Soil contains more carbon than the atmosphere and vegetation combined. Understanding the mechanisms controlling the accumulation and stability of soil carbon is critical to predicting the Earth's ...future climate. Recent studies suggest that decomposition of soil organic matter is often limited by nitrogen availability to microbes and that plants, via their fungal symbionts, compete directly with free-living decomposers for nitrogen. Ectomycorrhizal and ericoid mycorrhizal (EEM) fungi produce nitrogen-degrading enzymes, allowing them greater access to organic nitrogen sources than arbuscular mycorrhizal (AM) fungi. This leads to the theoretical prediction that soil carbon storage is greater in ecosystems dominated by EEM fungi than in those dominated by AM fungi. Using global data sets, we show that soil in ecosystems dominated by EEM-associated plants contains 70% more carbon per unit nitrogen than soil in ecosystems dominated by AM-associated plants. The effect of mycorrhizal type on soil carbon is independent of, and of far larger consequence than, the effects of net primary production, temperature, precipitation and soil clay content. Hence the effect of mycorrhizal type on soil carbon content holds at the global scale. This finding links the functional traits of mycorrhizal fungi to carbon storage at ecosystem-to-global scales, suggesting that plant-decomposer competition for nutrients exerts a fundamental control over the terrestrial carbon cycle.
Globally, root production accounts for 33–67% of terrestrial net primary productivity and influences decomposition via root production and turnover, carbon (C) allocation to mycorrhizal fungi and ...root exudation. As recognized above ground, the timing of phenological events affects terrestrial C balance, yet there is no parallel understanding for below‐ground phenology. In this paper we examine the phenology of root production and its relationship to temperature, soil moisture, and above‐ground phenology. Synthesizing 87 observations of whole‐plant phenology from 40 studies, we found that, on average, root growth occurs 25 ± 8 d after shoot growth but that the offset between the peak in root and shoot growth varies > 200 d across biomes (boreal, temperate, Mediterranean, and subtropical). Root and shoot growth are positively correlated with median monthly temperature and mean monthly precipitation in boreal, temperate, and subtropical biomes. However, a temperature hysteresis in these biomes leads to the hypothesis that internal controls over C allocation to roots are an equally, if not more, important driver of phenology. The specific mechanisms are as yet unclear but they are likely mediated by some combination of photoassimilate supply, hormonal signaling, and growth form.
Respiration by soil bacteria and fungi is one of the largest fluxes of carbon (C) from the land surface. Although this flux is a direct product of microbial metabolism, controls over metabolism and ...their responses to global change are a major uncertainty in the global C cycle. Here, we explore an in silico approach to predict bacterial C-use efficiency (CUE) for over 200 species using genome-specific constraint-based metabolic modeling. We find that potential CUE averages 0.62 ± 0.17 with a range of 0.22 to 0.98 across taxa and phylogenetic structuring at the subphylum levels. Potential CUE is negatively correlated with genome size, while taxa with larger genomes are able to access a wider variety of C substrates. Incorporating the range of CUE values reported here into a next-generation model of soil biogeochemistry suggests that these differences in physiology across microbial taxa can feed back on soil-C cycling.
Ecology Letters (2011) 14: 187-194 ABSTRACT: The degree to which rising atmospheric CO₂ will be offset by carbon (C) sequestration in forests depends in part on the capacity of trees and soil ...microbes to make physiological adjustments that can alleviate resource limitation. Here, we show for the first time that mature trees exposed to CO₂ enrichment increase the release of soluble C from roots to soil, and that such increases are coupled to the accelerated turnover of nitrogen (N) pools in the rhizosphere. Over the course of 3 years, we measured in situ rates of root exudation from 420 intact loblolly pine (Pinus taeda L.) roots. Trees fumigated with elevated CO₂ (200 p.p.m.v. over background) increased exudation rates (μg C cm⁻¹ root h⁻¹) by 55% during the primary growing season, leading to a 50% annual increase in dissolved organic inputs to fumigated forest soils. These increases in root-derived C were positively correlated with microbial release of extracellular enzymes involved in breakdown of organic N (R² = 0.66; P = 0.006) in the rhizosphere, indicating that exudation stimulated microbial activity and accelerated the rate of soil organic matter (SOM) turnover. In support of this conclusion, trees exposed to both elevated CO₂ and N fertilization did not increase exudation rates and had reduced enzyme activities in the rhizosphere. Collectively, our results provide field-based empirical support suggesting that sustained growth responses of forests to elevated CO₂ in low fertility soils are maintained by enhanced rates of microbial activity and N cycling fuelled by inputs of root-derived C. To the extent that increases in exudation also stimulate SOM decomposition, such changes may prevent soil C accumulation in forest ecosystems.
