整合分析增温和增CO2对土壤微生物的影响
付刚1, 张豪睿1,2, 李少伟1, 孙维1
1. 中国科学院地理科学与资源研究所生态系统网络观测与模拟重点实验室, 拉萨高原生态系统研究站,北京 100101
2. 中国科学院大学,北京 100049
摘要

土壤微生物在陆地生态系统碳氮循环中起着重要作用。气候变暖和CO2浓度增加是气候变化的两个重要方面。本研究整合分析了实验增温和CO2浓度增加对土壤微生物量和群落结构的影响。生态系统类型主要包括森林生态系统和草地生态系统。增温方法包括开顶式增温小室和热红外增温。增温时间有全天增温、白天增温和晚上增温。实验增温增加了土壤放线菌和腐生真菌,而CO2浓度增加减少了土壤革兰氏阳性细菌。实验增温对土壤革兰氏阴性细菌和总的磷脂脂肪酸量的影响随着年均温和年降水量的增加而减少。实验增温对土壤总的磷脂脂肪酸量、细菌含量、革兰氏阳性和阴性细菌的量的影响随着海拔的升高而增加。实验增温增加了草地生态系统的土壤总的磷脂脂肪酸量和放线菌含量,并增加了森林生态系统的土壤真菌和细菌的比值。开顶式增温小室增加了土壤革兰氏阴性细菌,而红外增温减少了土壤真菌和细菌的比值。白天增温增加了土壤革兰氏阴性细菌,而全天增温没有改变土壤革兰氏阴性细菌。因此,实验增温对土壤微生物的影响与生态系统类型、实验增温方法、增温时间、海拔和当地的气候条件有关。

关键词: 生态系统类型; CO2浓度增加; 增温; 响应比; 增温方法
A Meta-analysis of the Effects of Warming and Elevated CO2 on Soil Microbes
FU Gang1, ZHANG Haorui1,2, LI Shaowei1, SUN Wei1,*
1. Lhasa Plateau Ecosystem Research Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
*Corresponding author: SUN Wei, E-mail: wsun@igsnrr.ac.cn
Abstract

Soil microbes play important roles in terrestrial ecosystem carbon and nitrogen cycling. Climatic warming and elevated CO2are two aspects of climatic change. In this study, we used a meta-analysis approach to synthesise observations related to the effects of warming and elevated CO2on soil microbial biomass and community structure. Ecosystem types were mainly grouped into forests and grasslands. Warming methods included open top chambers and infrared radiators. Experimental settings included all-day warming, daytime warming and nighttime warming. Warming increased soil actinomycetes and saprotrophic fungi, while elevated CO2 decreased soil gram-positive bacteria (G+). Mean annual temperature and mean annual precipitation were negatively correlated with warming effects on gram-negative bacteria (G-) and total phospholipid fatty acid (PLFA), respectively. Elevation was positively correlated with the warming effect on total PLFA, bacteria, G+and G-. Grassland exhibited a positive response of total PLFA and actinomycetes to warming, while forest exhibited a positive response in the ratio of soil fungi to bacteria (F/B ratio) to warming. The open top chamber method increased G-, while the infrared radiator method decreased the F/B ratio. Daytime warming rather than all-day warming increased G-. Our findings indicated that the effects of warming on soil microbes differed with ecosystem types, warming methods, warming times, elevation and local climate conditions.

Keyword: ecosystem types; elevated CO2; increased temperature; response ratio; warming methods
1 Introduction

Soil microbes play important roles in terrestrial ecosystem carbon and nitrogen cycling (Zhou et al., 2012). There are several major soil microbial taxa, including fungi, gram- positive bacteria (G+), gram-negative bacteria (G-), actinomycetes, arbuscular mycorrhizal fungi (AMF), and saprotrophic fungi (SF). Most soil microbial biomass is composed of fungi and bacteria (Baath and Anderson, 2003). Different soil microbial taxa have different functions (Hu et al., 2001). Human activity has resulted in an increase in the atmospheric carbon dioxide (CO2) concentration and the global surface temperature has increased since the Industrial Revolution (IPCC, 2013). Elevated CO2 and warming will most likely alter soil microbial communities (Kanerva et al., 2008; Rinnan et al., 2007).

