Inhabiting the interface between plant roots and soil, mycorrhizal fungi play a unique but underappreciated role in soil organic matter (SOM) dynamics. Their hyphae provide an efficient mechanism for ...distributing plant carbon throughout the soil, facilitating its deposition into soil pores and onto mineral surfaces, where it can be protected from microbial attack. Mycorrhizal exudates and dead tissues contribute to the microbial necromass pool now known to play a dominant role in SOM formation and stabilization. While mycorrhizal fungi lack the genetic capacity to act as saprotrophs, they use several strategies to access nutrients locked in SOM and thereby promote its decay, including direct enzymatic breakdown, oxidation via Fenton chemistry, and stimulation of heterotrophic microorganisms through carbon provision to the rhizosphere. An additional mechanism, competition with free-living saprotrophs, potentially suppresses SOM decomposition, leading to its accumulation. How these various nutrient acquisition strategies differentially influence SOM formation, stabilization, and loss is an area of critical research need.
Soil organic matter (SOM) and the carbon and nutrients therein drive fundamental submicron- to global-scale biogeochemical processes and influence carbon-climate feedbacks. Consensus is emerging that ...microbial materials are an important constituent of stable SOM, and new conceptual and quantitative SOM models are rapidly incorporating this view. However, direct evidence demonstrating that microbial residues account for the chemistry, stability and abundance of SOM is still lacking. Further, emerging models emphasize the stabilization of microbial-derived SOM by abiotic mechanisms, while the effects of microbial physiology on microbial residue production remain unclear. Here we provide the first direct evidence that soil microbes produce chemically diverse, stable SOM. We show that SOM accumulation is driven by distinct microbial communities more so than clay mineralogy, where microbial-derived SOM accumulation is greatest in soils with higher fungal abundances and more efficient microbial biomass production.
Resolving fungal and bacterial groups within the microbial decomposer community is thought to capture disparate life strategies for soil microbial decomposers, associating bacteria with an
r
...-selected strategy for carbon (C) and nutrient use, and fungi with a
K
-selected strategy. Additionally, food-web model-based work has established a widely held belief that the bacterial decomposer pathway in soil supports high turnover rates of easily available substrates, while the slower fungal-dominated decomposition pathway supports the decomposition of more complex organic material, thus characterizing the biogeochemistry of the ecosystem. We used a field experiment, the Detritus Input and Removal Treatments, or DIRT, experiment (Harvard Forest Long-Term Ecological Research Site, USA) where litter and root inputs (control, no litter, double litter, or no tree roots) have been experimentally manipulated during 23 years, generating differences in soil C quality. We hypothesized (1) that δ
13
C enrichment would decrease with higher soil C quality and that a higher C quality would favor bacterial decomposers, (2) that the C mineralized in fungal-dominated treatments would be of lower quality and also depleted in δ
13
C relative to bacterial-dominated high-quality soil C treatments, and (3) that higher C mineralization along with higher gross N mineralization rates would occur in bacterial-dominated treatments compared with more fungal-dominated treatments. The DIRT treatments resulted in a gradient of soil C quality, as shown by up to 4.5-fold differences between the respiration per soil C between treatments. High-quality C benefited fungal dominance, in direct contrast with our hypothesis. Further, there was no difference between the δ
13
CO
2
produced by a fungal compared with a bacterial-dominated decomposer community. There were differences in C and N mineralization between DIRT treatments, but these were not related to the relative dominance of fungal and bacterial decomposers. Thus we find no support for the hypothesized differences between detrital food webs dominated by bacteria compared to those dominated by fungi. Rather, an association between high-quality soil C and fungi emerges from our results. Consequently there is a need to revise our basic understanding for microbial communities and the processes they regulate in soil.
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Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in ...regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combine distinct community inocula (a biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil. While community composition and diversity are the strongest predictors of CUE, abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity only under high moisture. Altogether these results indicate that the diversity × ecosystem-function relationship can be impaired under non-favorable conditions in soils, and that to understand changes in soil C cycling we need to account for the multiple facets of global changes.
Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of ...emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.
Historical increases in emissions and atmospheric deposition of oxidized and reduced nitrogen (N) provided the impetus for extensive, global-scale research investigating the effects of excess N in ...terrestrial and aquatic ecosystems, with several regions within the Eastern Deciduous Forest of the United States found to be susceptible to negative effects of excess N. The Clean Air Act and associated rules have led to decreases in emissions and deposition of oxidized N, especially in eastern U.S., representing a research challenge and opportunity for ecosystem ecologists and biogeochemists. The purpose of this paper is to predict changes in the structure and function of North American forest ecosystems in a future of decreased N deposition. Hysteresis is a property of a system wherein output is not a strict function of corresponding input, incorporating lag, delay, or history dependence, particularly when the response to decreasing input is different from the response to increasing input. We suggest a conceptual hysteretic model predicting varying lag times in recovery of soil acidification, plant biodiversity, soil microbial communities, forest carbon (C) and N cycling, and surface water chemistry toward pre-N impact conditions. Nearly all of these can potentially respond strongly to reductions in N deposition. Most responses are expected to show some degree of hysteresis, with the greatest delays in response occurring in processes most tightly linked to “slow pools” of N in wood and soil organic matter. Because experimental studies of declines in N loads in forests of North America are lacking and because of the expected hysteresis, it is difficult to generalize from experimental results to patterns expected from declining N deposition. These will likely be long-term phenomena, difficult to distinguish from other, concurrent environmental changes, including elevated atmospheric CO2, climate change, reductions in acidity, invasions of new species, and long-term vegetation responses to past disturbance.
