Gentsch N, Wild B, Mikutta R, Čapek P, Diáková K, Schrumpf M, Turner S, Minnich C, Schaarschmidt F, Shibistova O, Schnecker J, Urich T, Gittel A, Šantrůčková H, Bárta J, Lashchinskiy N, Fuß R, Richter A, Guggenberger G (2018). Temperature response of permafrost soil carbon is attenuated by mineral protection.Glob Change Biol, 24(8): 3401–3415

[18] Goldberg S (2014). Application of surface complexation models to anion adsorption by natural materials.Environ Toxicol Chem, 33(10): 2172–2180

[19] He Y, Zhou X, Jia Z, Zhou L, Chen H, Liu R, Du Z, Zhou G, Shao J, Ding J, Chen K, Hartley I P (2023). Apparent thermal acclimation of soil heterotrophic respiration mainly mediated by substrate availability.Glob Change Biol, 29(4): 1178–1187

[20] Huang R, Crowther T W, Sui Y, Sun B, Liang Y (2021). High stability and metabolic capacity of bacterial community promote the rapid reduction of easily decomposing carbon in soil.Commun Biol, 4(1): 1376

[21] Jewell M D, Shipley B, Low-Décarie E, Tobner C M, Paquette A, Messier C, Reich P B (2017). Partitioning the effect of composition and diversity of tree communities on leaf litter decomposition and soil respiration.Oikos, 126(7): 959–971

[22] Karhu K, Auffret M D, Dungait J A J, Hopkins D W, Prosser J I, Singh B K, Subke J A, Wookey P A, Ågren G I, Sebastià M T, Gouriveau F, Bergkvist G, Meir P, Nottingham A T, Salinas N, Hartley I P (2014). Temperature sensitivity of soil respiration rates enhanced by microbial community response.Nature, 513(7516): 81–84

[23] Komarova A, Ivashchenko K, Sushko S, Zhuravleva A, Vasenev V, Blagodatsky S (2022). Temperature sensitivity of topsoil organic matter decomposition does not depend on vegetation types in mountains.Plants, 11(20): 2765

[24] Lange M, Eisenhauer N, Sierra C A, Bessler H, Engels C, Griffiths R I, Mellado-Vázquez P G, Malik A A, Roy J, Scheu S, Steinbeiss S, Thomson B C, Trumbore S E, Gleixner G (2015). Plant diversity increases soil microbial activity and soil carbon storage.Nat Commun, 6(1): 6707

[25] Lefèvre R, Barré P, Moyano F E, Christensen B T, Bardoux G, Eglin T, Girardin C, Houot S, Kätterer T, van Oort F, Chenu C (2014). Higher temperature sensitivity for stable than for labile soil organic carbon – Evidence from incubations of long-term bare fallow soils.Glob Change Biol, 20(2): 633–640

[26] Leiva Soto A, Culman S W, Herms C, Sprunger C, Doohan D (2023). Managing soil acidity vs. soil Ca: Mg ratio: What is more important for crop productivity.Crop Forage Turfgrass Manage, 9(1): e20210

[27] Li D, Wang X, Mo J, Sheng G, Fu J (2007). Soil nitric oxide emissions from two subtropical humid forests in south China.J Geophys Res, 112(D23): 2007JD008680

[28] Li H, Yang S, Semenov M V, Yao F, Ye J, Bu R, Ma R, Lin J, Kurganova I, Wang X, Deng Y, Kravchenko I, Jiang Y, Kuzyakov Y (2021). Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community.Glob Change Biol, 27(12): 2763–2779

[29] Li Y, Qian Z, Li D (2023). Effects of tree diversity on soil microbial community in a subtropical forest in Southwest China.Eur J Soil Biol, 116: 103490

[30] Liu Y, He N, Xu L, Tian J, Gao Y, Zheng S, Wang Q, Wen X, Xu X, Yakov K (2019). A new incubation and measurement approach to estimate the temperature response of soil organic matter decomposition.Soil Biol Biochem, 138: 107596