Phospholipid fatty acid (PLFA) analysis is one of the most commonly used methods to determine soil microbial community composition. Based on the PLFA analysis, soil fungi, total bacteria, G+, G-, actinomycetes, AMF, SF and other soil taxa can be determined (Bardgett, et al., 1996; Frostegard, et al., 1993). The change of soil total PLFA can reflect changes of soil microbial biomass for soil biota from all taxa (Zhang et al., 2014). The changes in soil fungi, total bacteria, G+, G-, actinomycetes, AMF and SF can be used to reflect the changes in soil microbial biomass for a specific taxon, respectively (Zhang et al., 2014). The changes in soil fungi to bacteria ratio (F/B ratio) and the ratio of G+to G- (G+/G- ratio) can be used to reflect the changes in soil microbial community structure (Fu and Shen, 2017b). Soil microbial taxa can have inconsistent responses to experimental warming with regard to ecosystem types and climatic conditions. Elevated temperature can either increase (Shen et al., 2014), decrease (Allison and Treseder, 2008; Ma et al., 2011) or have a negligible effect on soil fungi and bacteria (Liu et al., 2014; Schindlbacher et al., 2011). Elevated temperature can also have inconsistent effects on soil G+, G-, actinomycetes and AMF (Li et al., 2013; Rousk et al., 2013). Elevated temperature can increase (Zhang et al., 2004), reduce (Zhang et al., 2014) or have a negligible effect (Gutknecht et al., 2012; Zhang et al., 2013) on soil F/B ratio. Elevated temperature effects on the soil G+/G- ratio have been found to vary with landscape types, including increases in an alpine swamp meadow and forest ecosystem on the Tibetan Plateau, reductions in an alpine meadow and steppe on the Tibetan Plateau and a tundra ecosystem in the Changbai Mountain, and no obvious effect in a subarctic tundra (Rinnan et al., 2007; Wang et al., 2014; Zhang et al., 2014; Zhao et al., 2014).

There are inconsistent results on the relationship between warming duration and warming effects on soil microbial biomass, with either no relationship (Bai et al., 2013; Zhang et al., 2015) or a negative relationship (Blankinship et al., 2011). In addition, findings on the relationships between elevated CO2 duration and elevated CO2 effects on soil microbial biomass were also inconsistent, with either negative (Blankinship et al., 2011) or positive correlations (Ross et al., 2013). Several meta-analyses have indicated that soil microbial biomass in forest soils responded more strongly to warming than the microbial biomass in grassland soils (Bai et al., 2013; Lu et al., 2013), whereas Zhang et al. (2015) have found that microbial biomass in grassland soils responded more strongly to warming than that in forest soils. Therefore, it remains unclear whether treatment durations are related to treatment effects on soil microbes or whether soil microbial biomass in forest soils can respond more strongly to warming than microbial biomass in grassland soils.

To better understand these conflicting results, we compiled the data from 28 published warming and/or elevated CO2 studies related to soil microbial community composition derived from PLFA analyses. All of the 28 studies were based on field experiments. No previous meta-analyses have examined the relationship between the effect of warming on soil microbes and elevation. The main objectives of this study were to: 1) examine the general effects of warming or elevated CO2 on soil microbes; 2) test whether warming duration or warming magnitude can affect responses of soil microbes to warming; 3) check whether elevated CO2 duration or elevated CO2magnitude can influence responses of soil microbes to elevated CO2; and 4) investigate whether responses of soil microbes to warming can vary with ecosystem types or elevation.

2 Methods
2.1 Data compilation

The relevant articles published prior to 2017 were found using the Web of Science and the China National Knowledge Infrastructure. The compiled database included soil total PLFA, fungi, bacteria, G+, G-, actinomycetes, AMF, SF, the F/B ratio and the G+/G- ratio.

Our criteria for selecting relevant articles or subsets of data from articles included: 1) only field experimental studies were used; 2) for experiments with multiple factors, only the data from warming or elevated CO2treatments compared to a control were adopted; 3) at least one of the variables considered here was measured; 4) for experiments with multiple observations at different times from the same study site, only the latest results were adopted, considering that the observations included in the meta-analysis should be independent (Hedges et al., 1999); and (5) multiple soil depths, treatment magnitudes or ecosystem types were treated as independent variables.

We extracted the data (means, standard deviations or standard errors, and sample sizes) using the GetData software if the studies provided the data in figures (Fu and Shen, 2017c; Fu et al., 2015). Only one study analyzed the interactive effects of warming and elevated CO2 on the soil microbial community (Andresen et al., 2014). Therefore, we did not analyze the interactive effects of warming and elevated CO2.

