Ectomycorrhizal fungi slow soil carbon cycling

Respiration of soil organic carbon is one of the largest fluxes of CO₂ on earth. Understanding the processes that regulate soil respiration is critical for predicting future climate. Recent work has suggested that soil carbon respiration may be reduced by competition for nitrogen between symbiotic ectomycorrhizal fungi that associate with plant roots and free‐living microbial decomposers, which is consistent with increased soil carbon storage in ectomycorrhizal ecosystems globally. However, experimental tests of the mycorrhizal competition hypothesis are lacking. Here we show that ectomycorrhizal roots and hyphae decrease soil carbon respiration rates by up to 67% under field conditions in two separate field exclusion experiments, and this likely occurs via competition for soil nitrogen, an effect larger than 2 °C soil warming. These findings support mycorrhizal competition for nitrogen as an independent driver of soil carbon balance and demonstrate the need to understand microbial community interactions to predict ecosystem feedbacks to global climate.     

陆地生态系统土壤CO2排放对模拟增温的响应特征及影响因素

全球变暖已经成为不争的事实,陆地生态系统碳循环的研究受到了各界广泛关注,是当前全球变化研究中的重点。土壤CO₂排放是陆地生态系统与大气间二氧化碳交换的最大通量之一,当前陆地生态系统中土壤CO₂排放如何响应全球气候变暖及其影响因素仍不清楚,限制了对土壤碳循环过程及影响机制的深入认识。旨在明确全球变暖背景下陆地生态系统中土壤CO₂排放格局及影响因素。基于Web of Science、PubMed和中国知网等中英文期刊数据库,充分收集全球范围内的相关野外试验文献81篇,提取出65个研究位置和213组相关研究数据,采用Meta分析方法探讨陆地生态系统土壤CO₂排放对增温的响应特征,分析其与海拔、气候、土壤含水量、容重(BD)、pH、全氮(TN)和土壤有机碳(SOC)的相关关系。结果表明:陆地生态系统中土壤CO₂排放对增温整体有显著的正向响应,在农、林、草生态系统中,增温使土壤CO₂排放分别显著增加13.1%、18.0%、5.9% (P<0.05),森林生态系统对增温响应的正效应最强烈;增温能在短时期内促进土壤呼吸,但随着增温持续时间增加,土壤呼吸对温度的敏感性会降低,对温度变化产生适应性,从而使其对增温的响应能力减弱;响应特征受到环境因子、土壤特性以及其他试验条件等的影响,绝大多数条件下对增温表现出显著的正响应特征,不同影响因子之间共同作用、相互影响。增温通常能够改变植物生物量、土壤养分含量及微生物数量和活性,从而影响到植被根际呼吸和土壤呼吸速率。相关分析表明,海拔对土壤CO₂排放有显著负向影响,而年均气温、年均降水量、土壤含水量和仪器嵌入土壤深度则对土壤CO₂排放产生显著正向影响。这些结果对于理解全球土壤CO₂排放的时空变化格局有重要意义,也为准确评价全球变暖背景下土壤碳汇功能及其持续性提供理论依据。     

Development of ectomycorrhizas in model beech–spruce ecosystems on siliceous and calcareous soil: a 4-year experiment with atmospheric CO2 enrichment and nitrogen fertilization

To study responses of forests to global change, model ecosystems consisting of beech and spruce trees were established in open top chambers. The ecosystems were exposed to four conditions for 4 years, each replicated four times: ambient and elevated CO₂, and low and high nitrogen input. At the end of the trial, the trees were 6–8 years old. Each chamber contained two separate compartments with siliceous and calcareous soil. Here, we focus on the development of ectomycorrhizas in the topsoil layer. Ectomycorrhizal fungal biomass associated with the fine roots, estimated by using ergosterol content as a marker, was much higher in the siliceous compared to the richer calcareous soil. Also, in root-free soil samples, the level of ergosterol, indicative of the extraradical mycelium of ectomycorrhizal fungi as well as the mycelium of other fungi, was about six times higher in the siliceous than in the calcareous soil. Conditions of elevated atmospheric CO₂ primarily affected ectomycorrhizas in the calcareous soil. Fungal biomass, calculated per soil volume of the top soil layer, increased significantly, as did the metabolic activity of the ectomycorrhizal fungi, measured as uptake of glucose and synthesis of trehalose. Conditions of nitrogen fertilization affected ectomycorrhizas in the siliceous, nutrient poor soil.     

Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas

Forests play a critical role in the global carbon cycle, being considered an important and continuing carbon sink. However, the response of carbon sequestration in forests to global climate change remains a major uncertainty, with a particularly poor understanding of the origins and environmental responses of soil CO₂ efflux. For example, despite their large biomass, the contribution of ectomycorrhizal (EM) fungi to forest soil CO₂ efflux and responses to changes in environmental drivers has, to date, not been quantified in the field. Their activity is often simplistically included in the ‘autotrophic’ root respiration term. We set up a multiplexed continuous soil respiration measurement system in a young Lodgepole pine forest, using a mycorrhizal mesh collar design, to monitor the three main soil CO₂ efflux components: root, extraradical mycorrhizal hyphal, and soil heterotrophic respiration. Mycorrhizal hyphal respiration increased during the first month after collar insertion and thereafter remained remarkably stable. During autumn the soil CO₂ flux components could be divided into ∼60% soil heterotrophic, ∼25% EM hyphal, and ∼15% root fluxes. Thus the extraradical EM mycelium can contribute substantially more to soil CO₂ flux than do roots. While EM hyphal respiration responded strongly to reductions in soil moisture and appeared to be highly dependent on assimilate supply, it did not responded directly to changes in soil temperature. It was mainly the soil heterotrophic flux component that caused the commonly observed exponential relationship with temperature. Our results strongly suggest that accurate modelling of soil respiration, particularly in forest ecosystems, needs to explicitly consider the mycorrhizal mycelium and its dynamic response to specific environmental factors. Moreover, we propose that in forest ecosystems the mycorrhizal CO₂ flux component represents an overflow ‘CO₂ tap’ through which surplus plant carbon may be returned directly to the atmosphere, thus limiting expected carbon sequestration from trees under elevated CO₂.     

Fungal community composition and function after long‐term exposure of northern forests to elevated atmospheric CO2 and tropospheric O3

The long‐term effects of rising atmospheric carbon dioxide (CO₂) and tropospheric O₃ concentrations on fungal communities in soil are not well understood. Here, we examine fungal community composition and the activities of cellobiohydrolase and N‐acetylglucosaminidase (NAG) after 10 years of exposure to 1.5 times ambient levels of CO₂ and O₃ in aspen and aspen–birch forest ecosystems, and compare these results to earlier studies in the same long‐term experiment. The forest floor community was dominated by saprotrophic fungi, and differed slightly between plant community types, as did NAG activity. Elevated CO₂ and O₃ had small but significant effects on the distribution of fungal genotypes in this horizon, and elevated CO₂ also lead to an increase in the proportion of Sistotrema spp. within the community. Yet, although cellobiohydrolase activity was lower in the forest floor under elevated O₃, it was not affected by elevated CO₂. NAG was also unaffected. The soil community was dominated by ectomycorrhizal species. Both CO₂ and O₃ had a minor effect on the distribution of genotypes; however, phylogenetic analysis indicated that under elevated O₃Cortinarius and Inocybe spp. increased in abundance and Laccaria and Tomentella spp. declined. Although cellobiohydrolase activity in soil was unaffected by either CO₂ or O₃, NAG was higher (～29%) under CO₂ in aspen–birch, but lower (～18%) under aspen. Time series analysis indicated that CO₂ increased cellulolytic enzyme activity during the first 5 years of the experiment, but that the magnitude of this effect diminished over time. NAG activity also showed strong early stimulation by elevated CO₂, but after 10 years this effect is no longer evident. Elevated O₃ appears to have variable stimulatory and repressive effects depending on the soil horizon and time point examined.     