[31] Liu Y, He N, Zhu J, Xu L, Yu G, Niu S, Sun X, Wen X (2017). Regional variation in the temperature sensitivity of soil organic matter decomposition in China’s forests and grasslands.Glob Change Biol, 23(8): 3393–3402

[32] Liu Y, Xu L, Zheng S, Chen Z, Cao Y, Wen X, He N (2021). Temperature sensitivity of soil microbial respiration in soils with lower substrate availability is enhanced more by labile carbon input.Soil Biol Biochem, 154: 108148

[33] Luan J, Liu S, Wang J, Chang S X, Liu X, Lu H, Wang Y (2018). Tree species diversity promotes soil carbon stability by depressing the temperature sensitivity of soil respiration in temperate forests.Sci Total Environ, 645: 623–629

[34] Luo Y H, Cadotte M W, Burgess K S, Liu J, Tan S L, Zou J Y, Xu K, Li D Z, Gao L M (2019). Greater than the sum of the parts: how the species composition in different forest strata influence ecosystem function.Ecol Lett, 22(9): 1449–1461

[35] Ma M, Zang Z, Xie Z, Chen Q, Xu W, Zhao C, Shen G (2019). Soil respiration of four forests along elevation gradient in northern subtropical China.Ecol Evol, 9(22): 12846–12857

[36] Ma Z, Jiao S, Zheng K, Ni H, Li D, Zhang N, Yang Y, Zhou J, Sun B, Liang Y (2024). Multiple spatial scales of bacterial and fungal structural and functional traits affect carbon mineralization.Mol Ecol, 33(3): e17235

[37] McGrath C R, Hicks Pries C E, Nguyen N, Glazer B, Lio S, Crow S E (2022). Minerals limit the deep soil respiration response to warming in a tropical Andisol.Biogeochemistry, 161(2): 85–99

[38] Meyer N, Welp G, Amelung W (2018). The temperature sensitivity (Q₁₀) of soil respiration: controlling factors and spatial prediction at regional scale based on environmental soil classes.Global Biogeochem Cycles, 32(2): 306–323

[39] Min K, Lehmeier C A, Ballantyne F, Tatarko A, Billings S A (2014). Differential effects of pH on temperature sensitivity of organic carbon and nitrogen decay.Soil Biol Biochem, 76: 193–200

[40] Niu B, Zhang X, Piao S, Janssens I A, Fu G, He Y, Zhang Y, Shi P, Dai E, Yu C, Zhang J, Yu G, Xu M, Wu J, Zhu L, Desai A R, Chen J, Bohrer G, Gough C M, Mammarella I, Varlagin A, Fares S, Zhao X, Li Y, Wang H, Ouyang Z (2021). Warming homogenizes apparent temperature sensitivity of ecosystem respiration.Sci Adv, 7(15): eabc7358

[41] Ontl T A, Janowiak M K, Swanston C W, Daley J, Handler S, Cornett M, Hagenbuch S, Handrick C, Mccarthy L, Patch N (2020). Forest management for carbon sequestration and climate adaptation.J For, 118(1): 86–101

[42] Pan Y, Birdsey R A, Fang J, Houghton R, Kauppi P E, Kurz W A, Phillips O L, Shvidenko A, Lewis S L, Canadell J G, Ciais P, Jackson R B, Pacala S W, McGuire A D, Piao S, Rautiainen A, Sitch S, Hayes D (2011). A large and persistent carbon sink in the world’s forests.Science, 333(6045): 988–993

[43] Pei J, Fang C, Li B, Nie M, Li J (2024). Direct evidence for microbial regulation of the temperature sensitivity of soil carbon decomposition.Glob Change Biol, 30(10): e17523

[44] Porras R C, Hicks Pries C E, McFarlane K J, Hanson P J, Torn M S (2017). Association with pedogenic iron and aluminum: effects on soil organic carbon storage and stability in four temperate forest soils.Biogeochemistry, 133(3): 333–345