Our knowledge of carbon (C) and nitrogen (N) dynamics during stand development is not only essential for evaluating the role of secondary forests in the global terrestrial C cycle, but also crucial ...for understanding long-term C—N interactions in terrestrial ecosystems. However, a comprehensive understanding of forest C and N dynamics over age sequence remains elusive due to the diverse results obtained across individual studies. Here, we synthesized the results of more than 100 studies to examine C and N dynamics during forest stand development. Our results showed that C accumulated in aboveground vegetation, litter and forest floor pools, while the mineral soil C pool did not exhibit significant changes in most studies. The rate of C changes declined with stand age and approached equilibrium during the later stage of stand development. The rate of N changes exhibited linear increases with that of C changes, indicating that N also accrued in various ecosystem components except mineral soil. These results demonstrate that substantial increases in C pools over age sequence are accompanied by N accretion in forest ecosystems. The concurrent C and N dynamics suggest that forest ecosystems may have an intrinsic ability to preclude progressive N limitation during stand development.
Theory and experiments suggest that rhizodeposition can accelerate N-cycling by stimulating microbial decomposition of soil organic matter (SOM). However, there are remarkably few experimental ...demonstrations on the degree to which variations in root exudation alter rhizosphere N dynamics in the field. We conducted a series of in situ substrate addition experiments and a modeling exercise to investigate how exudate mimics and enzyme solutions (at varying concentrations) influence rhizosphere SOM and N dynamics in a loblolly pine (Pinus taeda) plantation (Duke Forest). Exudates were added semi-continuously to unfertilized and fertilized soils in summer and fall; enzymes were added during the following summer. Exudate additions enhanced the microbial biomass specific activities of enzymes that degrade fast-cycling N pools (i.e., amino acids and amino sugars), and increased microbial allocation to N-degrading compounds. More, such effects occurred at low exudate concentrations in unfertilized soil and at higher concentrations in fertilized soil. Direct additions of a subset of enzymes (amino sugar- and cellulose-degrading) to soils increased net N mineralization rates, but additions of enzymes that cleave slow-cycling SOM did not. We conclude that exudates can stimulate microbes to decompose labile SOM and release N without concomitant changes in microbial biomass, yet the investment of plants to trigger this effect may be greater in N-rich soils.
•Evidence for a mechanistic link between root exudation and accelerated N cycling.•Exudate additions enhanced fast-cycling N degrading enzyme activities.•Additions of fast-cycling N degrading enzymes increased net N mineralization.•Much of the extra N is likely derived from amino acids and amino sugars.•Investment of plants to trigger SOM decomposition is much higher in N-rich soils.
While there is an emerging view that roots and their associated microbes actively alter resource availability and soil organic matter (SOM) decomposition, the ecosystem consequences of such ...rhizosphere effects have rarely been quantified. Using a meta‐analysis, we show that multiple indices of microbially mediated C and nitrogen (N) cycling, including SOM decomposition, are significantly enhanced in the rhizospheres of diverse vegetation types. Then, using a numerical model that combines rhizosphere effect sizes with fine root morphology and depth distributions, we show that root‐accelerated mineralization and priming can account for up to one‐third of the total C and N mineralized in temperate forest soils. Finally, using a stoichiometrically constrained microbial decomposition model, we show that these effects can be induced by relatively modest fluxes of root‐derived C, on the order of 4% and 6% of gross and net primary production, respectively. Collectively, our results indicate that rhizosphere processes are a widespread, quantitatively important driver of SOM decomposition and nutrient release at the ecosystem scale, with potential consequences for global C stocks and vegetation feedbacks to climate.
