Divergent rhizosphere and non-rhizosphere soil microbial structure and function in long-term warmed steppe due to altered root exudation.

While there is an extensive body of research on the influence of climate warming on total soil microbial communities, our understanding of how rhizosphere and non-rhizosphere soil microorganisms respond to warming remains limited. To address this knowledge gap, we investigated the impact of 4 years of soil warming on the diversity and composition of microbial communities in the rhizosphere and non-rhizosphere soil of a temperate steppe, focusing on changes in root exudation rates and exudate compositions. We used open top chambers to simulate warming conditions, resulting in an average soil temperature increase of 1.1°C over a span of 4 years. Our results showed that, in the non-rhizosphere soil, warming had no significant impact on dissolved organic carbon concentrations, compositions, or the abundance of soil microbial functional genes related to carbon and nitrogen cycling. Moreover, soil microbial diversity and community composition remained largely unaffected, although warming resulted in increased complexity of soil bacteria and fungi in the non-rhizosphere soil. In contrast, warming resulted in a substantial decrease in root exudate carbon (by 19%) and nitrogen (by 12%) concentrations and induced changes in root exudate compositions, primarily characterized by a reduction in the abundance in alcohols, coenzymes and vitamins, and phenylpropanoids and polyketides. These changes in root exudation rates and exudate compositions resulted in significant shifts in rhizosphere soil microbial diversity and community composition, ultimately leading to a reduction in the complexity of rhizosphere bacterial and fungal community networks. Altered root exudation and rhizosphere microbial community composition therefore decreased the expression of functional genes related to soil carbon and nitrogen cycling. Interestingly, we found that changes in soil carbon-related genes were primarily driven by the fungal communities and their responses to warming, both in the rhizosphere and non-rhizosphere soil. The study of soil microbial structure and function in rhizosphere and non-rhizosphere soil provides an ideal setting for understanding mechanisms for governing rhizosphere and non-rhizosphere soil carbon and nitrogen cycles. Our results highlight the distinctly varied responses of soil microorganisms in the rhizosphere and non-rhizosphere soil to climate warming. This suggests the need for models to address these processes individually, enabling more accurate predictions of the impacts of climate change on terrestrial carbon cycling.

Microbial autotrophy explains large-scale soil CO2 fixation.

Microbial communities play critical roles in fixing carbon from the atmosphere and fixing it in the soils. However, the large-scale variations and drivers of these microbial communities remain poorly understood. Here, we conducted a large-scale survey across China and found that soil autotrophic organisms are critical for explaining CO2 fluxes from the atmosphere to soils. In particular, we showed that large-scale variations in CO2 fixation rates are highly correlated to those in autotrophic bacteria and phototrophic protists. Paddy soils, supporting a larger proportion of obligate bacterial and protist autotrophs, display four-fold of CO2 fixation rates over upland and forest soils. Precipitation and pH, together with key ecological clusters of autotrophic microbes, also played important roles in controlling CO2 fixation. Our work provides a novel quantification on the contribution of terrestrial autotrophic microbes to soil CO2 fixation processes at a large scale, with implications for global carbon regulation under climate change.

Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long-term warming.

Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mechanisms have been suggested to explain the long-term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-term warming, we sampled soils from 13- and 28-year-old soil warming experiments in different seasons. We performed short-term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in summer, when warming had exacerbated the seasonally-induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-term warming effects on these soils.

Microbial communities in terrestrial surface soils are not widely limited by carbon.

Microbial communities in soils are generally considered to be limited by carbon (C), which could be a crucial control for basic soil functions and responses of microbial heterotrophic metabolism to climate change. However, global soil microbial C limitation (MCL) has rarely been estimated and is poorly understood. Here, we predicted MCL, defined as limited availability of substrate C relative to nitrogen and/or phosphorus to meet microbial metabolic requirements, based on the thresholds of extracellular enzyme activity across 847 sites (2476 observations) representing global natural ecosystems. Results showed that only about 22% of global sites in terrestrial surface soils show relative C limitation in microbial community. This finding challenges the conventional hypothesis of ubiquitous C limitation for soil microbial metabolism. The limited geographic extent of C limitation in our study was mainly attributed to plant litter, rather than soil organic matter that has been processed by microbes, serving as the dominant C source for microbial acquisition. We also identified a significant latitudinal pattern of predicted MCL with larger C limitation at mid- to high latitudes, whereas this limitation was generally absent in the tropics. Moreover, MCL significantly constrained the rates of soil heterotrophic respiration, suggesting a potentially larger relative increase in respiration at mid- to high latitudes than low latitudes, if climate change increases primary productivity that alleviates MCL at higher latitudes. Our study provides the first global estimates of MCL, advancing our understanding of terrestrial C cycling and microbial metabolic feedback under global climate change.