All 28 studies were grouped according to ecosystem type, which included forest, grassland, shrubland and tundra ecosystems (Table 1). Experimental durations (i.e., from the beginning of warming or elevated CO2 treatment to the soil sampling time) were calculated in years. The main warming methods included open top chamber and infrared radiator. There were all-day warming, daytime warming and nighttime warming treatments in different studies. Warming magnitudes ranged from 0.1° C to 4° C (including 23 levels) and mean annual temperatures ranged from -7.3° C to 16.3° C. The increased CO2 concentrations ranged from 36 ppm to 360 ppm (including 8 levels). The elevated CO2 methods employed in the experiments included regular FACE techniques, greenhouses and open-top chambers.

Table 1 Basic information for the 28 studies included in the meta-analysis
2.2 Statistical analyses

We used the METAWIN 2.1 software (Sinauer Associates Inc., Sunderland, MA, USA) to perform this meta-analysis. We treated the natural logarithm of the response ratio (R) as the effect size (Hedges et al., 1999).

\[\ln R=\ln \left( \frac{{{{\bar{X}}}_{t}}}{{{{\bar{X}}}_{c}}} \right)=\ln \left( {{{\bar{X}}}_{t}} \right)-\ln \left( {{{\bar{X}}}_{c}} \right)\ (1)\]

where \(\overline{{{X}_{t}}}\) and \(\overline{{{X}_{c}}}\) are the mean values of the treatments and control, respectively.

We used the inverse of the pooled variance (\(1/v\)) as the weighting factor (\(w\)) for each study,

\[v=\frac{S_{t}
{2}}{{{n}_{t}}\overline{X_{t}
{2}}}+\frac{S_{c}
{2}}{{{n}_{c}}\overline{X_{c}
{2}}}\ (2)\]

where \({{n}_{t}}\) and \({{n}_{c}}\) are the sample sizes of the treatments and control, respectively; and \(S_{t}
{2}\) and \(S_{c}
{2}\)are the standard deviations of the treatments and control, respectively.

Then, we obtained the mean effect size (\(\ln \bar{R}\)) derived from all observations,

\[\ln \bar{R}=\frac{\sum\limits_{i=1}
{m}{{{w}_{i}}\ln {{R}_{i}}}}{\sum\limits_{i=1}
{m}{{{w}_{i}}}}\ (3)\]

where \(\ln {{R}_{i}}\) and \({{w}_{i}}\) are \(\text{ln}R\) and \(w\) of theith observation, respectively.

A fixed effects model was used to examine whether warming or elevated atmospheric CO2had a significant effect on each variable across all studies. Mean effect sizes were generated and 95% bias-corrected bootstrap confidence intervals (CI) were estimated. If the 95% bias- corrected bootstrap CI did not include zero, the response of the variable to warming or elevated atmospheric CO2was considered significant (Fu and Shen, 2017a). Both of the common rank correlation tests, Kendall's tau and Spearman Rank-Order correlation, for publication bias were performed, and all the rank correlations were non-significant. The mean effect size of each variable was transformed to the percentage change as \(({{e}
{\overline{\text{Lo}{{\text{g}}_{\text{e}}}R}}}-1)\times 100%\) (Fu and Shen, 2016).

We used a fixed effects model with a grouping variable to compare responses among vegetation types, warming times and warming methods. For a specific group, the mean effect size was calculated using only the data of that group. If the 95% bias-corrected bootstrap CI did not bracket zero for a specific group, the response of that specific variable to warming or elevated atmospheric CO2was considered significant.

We used a random effects model with a continuous variable (> 15 observations) to test the correlations of the effect sizes of warming or elevated CO2 with experimental duration or magnitude. If the regression coefficient (i.e., slope) was significant, then this independent variable could explain significantly the variation among the effect sizes of the treatments.

3 Results

Different soil microbe taxa may have different sensitivities to elevated temperature and CO2. Warming significantly increased soil actinomycetes by 11.1% and saprotrophic fungi by 13.8%, whereas warming did not significantly change soil total PLFA, fungi, bacteria, G+, G-, AMF, F/B ratio or G+/G- ratio (Fig. 1). Elevated CO2 only significantly decreased soil G+ by 6.6% (Fig. 2).

Fig. 1 Warming effects on soil microbial biomass
Note: G+: gram-positive bacteria, G-: gram-negative bacteria, F/B ratio: the ratio of soil fungi to bacteria, G+/G- ratio: the ratio of G+to G-, AMF: arbuscular mycorrhizal fungi, SF: saprotrophic fungi. The error bars indicate effect sizes and 95% bootstrap confidence intervals. The sample size for each variable is shown next to the bar.