大气CO2浓度升高对土壤碳库稳定性的影响

工业革命以来,大气CO₂浓度持续上升,升高的CO₂浓度会改变植物光合产物积累、土壤碳库的碳输入和碳输出过程,进而通过影响有机碳组成和周转特征来调控土壤碳库动态变化。土壤碳库是陆地生态系统碳库的重要组成部分,其碳储量的微小变化都会对大气CO₂浓度和气候变化产生巨大影响。但目前关于CO₂浓度升高对土壤碳库动态和稳定性的影响还不清楚,很大程度上限制了预测陆地生态系统碳循环对气候变化的反馈。系统综述国内外大气CO₂浓度升高对植被生产力、植被碳输入和土壤碳库影响的研究进展,旨在揭示土壤碳库物理、化学组成以及周转特征对CO₂浓度升高的响应过程和机理,探讨CO₂升高情境下土壤微生物特征对土壤碳库稳定性的影响和驱动机制,为深入理解全球变化下的土壤碳循环特征提供理论支撑。     

连续三年夜间增温和施氮对云杉外生菌根及菌根真菌多样性的影响

以西南亚高山针叶林建群种粗枝云杉(Picea asperata)为研究对象,采用红外加热模拟增温结合外施氮肥(NH₄NO₃ 25 g N m^-2 a^-1)的方法,研究连续3a夜间增温和施肥对云杉幼苗外生菌根侵染率、土壤外生菌根真菌生物量及其群落多样性的影响。结果表明:夜间增温对云杉外生菌根侵染率的影响具有季节性及根级差异。夜间增温对春季(2011年5月)云杉1级根,夏季(2011年7月)和秋季(2010年10月)云杉2级根侵染率影响显著。除2011年7月1级根外,施氮对云杉1、2级根侵染率无显著影响。夜间增温对土壤中外生菌根真菌的生物量和群落多样性无显著影响,施氮及增温与施氮联合处理使土壤中外生菌根真菌生物量显著降低,但却提高了外生菌根真菌群落的多样性。这说明云杉幼苗外生菌根侵染率对温度较敏感,土壤外生菌根真菌生物量及其群落多样性对施氮较敏感。这为进一步研究该区域亚高山针叶林地下过程对全球气候变化的响应机制提供了科学依据。     

Growing season net ecosystem CO2 exchange of two desert ecosystems with alkaline soils in Kazakhstan

Central Asia is covered by vast desert ecosystems, and the majority of these ecosystems have alkaline soils. Their contribution to global net ecosystem CO₂ exchange (NEE) is of significance simply because of their immense spatial extent. Some of the latest research reported considerable abiotic CO₂ absorption by alkaline soil, but the rate of CO₂ absorption has been questioned by peer communities. To investigate the issue of carbon cycle in Central Asian desert ecosystems with alkaline soils, we have measured the NEE using eddy covariance (EC) method at two alkaline sites during growing season in Kazakhstan. The diurnal course of mean monthly NEE followed a clear sinusoidal pattern during growing season at both sites. Both sites showed significant net carbon uptake during daytime on sunny days with high photosynthetically active radiation (PAR) but net carbon loss at nighttime and on cloudy and rainy days. NEE has strong dependency on PAR and the response of NEE to precipitation resulted in an initial and significant carbon release to the atmosphere, similar to other ecosystems. These findings indicate that biotic processes dominated the carbon processes, and the contribution of abiotic carbon process to net ecosystem CO₂ exchange may be trivial in alkaline soil desert ecosystems over Central Asia.     

An evaluation of abiotic carbon sinks in deserts

Recent field studies have reported anomalous CO₂ uptake using eddy‐covariance techniques in arid and semiarid ecosystems. The rates of CO₂ uptake are incompatible with changes in situ of organic carbon pools. Here, I examine several potential mechanisms of abiotic CO₂ uptake in arid and semiarid soils: atmospheric pressure pumping, carbonate dissolution, and percolation of soil water through the vadose zone. Each mechanism is deemed inadequate to explain the observations of the eddy‐covariance systems, which must now be questioned for their accuracy in desert ecosystems.     

Elevated CO2 and O3 effects on ectomycorrhizal fungal root tip communities in consideration of a post-agricultural soil nutrient gradient legacy

Despite the critical role of EMF in nutrient and carbon (C) dynamics, combined effects of global atmospheric pollutants on ectomycorrhizal fungi (EMF) are unclear. Here, we present research on EMF root-level community responses to elevated CO₂ and O₃. We discovered that belowground EMF community richness and similarity were both negatively affected by CO₂ and O₃, but the effects of CO₂ and O₃ on EMF communities were contingent on a site soil pH and cation availability gradient. These results contrast with our previous work showing a strong direct effect of CO₂ and O₃ on sporocarp community dynamics and production. We discuss the possible role of carbon demand and allocation by EMF taxa in the discrepancy of these results. EMF communities were structured by a legacy of spatially defined soil properties, changing atmospheric chemistry and temporal dynamics. It is therefore necessary to understand global change impacts across multiple environmental gradients and spatiotemporal scales.     