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•Past work on nitrogen (N) effects on ecosystems arose from increased N deposition.•Many forest ecosystems of the eastern U.S. have been sensitive to excess N inputs.•Federal laws have resulted in lower deposition of oxidized N in the eastern U.S.•A hysteretic model is proposed for forest recovery from decreased N deposition.•N-impacted forests should show time lags recovering toward pre-impact conditions.
Nitrogen (N)-impacted forest ecosystems are predicted to exhibit a time lag of varying duration toward recovery initiated by current declines in atmospheric N deposition.
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Predicting and mitigating changes in soil carbon (C) stocks under global change requires a coherent understanding of the factors regulating soil organic matter (SOM) formation and persistence, ...including knowledge of the direct sources of SOM (plants vs. microbes). In recent years, conceptual models of SOM formation have emphasized the primacy of microbial‐derived organic matter inputs, proposing that microbial physiological traits (e.g., growth efficiency) are dominant controls on SOM quantity. However, recent quantitative studies have challenged this view, suggesting that plants make larger direct contributions to SOM than is currently recognized by this paradigm. In this review, we attempt to reconcile these perspectives by highlighting that variation across estimates of plant‐ versus microbial‐derived SOM may arise in part from methodological limitations. We show that all major methods used to estimate plant versus microbial contributions to SOM have substantial shortcomings, highlighting the uncertainty in our current quantitative estimates. We demonstrate that there is significant overlap in the chemical signatures of compounds produced by microbes, plant roots, and through the extracellular decomposition of plant litter, which introduces uncertainty into the use of common biomarkers for parsing plant‐ and microbial‐derived SOM, especially in the mineral‐associated organic matter (MAOM) fraction. Although the studies that we review have contributed to a deeper understanding of microbial contributions to SOM, limitations with current methods constrain quantitative estimates. In light of recent advances, we suggest that now is a critical time to re‐evaluate long‐standing methods, clearly define their limitations, and develop a strategic plan for improving the quantification of plant‐ and microbial‐derived SOM. From our synthesis, we outline key questions and challenges for future research on the mechanisms of SOM formation and stabilization from plant and microbial pathways.
Soil organic matter (SOM) comprises ~80% of global terrestrial carbon stocks, much of which is stored as mineral‐associated organic matter (MAOM). MAOM is derived from both plant and microbial biomolecules, but the quantitative contributions of each remain uncertain (represented by the mixing of red and blue into purple). There is substantial overlap in the compounds produced by microbes, plant roots and those released through the extracellular decomposition of plant litter, and limitations in our current methods constrain quantification. We review the methods used to quantify plant‐ and microbial‐derived SOM, examining their limitations and key future research priorities towards elucidating the plant and microbial pathways of SOM formation.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Microbial carbon use efficiency (CUE) is a critical regulator of soil organic matter dynamics and terrestrial carbon fluxes, with strong implications for soil biogeochemistry models. While ecologists ...increasingly appreciate the importance of CUE, its core concepts remain ambiguous: terminology is inconsistent and confusing, methods capture variable temporal and spatial scales, and the significance of many fundamental drivers remains inconclusive. Here we outline the processes underlying microbial efficiency and propose a conceptual framework that structures the definition of CUE according to increasingly broad temporal and spatial drivers where (1) CUE P reflects population-scale carbon use efficiency of microbes governed by species-specific metabolic and thermodynamic constraints, (2) CUE C defines community-scale microbial efficiency as gross biomass production per unit substrate taken up over short time scales, largely excluding recycling of microbial necromass and exudates, and (3) CUE E reflects the ecosystem-scale efficiency of net microbial biomass production (growth) per unit substrate taken up as iterative breakdown and recycling of microbial products occurs. CUEE integrates all internal and extracellular constraints on CUE and hence embodies an ecosystem perspective that fully captures all drivers of microbial biomass synthesis and decay. These three definitions are distinct yet complementary, capturing the capacity for carbon storage in microbial biomass across different ecological scales. By unifying the existing concepts and terminology underlying microbial efficiency, our framework enhances data interpretation and theoretical advances.
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BFBNIB, DOBA, EMUNI, FZAB, GEOZS, IJS, IMTLJ, IZUM, KILJ, KISLJ, MFDPS, NMLJ, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UILJ, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
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.
Warming can accelerate or decelerate soil microbial response to warmer temperatures. Here we provide support for the hypothesis that microbial temperature sensitivity is contingent upon substrate availability, which itself is reduced by warming. Thus we show the complex interplay between microbial activity and changes in soil carbon stocks.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Decomposition of organic material by soil microbes generates an annual global release of 50–75 Pg carbon to the atmosphere, ∼7.5–9 times that of anthropogenic emissions worldwide. This process is ...sensitive to global change factors, which can drive carbon cycle–climate feedbacks with the potential to enhance atmospheric warming. Although the effects of interacting global change factors on soil microbial activity have been a widespread ecological focus, the regulatory effects of interspecific interactions are rarely considered in climate feedback studies. We explore the potential of soil animals to mediate microbial responses to warming and nitrogen enrichment within a long-term, field-based global change study. The combination of global change factors alleviated the bottom-up limitations on fungal growth, stimulating enzyme production and decomposition rates in the absence of soil animals. However, increased fungal biomass also stimulated consumption rates by soil invertebrates, restoring microbial process rates to levels observed under ambient conditions. Our results support the contemporary theory that top-down control in soil food webs is apparent only in the absence of bottom-up limitation. As such, when global change factors alleviate the bottom-up limitations on microbial activity, top-down control becomes an increasingly important regulatory force with the capacity to dampen the strength of positive carbon cycle–climate feedbacks.
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