Fig. 2 Elevated CO2 effects on soil microbial biomass
Note: Related descriptions as shown in Fig. 1.

Warming duration and magnitude were not correlated with warming effects on soil total PLFA, fungi, bacteria, G+, G-or F/B ratio (Table 2). Increased CO2 duration (QM = 1.20, p = 0.274, n = 17) and magnitude (QM = 0.74, p = 0.389, n = 17) were not correlated with elevated CO2 effects on soil total PLFA.

Table 2 Relationships between warming effects on soil microbial biomass and relevant variables

Mean annual air temperature and mean annual precipitation were negatively correlated with warming effect on soil G- and soil total PLFA, respectively (Table 2). Elevation was positively correlated with warming effect on soil total PLFA, bacteria, G+ and G-(Table 2).

Warming increased soil total PLFA by 29.5% and actinomycetes by 19.9% in grasslands, whereas soil total PLFA and actinomycetes in forests did not change under warming (Fig. 3). The OTC method increased G- by 19.3%, while the IR method did not affect G- (Fig. 4). The IR method decreased the F/B ratio by 6.8%, while the OTC method did not affect the F/B ratio (Fig. 4). Daytime warming increased G- by 10.7%, while all-day warming did not affect G- (Fig. 5).

Fig. 3 Warming effects on soil microbial biomass for (a) forest and (b) grassland
Note: Related descriptions as shown in Fig. 1.

Fig. 4 Effects of (a) infrared radiator and (b) open top chamber on soil microbial biomass
Note: Related descriptions as shown in Fig.1

Fig. 5 Effects of (a) all-day, (b) daytime and (c) nighttime warming on soil microbial biomass
Note: Related descriptions as shown in Fig. 1.

4 Discussion

Elevated CO2 may affect the soil microbial community considering the decrease in soil gram-positive bacteria (G+) found in our study, which was likely attributed to the following mechanisms. First, elevated CO2 generally increases ratios of soil carbon to nitrogen and litter carbon to nitrogen (de Graaff et al., 2006; Luo et al., 2006; Yang et al., 2011), while soil gram-positive bacteria decreases with increasing ratios of soil carbon to nitrogen and litter carbon to nitrogen (Huang et al., 2014; Lange et al., 2014). Second, elevated CO2 generally decreases soil nitrogen availability (de Graaff et al., 2006) and soil bacterial growth may be suppressed in nitrogen-limited systems (Hu et al., 2001).

Our findings implied that soil microbes might have stronger responses to warming in colder and drier areas, and the responses of soil microbes to warming increased with increasing elevation. These findings were in line with some previous studies (Chen et al., 2015; Zhang et al., 2015). Therefore, the temperature sensitivity of soil microbes may increase with increasing elevation, and decreasing temperature and water availability. Our findings were also in agreement with a previous meta-analysis which showed that daytime warming had a stronger positive effect on soil microbial abundance than all-day warming (Chen et al., 2015).

Our findings supported a previous study which showed that warming increased soil microbial biomass carbon and nitrogen in alpine grasslands but not in forests on the Tibetan Plateau (Zhang et al., 2015). This phenomenon may be attributed to the following mechanisms. First, the positive effects of warming on soil microbial total PLFA decreased with increasing mean annual precipitation (Table 2) and the grasslands had a lower mean annual precipitation than the forests in our meta-analysis (most < 800 mm vs. > 800 mm). Second, the positive effects of warming on soil microbial total PLFA increased with increasing elevation (Table 2) and the grasslands had a higher average elevation than the forests in our meta-analysis (3994 m vs. 2535 m). In addition, warming increased the F/B ratio by 16.4% in forests but not in grasslands (Fig.3). Therefore, forest and grassland soil microbes appear to have different sensitivities to elevated temperature.

Our findings also supported recent a meta-analysis which indicated that warming effects on soil microbial biomass varied between the OTC and IR methods (Chen, et al., 2015). The finding that warming effects on the F/B ratio varied between the OTC and IR methods can be attributed to the following mechanisms. First, the F/B ratio decreased with increasing soil nitrogen availability (Zhang et al., 2005), and the increased magnitude of soil nitrogen availability caused by the IR method was greater than that caused by the OTC method (Bai et al., 2013). Second, the IR and OTC methods resulted in different magnitudes of increases in plant belowground biomass and decreases in soil moisture (Lu et al., 2013), which in turn caused different changes in the soil F/B ratios between the IR and OTC methods (Gutknecht et al., 2012).