中国农田生态系统土壤呼吸作用研究与展望

 农田生态系统是陆地生态系统的重要组成部分,占全球陆地面积的10.5%,其CO₂排放量占人为温室气体排放量的21%～25%;由于农田生态系统 受到强烈的人为干扰,因此农田生态系统土壤呼吸作用及其影响因素对准确评估陆地生态系统碳收支具有重要的意义。中国是个有悠久历史的 农业大国,不仅为农田土壤作用的研究提供了天然的实验室, 而且中国农田土壤呼吸作用的研究对全球的碳循环研究及碳收支准确评估具有非 常重要的示范与指导意义。该文综述了近10年来中国农田生态系统土壤呼吸作用研究进展,指出水热因子、作物生物学特性和农业管理活动是 造成中国农田生态系统土壤呼吸作用时空变异 的主要因素;作物根系呼吸作用占土壤作用的比例在13%～77.2%之间,存在极大的不确定性;合 理施肥、秸秆还田和免耕有助于农田生态系统土壤呼吸作用减排和固碳。指出了中国农田生态系统土壤呼吸作用拟重点加强不同区域典型农田 生态系统土壤呼吸作用的比较、空间异质性、影响因素模拟及减排对策等方面的研究。     

Carbon balance and allocation of assimilated CO2 in Scots pine, Norway spruce, and Silver birch seedlings determined with gas exchange measurements and 14C pulse labelling

Carbon dioxide is released from the soil to the atmosphere in heterotrophic respiration when the dead organic matter is used for substrates for soil micro-organisms and soil animals. Respiration of roots and mycorrhiza is another major source of carbon dioxide in soil CO₂ efflux. The partitioning of these two fluxes is essential for understanding the carbon balance of forest ecosystems and for modelling the carbon cycle within these ecosystems. In this study, we determined the carbon balance of three common tree species in boreal forest zone, Scots pine, Norway spruce, and Silver birch with gas exchange measurements conducted in laboratory in controlled temperature and light conditions. We also studied the allocation pattern of assimilated carbon with ¹⁴C pulse labelling experiment. The photosynthetic light responses of the tree species were substantially different. The maximum photosynthetic capacity (P _max) was 2.21 μg CO₂ s⁻¹ g⁻¹ in Scots pine, 1.22 μg CO₂ s⁻¹ g⁻¹ in Norway spruce and 3.01 μg CO₂ s⁻¹ g⁻¹ in Silver birch seedlings. According to the pulse labelling experiments, 43–75% of the assimilated carbon remained in the aboveground parts of the seedlings. The amount of carbon allocated to root and rhizosphere respiration was about 9–26%, and the amount of carbon allocated to root and ectomycorrhizal biomass about 13–21% of the total assimilated CO₂. The ¹⁴CO₂ pulse reached the root system within few hours after the labelling and most of the pulse had passed the root system after 48 h. The transport rate of carbon from shoot to roots was fastest in Silver birch seedlings.     

Using soil sensing technology to examine interactions and controls between ectomycorrhizal growth and environmental factors on soil CO2 dynamics

Soils play a critical role in the global carbon cycle, yet the biophysical factors regulating soil CO₂ dynamics remain unclear. We combined high-frequency in situ observations of fine roots and ectomycorrhizal (EM) fungi with data from multiple soil sensor arrays to examine the biophysical interactions influencing soil CO₂ production for one year in a mixed conifer forest. Using structural equation modeling we constructed a hypothesized model to test for causal interactions among environmental factors, biotic factors, and soil CO₂ dynamics throughout the soil profile. According to our model, seasonal variation in CO₂ production was significantly influenced by EM rhizomorph production, soil temperature, and soil moisture. Fine root production, on the other hand, did not appear to significantly influence soil CO₂ production. The relationship between EM rhizomorph production and soil CO₂ production was also supported by a zero temporal lag between these two measurements in a cross-correlation analysis. In contrast, CO₂ production increased before fine root production suggesting that these two measurements were decoupled in time. Results from this study highlight the need to better understand differences in carbon allocation between plant roots and EM fungi to improve our predictions of soil carbon dynamics under global climate change.     