Herbivory changes soil microbial communities and greenhouse gas fluxes in a high-latitude wetland.

Herbivory can have strong impacts on greenhouse gas fluxes in high-latitude ecosystems. For example, in the Yukon-Kuskokwim (Y-K) Delta in western Alaska, migratory goose grazing affects the magnitude of soil carbon dioxide (CO2) and methane (CH4) fluxes. However, the underlying drivers of this relationship are unclear, as few studies systematically tease apart the processes by which herbivores influences soil biogeochemistry. To examine these mechanisms in detail, we conducted a laboratory incubation experiment to quantify changes in greenhouse gas fluxes in response to three parameters altered by herbivores in situ: temperature, soil moisture content, and nutrient inputs. These treatments were applied to soils collected in grazing lawns and nearby ungrazed habitat, allowing us to assess how variation in microbial community structure influenced observed responses. We found pronounced differences in both fungal and prokaryotic community composition between grazed and ungrazed areas. In the laboratory incubation experiment, CO2 and CH4 fluxes increased with temperature, soil moisture, and goose fecal addition, suggesting that grazing-related changes in the soil abiotic environment may enhance soil C losses. Yet, these abiotic drivers were insufficient to explain variation in fluxes between soils with and without prior grazing. Differences in trace gas fluxes between grazed and ungrazed areas may result both from herbivore-induced shifts in abiotic parameters and grazing-related alterations in microbial community structure. Our findings suggest that relationships among herbivores and soil microbial communities could mediate carbon-climate feedbacks in rapidly changing high-latitude ecosystems.

Nitrogen-rich microbial products provide new organo-mineral associations for the stabilization of soil organic matter.

Understanding the cycling of C and N in soils is important for maintaining soil fertility while also decreasing greenhouse gas emissions, but much remains unknown about how organic matter (OM) is stabilized in soils. We used nano-scale secondary ion mass spectrometry (NanoSIMS) to investigate the changes in C and N in a Vertisol and an Alfisol incubated for 365 days with 13 C and 15 N pulse labeled lucerne (Medicago sativa L.) to discriminate new inputs of OM from the existing soil OM. We found that almost all OM within the free stable microaggregates of the soil was associated with mineral particles, emphasizing the importance of organo-mineral interactions for the stabilization of C. Of particular importance, it was also found that 15 N-rich microbial products originating from decomposition often sorbed directly to mineral surfaces not previously associated with OM. Thus, we have shown that N-rich microbial products preferentially attach to distinct areas of mineral surfaces compared to C-dominated moieties, demonstrating the ability of soils to store additional OM in newly formed organo-mineral associations on previously OM-free mineral surfaces. Furthermore, differences in 15 N enrichment were observed between the Vertisol and Alfisol presumably due to differences in mineralogy (smectite-dominated compared to kaolinite-dominated), demonstrating the importance of mineralogy in regulating the sorption of microbial products. Overall, our findings have important implications for the fundamental understanding of OM cycling in soils, including the immobilization and storage of N-rich compounds derived from microbial decomposition and subsequent N mineralization to sustain plant growth.

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 (SOCorg ) 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.

Limiting Resources Define the Global Pattern of Soil Microbial Carbon Use Efficiency.

Microbial carbon (C) use efficiency (CUE) delineates the proportion of organic C used by microorganisms for anabolism and ultimately influences the amount of C sequestered in soils. However, the key factors controlling CUE remain enigmatic, leading to considerable uncertainty in understanding soil C retention and predicting its responses to global change factors. Here, we investigate the global patterns of CUE estimate by stoichiometric modeling in surface soils of natural ecosystems, and examine its associations with temperature, precipitation, plant-derived C and soil nutrient availability. We found that CUE is determined by the most limiting resource among these four basic environmental resources within specific climate zones (i.e., tropical, temperate, arid, and cold zones). Higher CUE is common in arid and cold zones and corresponds to limitations in temperature, water, and plant-derived C input, while lower CUE is observed in tropical and temperate zones with widespread limitation of nutrients (e.g., nitrogen or phosphorus) in soil. The contrasting resource limitations among climate zones led to an apparent increase in CUE with increasing latitude. The resource-specific dependence of CUE implies that soils in high latitudes with arid and cold environments may retain less organic C in the future, as warming and increased precipitation can reduce CUE. In contrast, oligotrophic soils in low latitudes may increase organic C retention, as CUE could be increased with concurrent anthropogenic nutrient inputs. The findings underscore the importance of resource limitations for CUE and suggest asymmetric responses of organic C retention in soils across latitudes to global change factors.

Effects of livestock grazing on the relationships between soil microbial community and soil carbon in grassland ecosystems.

