Colin Averill

Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage

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.

Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models

Since fungi and bacteria are the dominant decomposers in soil, their distinct physiologies are likely to differentially influence rates of ecosystem carbon (C) and nitrogen (N) cycling. We used meta-analysis and an enzyme-driven biogeochemical model to explore the drivers and biogeochemical consequences of changes in the fungal-to-bacterial ratio (F : B). In our meta-analysis data set, F : B increased with soil C : N ratio (R(2) = 0.224, P < 0.001), a relationship predicted by our model. We found that differences in biomass turnover rates influenced F : B under conditions of C limitation, while differences in biomass stoichiometry set the upper bounds on F : B once a nutrient limitation threshold was reached. Ecological interactions between the two groups shifted along a gradient of resource stoichiometry. At intermediate substrate C : N, fungal N mineralisation fuelled bacterial growth, increasing total microbial biomass and decreasing net N mineralisation. Therefore, we conclude that differences in bacterial and fungal physiology may have large consequences for ecosystem-scale C and N cycling.

Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N

It is hypothesized that decreasing mean annual temperature and rates of nitrogen (N) cycling causes plants to switch from inorganic to organic forms of N as the primary mode of N nutrition. To test this hypothesis, we conducted field experiments and collected natural-abundance delta15N signatures of foliage, soils, and ectomycorrhizal sporocarps along a steep elevation-climate gradient in the White Mountains, New Hampshire, USA. Here we show that with increasing elevation organic forms of N became the dominant source of N taken up by hardwood and coniferous tree species based on dual-labeled glycine uptake analysis, an important confirmation of an emerging theory for the biogeochemistry of the N cycle. Variation in natural abundance foliar delta15N with elevation was also consistent with increasing organic N uptake, though a simple, mass balance model demonstrated that the uptake of delta15N depleted inorganic N, rather than fractionation upon transfer of N from mycorrhizal fungi, best explains variations in foliar delta15N with elevation.

Nitrogen limitation of decomposition and decay: how can it occur?

The availability of nitrogen (N) is a critical control on the cycling and storage of soil carbon (C). Yet, there are conflicting conceptual models to explain how N availability influences the decomposition of organic matter by soil microbial communities. Several lines of evidence suggest that N availability limits decomposition; the earliest stages of leaf litter decay are associated with a net import of N from the soil environment, and both observations and models show that high N organic matter decomposes more rapidly. In direct contrast to these findings, experimental additions of inorganic N to soils broadly show a suppression of microbial activity, which is inconsistent with N limitation of decomposition. Resolving this apparent contradiction is critical to representing nutrient dynamics in predictive ecosystem models under a multitude of global change factors that alter soil N availability. Here, we propose a new conceptual framework, the Carbon, Acidity, and Mineral Protection hypothesis, to understand the effects of N availability on soil C cycling and storage and explore the predictions of this framework with a mathematical model. Our model simulations demonstrate that N addition can have opposing effects on separate soil C pools (particulate and mineral-protected carbon) because they are differentially affected by microbial biomass growth. Moreover, changes in N availability are frequently linked to shifts in soil pH or osmotic stress, which can independently affect microbial biomass dynamics and mask N stimulation of microbial activity. Thus, the net effect of N addition on soil C is dependent upon interactions among microbial physiology, soil mineralogy, and soil acidity. We believe that our synthesis provides a broadly applicable conceptual framework to understand and predict the effect of changes in soil N availability on ecosystem C cycling under global change.

Historical precipitation predictably alters the shape and magnitude of microbial functional response to soil moisture

Soil moisture constrains the activity of decomposer soil microorganisms, and in turn the rate at which soil carbon returns to the atmosphere. While increases in soil moisture are generally associated with increased microbial activity, historical climate may constrain current microbial responses to moisture. However, it is not known if variation in the shape and magnitude of microbial functional responses to soil moisture can be predicted from historical climate at regional scales. To address this problem, we measured soil enzyme activity at 12 sites across a broad climate gradient spanning 442-887 mm mean annual precipitation. Measurements were made eight times over 21 months to maximize sampling during different moisture conditions. We then fit saturating functions of enzyme activity to soil moisture and extracted half saturation and maximum activity parameter values from model fits. We found that 50% of the variation in maximum activity parameters across sites could be predicted by 30-year mean annual precipitation, an indicator of historical climate, and that the effect is independent of variation in temperature, soil texture, or soil carbon concentration. Based on this finding, we suggest that variation in the shape and magnitude of soil microbial response to soil moisture due to historical climate may be remarkably predictable at regional scales, and this approach may extend to other systems. If historical contingencies on microbial activities prove to be persistent in the face of environmental change, this approach also provides a framework for incorporating historical climate effects into biogeochemical models simulating future global change scenarios.

Divergence in plant and microbial allocation strategies explains continental patterns in microbial allocation and biogeochemical fluxes

Allocation trade-offs shape ecological and biogeochemical phenomena at local to global scale. Plant allocation strategies drive major changes in ecosystem carbon cycling. Microbial allocation to enzymes that decompose carbon vs. organic nutrients may similarly affect ecosystem carbon cycling. Current solutions to this allocation problem prioritise stoichiometric tradeoffs implemented in plant ecology. These solutions may not maximise microbial growth and fitness under all conditions, because organic nutrients are also a significant carbon resource for microbes. I created multiple allocation frameworks and simulated microbial growth using a microbial explicit biogeochemical model. I demonstrate that prioritising stoichiometric trade-offs does not optimise microbial allocation, while exploiting organic nutrients as carbon resources does. Analysis of continental-scale enzyme data supports the allocation patterns predicted by this framework, and modelling suggests large deviations in soil C loss based on which strategy is implemented. Therefore, understanding microbial allocation strategies will likely improve our understanding of carbon cycling and climate.