[45] Prommer J, Walker T W N, Wanek W, Braun J, Zezula D, Hu Y, Hofhansl F, Richter A (2020). Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity.Glob Change Biol, 26: 669–681

[46] Qian Z, Li Y, Du H, Wang K, Li D (2023). Increasing plant species diversity enhances microbial necromass carbon content but does not alter its contribution to soil organic carbon pool in a subtropical forest.Soil Biol Biochem, 187: 109183

[47] Qin S, Chen L, Fang K, Zhang Q, Wang J, Liu F, Yu J, Yang Y (2019). Temperature sensitivity of SOM decomposition governed by aggregate protection and microbial communities.Sci Adv, 5(7): eaau1218

[48] Qin S, Kou D, Mao C, Chen Y, Chen L, Yang Y (2021). Temperature sensitivity of permafrost carbon release mediated by mineral and microbial properties.Sci Adv, 7(32): eabe3596

[49] Rousk J, Bååth E, Brookes P C, Lauber C L, Lozupone C, Caporaso J G, Knight R, Fierer N (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil.ISME J, 4(10): 1340–1351

[50] Rowley M C, Grand S, Verrecchia É P (2018). Calcium-mediated stabilisation of soil organic carbon.Biogeochemistry, 137: 27–49

[51] Sáez-Sandino T, García-Palacios P, Maestre F T, Plaza C, Guirado E, Singh B K, Wang J, Cano-Díaz C, Eisenhauer N, Gallardo A, Delgado-Baquerizo M (2023). The soil microbiome governs the response of microbial respiration to warming across the globe.Nat Clim Chang, 13(12): 1382–1387

[52] Schimel J P (2018). Life in dry soils: effects of drought on soil microbial communities and processes. Annual Review of Ecology, Evolution, and Systematics, 49: 409–432

[53] Soares M, Rousk J (2019). Microbial growth and carbon use efficiency in soil: links to fungal-bacterial dominance, SOC-quality and stoichiometry.Soil Biol Biochem, 131: 195–205

[54] Walker T W N, Kaiser C, Strasser F, Herbold C W, Leblans N I W, Woebken D, Janssens I A, Sigurdsson B D, Richter A (2018). Microbial temperature sensitivity and biomass change explain soil carbon loss with warming.Nat Clim Chang, 8(10): 885–889

[55] Wang Q, He N, Yu G, Gao Y, Wen X, Wang R, Koerner S E, Yu Q (2016). Soil microbial respiration rate and temperature sensitivity along a north-south forest transect in eastern China: patterns and influencing factors.J Geophys Res Biogeosci, 121(2): 399–410

[56] Wang Q, Liu S, Tian P (2018). Carbon quality and soil microbial property control the latitudinal pattern in temperature sensitivity of soil microbial respiration across Chinese forest ecosystems.Glob Change Biol, 24(7): 2841–2849

[57] Wong V N L, Dalal R C, Greene R S B (2008). Salinity and sodicity effects on respiration and microbial biomass of soil.Biol Fertil Soils, 44(7): 943–953

[58] Wu J, Zeng H, Zhao F, Chen C, Liu W, Yang B, Zhang W (2020). Recognizing the role of plant species composition in the modification of soil nutrients and water in rubber agroforestry systems.Sci Total Environ, 723: 138042

[59] Zhang Y, Zou J, Meng D, Dang S, Zhou J, Osborne B, Ren Y, Liang T, Yu K (2020). Effect of soil microorganisms and labile C availability on soil respiration in response to litter inputs in forest ecosystems: a meta-analysis.Ecol Evol, 10(24): 13602–13612

[60] Zhu Z, Du H, Gao K, Fang Y, Wang K, Zhu T, Zhu J, Cheng Y, Li D (2023). Plant species diversity enhances soil gross nitrogen transformations in a subtropical forest, southwest China.J Appl Ecol, 60(7): 1364–1375

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