Nutrient limitation is pervasive in the terrestrial biosphere, although the relationship between global carbon (C) nitrogen (N) and phosphorus (P) cycles remains uncertain. Using meta‐analysis we ...show that gross primary production (GPP) partitioning belowground is inversely related to soil‐available N : P, increasing with latitude from tropical to boreal forests. N‐use efficiency is highest in boreal forests, and P‐use efficiency in tropical forests. High C partitioning belowground in boreal forests reflects a 13‐fold greater C cost of N acquisition compared to the tropics. By contrast, the C cost of P acquisition varies only 2‐fold among biomes. This analysis suggests a new hypothesis that the primary limitation on productivity in forested ecosystems transitions from belowground resources at high latitudes to aboveground resources at low latitudes as C‐intensive root‐ and mycorrhizal‐mediated nutrient capture is progressively replaced by rapidly cycling, enzyme‐derived nutrient fluxes when temperatures approach the thermal optimum for biogeochemical transformations.
Land ecosystems sequester on average about a quarter of anthropogenic CO2 emissions. It has been proposed that nitrogen (N) availability will exert an increasingly limiting effect on plants’ ability ...to store additional carbon (C) under rising CO2, but these mechanisms are not well understood. Here, we review findings from elevated CO2 experiments using a plant economics framework, highlighting how ecosystem responses to elevated CO2 may depend on the costs and benefits of plant interactions with mycorrhizal fungi and symbiotic N-fixing microbes. We found that N-acquisition efficiency is positively correlated with leaf-level photosynthetic capacity and plant growth, and negatively with soil C storage. Plants that associate with ectomycorrhizal fungi and N-fixers may acquire N at a lower cost than plants associated with arbuscular mycorrhizal fungi. However, the additional growth in ectomycorrhizal plants is partly offset by decreases in soil C pools via priming. Collectively, our results indicate that predictive models aimed at quantifying C cycle feedbacks to global change may be improved by treating N as a resource that can be acquired by plants in exchange for energy, with different costs depending on plant interactions with microbial symbionts.
The exudation of carbon (C) by tree roots stimulates microbial activity and the production of extracellular enzymes in the rhizosphere. Here, we investigated whether the strength of rhizosphere ...processes differed between temperate forest trees that vary in soil organic matter (SOM) chemistry and associate with either ectomycorrhizal (ECM) or arbuscular mycorrhizal (AM) fungi. We measured rates of root exudation, microbial and extracellular enzyme activity, and nitrogen (N) availability in samples of rhizosphere and bulk soil influenced by four temperate forest tree species (i.e., to estimate a rhizosphere effect). Although not significantly different between species, root exudation ranged from 0.36 to 1.10 g C m⁻² day⁻¹, representing a small but important transfer of C to rhizosphere microbes. The magnitude of the rhizosphere effects could not be easily characterized by mycorrhizal associations or SOM chemistry. Ash had the lowest rhizosphere effects and beech had the highest rhizosphere effects, representing one AM and one ECM species, respectively. Hemlock and sugar maple had equivalent rhizosphere effects on enzyme activity. However, the form of N produced in the rhizosphere varied with mycorrhizal association. Enhanced enzyme activity primarily increased amino acid availability in ECM rhizospheres and increased inorganic N availability in AM rhizospheres. These results show that the exudation of C by roots can enhance extracellular enzyme activity and soil-N cycling. This work suggests that global changes that alter belowground C allocation have the potential to impact the form and amount of N to support primary production in ECM and AM stands.
PDF