The effect of fire on microbial biomass: a meta-analysis of field studies

Soil microbes regulate the transfer of carbon (C) from ecosystems to the atmosphere and in doing so influence feedbacks between terrestrial ecosystems and global climate change. Fire is one element of global change that may influence soil microbial communities and, in turn, their contribution to the C dynamics of ecosystems. In order to improve our understanding of how fire influences belowground communities, we conducted a meta-analysis of 42 published microbial responses to fire. We hypothesized that microbial biomass as a whole, and fungal biomass specifically, would be altered following fires. Across all studies, fire reduced microbial abundance by an average of 33.2% and fungal abundance by an average of 47.6%. However, microbial responses to fire differed significantly among biomes and fire types. For example, microbial biomass declined following fires in boreal and temperate forests but not following grasslands fires. In addition, wildfires lead to a greater reduction in microbial biomass than prescribed burns. These differences are likely attributable to differences in fire severity among biomes and fire types. Changes in microbial abundance were significantly correlated with changes in soil CO₂ emissions. Altogether, these results suggest that fires may significantly decrease microbial abundance, with corresponding consequences for soil CO₂ emissions.     

Production dynamics of Cenococcum geophilum ectomycorrhizas in response to long-term elevated CO2 and N fertilization

Ectomycorrhizal fungi are important in many forest ecosystems, yet their production dynamics and responses to environmental changes are poorly understood. Cenococcum geophilum is a common ectomycorrhizal fungus important to plant and forest soil biogeochemical cycles. The seasonal and inter-annual patterns of production and persistence of mycorrhizas formed by C. geophilum in a pine forest exposed to elevated atmospheric CO₂ and nitrogen fertilization were monitored using a 12 y minirhizotron dataset. Production of C. geophilum mycorrhizas was distinctly seasonal and peaked in late summer/autumn. Elevated CO₂ generally increased production while nitrogen fertilization strongly decreased production. Persistence times of C. geophilum mycorrhizas was ca. 2.7 y and was unaffected by CO₂ and nitrogen addition. Total production was greater in shallow soil (0–16 cm) but persistence was longer in deeper soil (17–32 cm). These observations provide insights into the autecology of C. geophilum and suggest that its tissues may be slow to decompose compared to other ectomycorrhizal species.     

Rapid carbon turnover beneath shrub and tree vegetation is associated with low soil carbon stocks at a subarctic treeline

Climate warming at high northern latitudes has caused substantial increases in plant productivity of tundra vegetation and an expansion of the range of deciduous shrub species. However significant the increase in carbon (C) contained within above‐ground shrub biomass, it is modest in comparison with the amount of C stored in the soil in tundra ecosystems. Here, we use a ‘space‐for‐time’ approach to test the hypothesis that a shift from lower‐productivity tundra heath to higher‐productivity deciduous shrub vegetation in the sub‐Arctic may lead to a loss of soil C that out‐weighs the increase in above‐ground shrub biomass. We further hypothesize that a shift from ericoid to ectomycorrhizal systems coincident with this vegetation change provides a mechanism for the loss of soil C. We sampled soil C stocks, soil surface CO₂ flux rates and fungal growth rates along replicated natural transitions from birch forest (Betula pubescens), through deciduous shrub tundra (Betula nana) to tundra heaths (Empetrum nigrum) near Abisko, Swedish Lapland. We demonstrate that organic horizon soil organic C (SOC_org) is significantly lower at shrub (2.98 ± 0.48 kg m^?2) and forest (2.04 ± 0.25 kg m^?2) plots than at heath plots (7.03 ± 0.79 kg m^?2). Shrub vegetation had the highest respiration rates, suggesting that despite higher rates of C assimilation, C turnover was also very high and less C is sequestered in the ecosystem. Growth rates of fungal hyphae increased across the transition from heath to shrub, suggesting that the action of ectomycorrhizal symbionts in the scavenging of organically bound nutrients is an important pathway by which soil C is made available to microbial degradation. The expansion of deciduous shrubs onto potentially vulnerable arctic soils with large stores of C could therefore represent a significant positive feedback to the climate system.     