5 Conclusions

Warming increased soil actinomycetes and saprotrophic fungi, while elevated CO2 decreased soil gram-positive bacteria (G+). Mean annual temperature and mean annual precipitation were negatively correlated with the warming effect on gram-negative bacteria (G-) and total phospholipid fatty acid (PLFA), respectively. Elevation was positively correlated with the warming effect on total PLFA, bacteria, G+and G-. Grassland exhibited a positive response of total PLFA and actinomycetes to warming, while forest exhibited a positive response in the ratio of soil fungi to bacteria (F/B ratio) to warming. The open top chamber method increased G-, while the infrared radiator method decreased the F/B ratio. Daytime warming, rather than all-day warming, increased G-. Therefore, the sensitivities of soil microbial communities to warming varied with ecosystem types, warming methods and warming times. In colder and drier areas, soil microbial biomass appeared to have a higher temperature sensitivity. The temperature sensitivity of soil microbial biomass also increased with increasing elevation.

The authors have declared that no competing interests exist.

Reference
[1] Allison S D, Treseder K K. 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology, 14(12): 2898-2909. [Cited within:1]
[2] Andresen L C, Dungait J A J, Bol R, et al. 2014. Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland , traced with 13C-glycine and FACE CO2. PLoS ONE, 9(1): e85070. doi: 85010.81371/journal.pone.0085070. [Cited within:1]
[3] Baath E, Anderson T H. 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology & Biochemistry, 35(7): 955-963. [Cited within:1]
[4] Bai E, Li S L, Xu W H, et al. 2013. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytologist, 199(2): 441-451. [Cited within:3]
[5] Bardgett R D, Hobbs P J, Frostegard A1996. Changes in soil fungal: bacterial biomass ratios following reductions in the intensity of management of an upland grassland . Biology and Fertility of Soils, 22(3): 261-264. [Cited within:1]
[6] Blankinship J C, Niklaus P A, Hungate B A2011. A meta-analysis of responses of soil biota to global change. Oecologia, 165(3): 553-565. [Cited within:1]
[7] Chen J, Luo Y Q, Xia J Y, et al. 2015. Stronger warming effects on microbial abundances in colder regions. Scientific Reports, 5: 18032. [Cited within:3]
[8] de Graaff M A, van Groenigen K J, Six J, et al. 2006. Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta- analysis. Global Change Biology, 12(11): 2077-2091. [Cited within:2]
[9] Frostegard A, Tunlid A, Baath E. 1993. Phospholipid Fatty Acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Applied and Environmental Microbiology, 59(11): 3605-3617. [Cited within:1]
[10] Fu G, Shen Z X. 2016. Response of alpine plants to nitrogen addition on the Tibetan Plateau: A meta-analysis. Journal of Plant Growth Regulation, 35(4): 974-979. [Cited within:1]
[11] Fu G, Shen Z X. 2017 a. Effects of enhanced UV-B radiation on plant physiology and growth on the Tibetan Plateau: a meta-analysis. Acta Physiologiae Plantarum, 39(3): doi: DOI:10.1007/s11738-11017-12387-11738. [Cited within:1]
[12] Fu G, Shen Z X. 2017 b. Grazing alters soil microbial community in alpine grassland s of the Northern Tibet. Acta Aprataculturae Sinica, 26(10): 170-178. [Cited within:1]
[13] Fu G, Shen Z X. 2017c. Response of alpine soils to nitrogen addition on the Tibetan Plateau: A meta-analysis. Applied Soil Ecology, 114(99-104). [Cited within:1]
[14] Fu G, Shen Z X, Sun W, et al. 2015. A meta-analysis of the effects of experimental warming on plant physiology and growth on the Tibetan Plateau. Journal of Plant Growth Regulation, 34(1): 57-65. [Cited within:1]
[15] Gutknecht J L M, Field C B, Balser T C. 2012. Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Global Change Biology, 18(7): 2256-2269. [Cited within:2]
[16] Hedges L V, Gurevitch J, Curtis P S. 1999. The meta-analysis of response ratios in experimental ecology. Ecology, 80(4): 1150-1156. [Cited within:2]
[17] Hu S, Chapin F S, Firestone M K, et al. 2001. Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature, 409(6817): 188-191. [Cited within:2]
[18] Huang X M, Liu S R, Wang H, et al. 2014. Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China. Soil Biology & Biochemistry, 73: 42-48. [Cited within:1]