Livestock grazing of grassland ecosystems may induce shifts in microbe community traits and soil carbon (C) cycling; however, impacts of grassland management (grazing) on soil C- microbe community trait (microbial biomass, diversity, community structure, and enzyme activity) relationships are unclear. To address this, we conducted a global meta-analysis of 95 articles of livestock grazing studies that vary in grazing intensities (light, moderate, and high) and durations (<5 years, 5-10 years, and > 10 years). We found that gazing decreased soil organic carbon content (SOC; 10.1 %), and activities of the enzymes of saccharase (SA; 31.1 %), urease (UA; 7.0 %), and acid phosphatase (11.9 %) in topsoil. Meanwhile, the SOC, soil microbial biomass and enzyme activities consistently decreased as grazing intensity and duration prolonged. Furthermore, we observed strong linear relationships of microbe community traits with SOC (p < 0.05), but weak relationships with soil N or P (p > 0.05) in grasslands, which also depends on the grazing intensity and duration. In conclusion, our results indicate that traits of soil carbon content, soil microbe community, and in particular their relationships in global grasslands are overall significantly affected by livestock grazing, but the effects strongly depend on the grazing intensity and duration.

Global magnitude of rhizosphere effects on soil microbial communities and carbon cycling in natural terrestrial ecosystems.

The rhizosphere is one of the most dynamic interfaces on the Earth. Understanding the magnitudes of rhizosphere effects (RE, difference in bio-physicochemical properties between rhizosphere and bulk soils) on soil microbial communities and their moderators is important for studying on below-ground carbon (C) cycling. A comprehensive meta-analysis was conducted to quantify the REs on soil microbial biomass, community structure, respiration, and C-degrading enzymes. We found that REs on soil C and nutrients, total microbial biomass, the abundance of specific microbial groups, fungi to bacteria ratio, respiration, and C-degrading enzymes were positive, but the magnitudes were varied with biomes, plant functional types, and mycorrhizal types. REs on microbial biomass, respiration, and C-degrading enzymes increased with the increase of mean annual temperature and mean annual precipitation, but decreased with the increase of soil clay, C, nitrogen (N), and phosphorus (P) contents. The REs on microbial biomass and respiration also increased as the REs on soil C:N:P increased. Compared with bulk soil, per unit rhizosphere soil C supported more microbial biomass, per unit of which respired more C, leading to faster C decomposition in rhizosphere. Our findings indicate that the increase in microbial biomass, co-metabolism induced by labile and energy-rich organic C of root exudates, and overflow respiration induced by stoichiometric imbalance together contribute to the enhanced C decomposition in rhizosphere. The global pattern of REs on soil microbial communities is critical to revealing the plant-microbe-soil interactions in terrestrial ecosystems.

Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil.

Microorganisms that degrade cellulose utilize extracellular reactions that yield free by-products which can promote interactions with noncellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We performed comparative genomics with genome bins from a shotgun metagenomic-stable isotope probing experiment to characterize the attributes of cellulolytic and noncellulolytic taxa accessing 13C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits that limit access, while noncellulolytic taxa would display greater metabolic dependency, such as signatures of adaptive gene loss. We tested our hypotheses by evaluating genomic traits indicative of competitive exclusion or metabolic dependency, such as antibiotic production, growth rate, surface attachment, biomass degrading potential, and auxotrophy. The most 13C-enriched taxa were cellulolytic Cellvibrio (Gammaproteobacteria) and Chaetomium (Ascomycota), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria, demonstrating differences in dependency among cellulose degraders. Noncellulolytic taxa that accessed 13C from cellulose (Planctomycetales, Verrucomicrobia, and Vampirovibrionales) were also more dependent, as indicated by patterns of auxotrophy and 13C labeling (i.e., partial labeling or labeling at later stages). Major 13C-labeled cellulolytic microbes (e.g., Sorangium, Actinomycetales, Rhizobiales, and Caulobacteraceae) possessed adaptations for surface colonization (e.g., gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposing particulate organic matter. Our results demonstrated that access to cellulosic C was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion.IMPORTANCE Our study reveals the ecogenomic traits of microorganisms participating in the cellulose economy of soil. We identified three major categories of participants in this economy: (i) independent primary degraders, (ii) interdependent primary degraders, and (iii) secondary consumers (mutualists, opportunists, and parasites). Trade-offs between independent primary degraders, whose adaptations favor antagonism and competitive exclusion, and interdependent and secondary degraders, whose adaptations favor complex interspecies interactions, are expected to affect the fate of microbially processed carbon in soil. Our findings provide useful insights into the ecological relationships that govern one of the planet's most abundant resources of organic carbon. Furthermore, we demonstrate a novel gradient-resolved approach for stable isotope probing, which provides a cultivation-independent, genome-centric perspective into soil microbial processes.