Tradeoffs in microbial carbon allocation may mediate soil carbon storage in future climates

Climate-induced changes in soil microbial physiology impact ecosystem carbon (C) storage and alter the rate of CO2 flux from soils to the atmosphere (Allison et al., 2010). The direction and magnitude of these microbial feedbacks depend on changes in saprotrophic bacterial and fungal C allocation in response to altered temperature, precipitation, and nutrient availability. Soil microbes may differentially allocate C in changing environments by altering processes such as enzyme production, C use efficiency (CUE), or biomass stoichiometry (Figure ​(Figure1).1). However, because these mechanisms may operate simultaneously and interact, microbial physiological feedbacks on soil C storage are difficult to predict. For example, initial increases in microbial CUE or biomass C:N may be counteracted by increases in enzyme production to acquire limiting organic nutrients. Figure 1 Three mechanisms through which microorganisms can shift C allocation: (A) extracellular enzyme activities, (B) carbon use efficiency, or (C) biomass stoichiometry. Each of these pathways can alter C storage in soils. Trend lines indicate expected responses ... Few studies have standardized microbial process rates, such as extracellular enzyme production or respiration, to the size of the microbial biomass. Examining process rates alone may obscure the microbial physiological mechanisms that underlie climate-induced changes in soil C cycling, leading to contradictory patterns among different studies. For instance, in a large-scale survey of soil protease activities from climate manipulations, drier and warmer conditions resulted in lower extracellular enzyme activities (EEA) compared to ambient conditions (Brzostek et al., 2012). In contrast, drier soils have also been found to stabilize extracellular enzymes in water films, reducing enzyme turnover rates and increasing potential activities (Lawrence et al., 2009; German et al., 2012).

Microbial-mediated redistribution of ecosystem nitrogen cycling can delay progressive nitrogen limitation

Soil nitrogen (N) availability constrains future predictions of ecosystem primary productivity and carbon storage. The progressive N limitation (PNL) hypothesis predicts that forest net primary productivity (NPP) will decline with age, and that the response of NPP to elevated CO2 will attenuate through time due to negative feedbacks of NPP on the soil N cycle. A central assumption of the PNL hypothesis is that, without changes in exogenous exchange of N in an ecosystem, increases in plant N uptake require increased soil N cycling rates. However, at ecosystem scale, microbial N uptake exceeds plant uptake. Hence, a change in the partitioning of N between plants and soil microorganisms may represent an alternative mechanism to sustain plant N uptake in the face of PNL. To estimate N partitioning of total N cycling between plants and microbes, we measured and modeled growth and N uptake of trees, bacteria, saprotrophic fungi, and ectomycorrhizal fungi across a forest succession and N limitation gradient. The combined plant and ectomycorrhizal N uptake increased from early to late succession, and nearly matched saprotrophic N uptake in late successional sites, while total N cycling remained stable or even declined. Changes in microbial community structure can thus mediate a redistribution of ecosystem nitrogen cycling, allowing an increase in plant N uptake without concomitant increases in soil N cycling. We further suggest that microbe-mediated changes in N partitioning can delay PNL and may thereby act as a mechanism to extend the duration of the land carbon sink in response to rising atmospheric CO2.

Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks

Most tree roots on Earth form a symbiosis with either ecto- or arbuscular mycorrhizal fungi. Nitrogen fertilization is hypothesized to favor arbuscular mycorrhizal tree species at the expense of ectomycorrhizal species due to differences in fungal nitrogen acquisition strategies, and this may alter soil carbon balance, as differences in forest mycorrhizal associations are linked to differences in soil carbon pools. Combining nitrogen deposition data with continental-scale US forest data, we show that nitrogen pollution is spatially associated with a decline in ectomycorrhizal vs. arbuscular mycorrhizal trees. Furthermore, nitrogen deposition has contrasting effects on arbuscular vs. ectomycorrhizal demographic processes, favoring arbuscular mycorrhizal trees at the expense of ectomycorrhizal trees, and is spatially correlated with reduced soil carbon stocks. This implies future changes in nitrogen deposition may alter the capacity of forests to sequester carbon and offset climate change via interactions with the forest microbiome.

Multiple models and experiments underscore large uncertainty in soil carbon dynamics

Soils contain more carbon than plants or the atmosphere, and sensitivities of soil organic carbon (SOC) stocks to changing climate and plant productivity are a major uncertainty in global carbon cycle projections. Despite a consensus that microbial degradation and mineral stabilization processes control SOC cycling, no systematic synthesis of long-term warming and litter addition experiments has been used to test process-based microbe-mineral SOC models. We explored SOC responses to warming and increased carbon inputs using a synthesis of 147 field manipulation experiments and five SOC models with different representations of microbial and mineral processes. Model projections diverged but encompassed a similar range of variability as the experimental results. Experimental measurements were insufficient to eliminate or validate individual model outcomes. While all models projected that CO2 efflux would increase and SOC stocks would decline under warming, nearly one-third of experiments observed decreases in CO2 flux and nearly half of experiments observed increases in SOC stocks under warming. Long-term measurements of C inputs to soil and their changes under warming are needed to reconcile modeled and observed patterns. Measurements separating the responses of mineral-protected and unprotected SOC fractions in manipulation experiments are needed to address key uncertainties in microbial degradation and mineral stabilization mechanisms. Integrating models with experimental design will allow targeting of these uncertainties and help to reconcile divergence among models to produce more confident projections of SOC responses to global changes.