[19] IPCC. 2013. Summary for Policymakers. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker, T F, D Qin, G K Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P. M. Midgley (eds. )]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. [Cited within:1]
[20] Kanerva T, Palojarvi A, Ramo K, et al. 2008. Changes in soil microbial community structure under elevated tropospheric O3 and CO2. Soil Biology & Biochemistry, 40(10): 2502-2510. [Cited within:1]
[21] Lange M, Habekost M, Eisenhauer N, et al. 2014. Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland . PLoS ONE, 9(5): e96182. doi: 96110.91371/journal.pone.0096182. [Cited within:1]
[22] Li Q, Bai H H, Liang W J, et al. 2013. Nitrogen addition and warming independently influence the belowground micro-food web in a temperate steppe. PLoS ONE, 8(3): doi: DOI:10.1371/journal.pone.0060441. [Cited within:1]
[23] Liu Y, Li M, Zheng J W, et al. 2014. Short-term responses of microbial community and functioning to experimental CO2 enrichment and warming in a Chinese paddy field. Soil Biology & Biochemistry, 77: 58-68. [Cited within:1]
[24] Lu M, Zhou X H, Yang Q, et al. 2013. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology, 94(3): 726-738. [Cited within:2]
[25] Luo Y Q, Hui D F, Zhang D Q. 2006. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: A meta-analysis. Ecology, 87(1): 53-63. [Cited within:1]
[26] Ma L N, Lu X T, Liu Y, et al. 2011. The effects of warming and nitrogen addition on soil nitrogen cycling in a temperate grassland , Northeastern China. PLoS ONE, 6(11): e27645. doi: 27610.21371/journal.pone.0027645. [Cited within:1]
[27] Rinnan R, Michelsen A, Baath E, et al. 2007. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Global Change Biology, 13(1): 28-39. [Cited within:2]
[28] Ross D J, Newton P C D, Tate K R, et al. 2013. Impact of a low level of CO2 enrichment on soil carbon and nitrogen pools and mineralization rates over ten years in a seasonally dry, grazed pasture. Soil Biology & Biochemistry: 58(265-274). [Cited within:1]
[29] Rousk J, Smith A R, Jones D L. 2013. Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems. Global Change Biology, 19(12): 3872-3884. [Cited within:1]
[30] Schindlbacher A, Rodler A, Kuffner M, et al. 2011. Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biology & Biochemistry, 43(7): 1417-1425. [Cited within:1]
[31] Shen R C, Xu M, Chi Y G, et al. 2014. Soil microbial responses to experimental warming and nitrogen addition in a temperate steppe of Northern China. Pedosphere, 24(4): 427-436. [Cited within:1]
[32] Wang X J, Zhou Y M, Jiang X J, et al. 2014. Effects of warming on soil microbial community structure in Changbai Mountain tundra. Acta Ecologica Sinica, 34(20): 5706-5713. [Cited within:1]
[33] Yang Y, Luo Y, Lu M, et al. 2011. Terrestrial C: N stoichiometry in response to elevated CO2 and N addition: a synthesis of two meta-analyses. Plant and Soil, 343(1-2): 393-400. [Cited within:1]
[34] Zhang B, Chen S, He X, et al. 2014. Responses of soil microbial communities to experimental warming in alpine grassland s on the Qinghai-Tibet Plateau. PLoS ONE, 9(8): e103859. doi: DOI:10.810.101371/journal.pone.0103859. [Cited within:4]
[35] Zhang N, Liu W, Yang H, et al. 2013. Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling. Oecologia, 173(3): 1125-1142. [Cited within:1]
[36] Zhang W, Parker K M, Luo Y, et al. 2005. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Global Change Biology, 11(2): 266-277. [Cited within:1]
[37] Zhang W J, Xu Q, Wang X K, et al. 2004. Impacts of experimental atmospheric warming on soil microbial community structure in a tallgrass prairie. Acta Ecologica Sinica, 24(8): 1742-1747. [Cited within:1]
[38] Zhang X Z, Shen Z X, Fu G. 2015. A meta-analysis of the effects of experimental warming on soil carbon and nitrogen dynamics on the Tibetan Plateau. Applied Soil Ecology, 87: 32-38. [Cited within:3]
[39] Zhao C Z, Zhu L Y, Liang J, et al. 2014. Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in Eastern Tibetan Plateau, China. Plant and Soil, 382(1-2): 189-201. [Cited within:1]
[40] Zhou J Z, Xue K, Xie J P, et al. 2012. Microbial mediation of carbon- cycle feedbacks to climate warming. Nature Climate Change, 2(2): 106-110. [Cited within:1]