Soil Bacterial and Fungal Richness Forecast Patterns of Early Pine Litter Decomposition.

Discovering widespread microbial processes that drive unexpected variation in carbon cycling may improve modeling and management of soil carbon (Prescott, 2010; Wieder et al., 2015a, 2018). A first step is to identify community features linked to carbon cycle variation. We addressed this challenge using an epidemiological approach with 206 soil communities decomposing Ponderosa pine litter in 618 microcosms. Carbon flow from litter decomposition was measured over a 6-week incubation. Cumulative CO2 from microbial respiration varied two-fold among microcosms and dissolved organic carbon (DOC) from litter decomposition varied five-fold, demonstrating large functional variation despite constant environmental conditions where strong selection is expected. To investigate microbial features driving DOC concentration, two microbial community cohorts were delineated as "high" and "low" DOC. For each cohort, communities from the original soils and from the final microcosm communities after the 6-week incubation with litter were taxonomically profiled. A logistic model including total biomass, fungal richness, and bacterial richness measured in the original soils or in the final microcosm communities predicted the DOC cohort with 72 (P < 0.05) and 80 (P < 0.001) percent accuracy, respectively. The strongest predictors of the DOC cohort were biomass and either fungal richness (in the original soils) or bacterial richness (in the final microcosm communities). Successful forecasting of functional patterns after lengthy community succession in a new environment reveals strong historical contingencies. Forecasting future community function is a key advance beyond correlation of functional variance with end-state community features. The importance of taxon richness-the same feature linked to carbon fate in gut microbiome studies-underscores the need for increased understanding of biotic mechanisms that can shape richness in microbial communities independent of physicochemical conditions.

[Investigation on effects of elevated atmospheric CO2 concentration on plant-soil system carbon cycling: Based on stable isotopic technique]. / åŸºäºŽç¨³å®šç¢³åŒä½ç´ æŠ€æœ¯ç ”ç©¶å¤§æ°”CO2浓度升高对植物-土壤系统碳循环的影响.

Elevated atmospheric CO2 affects plant photosynthesis process and biomass accumulation, furthermore alters the distribution of photosynthetic carbon (C) above- and below-ground. The formation and turnover of soil organic carbon (SOC) depends on the input of photosynthetic C, so the change of plant physiology and metabolism caused by increasing CO2 concentration will further affect the balance of SOC pool. Therefore, stable isotope 13C technique is powerful for clarifying the influence of elevated atmospheric CO2 on C cycling in plant-soil system, including the distribution of photosynthetic C among plant organs, and the transformation and accumulation of photosynthetic C in soil. This review summarized research focused on the effects of elevated atmospheric CO2 on C cycling in terrestrial ecosystems based on 13C natural abundance or 13C tracing technique, including: 1) isotopic fractionation effect in plant photosynthesis; 2) the distribution of photosynthetic C in plant organs; 3) the transformation and stabilization of photosynthetic C in SOC driven by microbial process. Clarifying the above processes and controlling mechanisms is essential to predict long-term influence of elevated CO2 on C cycling and evaluate the source-sink function of SOC in terrestrial ecosystems.

Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone.

We hypothesized that changes in plant growth resulting from atmospheric CO2 and O3 enrichment would alter the flow of C through soil food webs and that this effect would vary with tree species. To test this idea, we traced the course of C through the soil microbial community using soils from the free-air CO2 and O3 enrichment site in Rhinelander, Wisconsin. We added either 13C-labeled cellobiose or 13C-labeled N-acetylglucosamine to soils collected beneath ecologically distinct temperate trees exposed for 3 years to factorial CO2 (ambient and 200 µl l-1 above ambient) and O3 (ambient and 20 µl l-1 above ambient) treatments. For both labeled substrates, recovery of 13C in microbial respiration increased beneath plants grown under elevated CO2 by 29% compared to ambient; elevated O3 eliminated this effect. Production of 13C-CO2 from soils beneath aspen (Populus tremuloides Michx.) and aspen-birch (Betula papyrifera Marsh.) was greater than that beneath aspen-maple (Acer saccharum Marsh.). Phospholipid fatty acid analyses (13C-PLFAs) indicated that the microbial community beneath plants exposed to elevated CO2 metabolized more 13C-cellobiose, compared to the microbial community beneath plants exposed to the ambient condition. Recovery of 13C in PLFAs was an order of magnitude greater for N-acetylglucosamine-amended soil compared to cellobiose-amended soil, indicating that substrate type influenced microbial metabolism and soil C cycling. We found that elevated CO2 increased fungal activity and microbial metabolism of cellobiose, and that microbial processes under early-successional aspen and birch species were more strongly affected by CO2 and O3 enrichment than those under late-successional maple.