Nitrogen deposition and carbon sequestration in alpine meadows

Nitrogen deposition experiments were carried out in alpine meadow ecosystems in Qinghai-Xizang Plateau in China, in order to explore the contribution of nitrogen deposition to carbon sequestration in alpine meadows. Two methods were used in this respect. First, we used the allocation of ¹⁵N tracer to soil and plant pools. Second, we used increased root biomass observed in the nitrogen-amended plots. Calculating enhanced carbon storage, we considered the net soil CO₂ emissions exposed to nitrogen deposition in alpine meadows. Our results show that nitrogen deposition can enhance the net soil CO₂ emissions, and thus offset part of carbon uptake by vegetation and soils. It means that we have to be cautious to draw a conclusion when we estimate the contribution of nitrogen deposition to carbon sequestration based on the partitioning of ¹⁵N tracer in terrestrial ecosystems, in particular in N-limited ecosystems. Even if we assess the contribution of nitrogen deposition to carbon sequestration based on increased biomass exposed to nitrogen deposition in terrestrial ecosystems, likewise, we have to consider the effects of nitrogen deposition on the soil CO₂ emissions.     

The microfood web of grassland soils responds to a moderate increase in atmospheric CO2

The response of the soil microfood web (microflora, nematodes) to a moderate increase in atmospheric CO₂ (+20%) was investigated by means of a free air CO₂ enrichment experiment. The study was carried out in a seminatural temperate grassland for a period of 4 consecutive years (1 year before fumigation commenced and 3 years with fumigation). Several soil biological parameters showed no change (microbial biomass, bacterial biomass) or decline (microbial respiration) in the first year of elevated CO₂ treatment as compared with controls. Each of these parameters were higher than controls, however, after 3 years of treatment. The relative abundance of predaceous nematodes also decreased in year 1 of the experiment, increased in year 2, but decreased again in year 3. In contrast, the relative abundance of root hair feeding nematodes, at first, increased under elevated CO₂ and then returned to the initial level again. Increased microbial biomass indicates enhanced C storage in the labile carbon pool of the active microfood web in subsequent years. According to measurements on the amounts of soil extractable C, changes in resource availability seem to be key to the response of the soil microfood web. We found a strong response of bacteria to elevated CO₂, while the fungal biomass remained largely unchanged. This contrasts to findings reported in the literature. We hypothesize that this may be because of contrasting effects of different levels of CO₂ enrichment on the microbial community (i.e. stimulation of bacteria at moderate levels and stimulation of fungi at high levels of CO₂ enrichment). However, various CO₂ effects observed in our study are similar in magnitude to those observed in other studies for a much higher level of atmospheric carbon. These include the particular sensitivity of predaceous nematodes and the long‐term increase of microbial respiration. Our findings confirm that the potential of terrestrial ecosystems to accumulate additional carbon might be lower than previously thought. Furthermore, CO₂‐induced changes of temperate grassland ecosystems might emerge much earlier than expected.     

Effects of elevated CO2 and nitrogen addition on soil organic carbon fractions in a subtropical forest

Aims

The aim of this study was to investigate the effects of elevated CO₂ concentration and nitrogen addition on soil organic carbon fractions in subtropical forests where the ambient N deposition was high.

Methods

Seedlings of typical subtropical forest ecosystems were transplanted in ten open-top chambers and grown under CO₂ and nitrogen treatments. The treatments included: 1) elevated CO₂ (700?μmol?mol^-1); 2) N addition of 100?kg NH₄NO₃ ha^-1?yr^-1; 3) combined elevated CO₂ and N addition; and 4) control. We measured soil total organic carbon (TOC), particulate organic carbon (POC), readily oxidizable organic carbon (ROC), and microbial biomass carbon (MBC).

Results

Results showed that elevated CO₂ alone did not significantly affect soil TOC, POC and ROC after 4?years of treatment, but increased soil MBC and soil respiration compared to the control. N addition alone had no significant effect neither on soil TOC, POC and ROC, but decreased MBC and soil respiration over time. However, the elevated CO₂ and N addition together significantly increased soil POC and ROC, and had no significant effect on soil MBC.

Conclusions

This study indicated that even in N-rich subtropical forest ecosystems, inputs of N are still needed in order to sustain soil C accumulation under elevated CO₂.