skip to main content


Title: A holistic framework integrating plant-microbe-mineral regulation of soil bioavailable nitrogen
Abstract

Soil organic nitrogen (N) is a critical resource for plants and microbes, but the processes that govern its cycle are not well-described. To promote a holistic understanding of soil N dynamics, we need an integrated model that links soil organic matter (SOM) cycling to bioavailable N in both unmanaged and managed landscapes, including agroecosystems. We present a framework that unifies recent conceptual advances in our understanding of three critical steps in bioavailable N cycling: organic N (ON) depolymerization and solubilization; bioavailable N sorption and desorption on mineral surfaces; and microbial ON turnover including assimilation, mineralization, and the recycling of microbial products. Consideration of the balance between these processes provides insight into the sources, sinks, and flux rates of bioavailable N. By accounting for interactions among the biological, physical, and chemical controls over ON and its availability to plants and microbes, our conceptual model unifies complex mechanisms of ON transformation in a concrete conceptual framework that is amenable to experimental testing and translates into ideas for new management practices. This framework will allow researchers and practitioners to use common measurements of particulate organic matter (POM) and mineral-associated organic matter (MAOM) to design strategic organic N-cycle interventions that optimize ecosystem productivity and minimize environmental N loss.

 
more » « less
NSF-PAR ID:
10226708
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
Biogeochemistry
ISSN:
0168-2563
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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.

     
    more » « less
  2. Abstract

    To predict the behavior of the terrestrial carbon cycle, it is critical to understand the source, formation pathway, and chemical composition of soil organic matter (SOM). There is emerging consensus that slow‐cycling SOM generally consists of relatively low molecular weight organic carbon substrates that enter the mineral soil as dissolved organic matter and associate with mineral surfaces (referred to as “mineral‐associated OM,” or MAOM). However, much debate and contradictory evidence persist around: (a) whether the organic C substrates within the MAOM pool primarily originate from aboveground vs. belowground plant sources and (b) whether C substrates directly sorb to mineral surfaces or undergo microbial transformation prior to their incorporation into MAOM. Here, we attempt to reconcile disparate views on the formation of MAOM by proposing a spatially explicit set of processes that link plant C source with MAOM formation pathway. Specifically, because belowground vs. aboveground sources of plant C enter spatially distinct regions of the mineral soil, we propose that fine‐scale differences in microbial abundance should determine the probability of substrate–microbe vs. substrate–mineral interaction. Thus, formation of MAOM in areas of high microbial density (e.g., the rhizosphere and other microbial hotspots) should primarily occur through an in vivo microbial turnover pathway and favor C substrates that are first biosynthesized with high microbial carbon‐use efficiency prior to incorporation in the MAOM pool. In contrast, in areas of low microbial density (e.g., certain regions of the bulk soil), MAOM formation should primarily occur through the direct sorption of intact or partially oxidized plant compounds to uncolonized mineral surfaces, minimizing the importance of carbon‐use efficiency, and favoring C substrates with strong “sorptive affinity.” Through this framework, we thus describe how the primacy of biotic vs. abiotic controls on MAOM dynamics is not mutually exclusive, but rather spatially dictated. Such an understanding may be integral to more accurately modeling soil organic matter dynamics across different spatial scales.

     
    more » « less
  3. Abstract

    Decomposition of soil organic matter (SOM) can be stimulated by fresh organic matter input, a phenomenon known as the ‘priming effect’. Despite its global importance, the relationship of the priming effect to mineral weathering and nutrient release remains unclear. Here we show close linkages between mineral weathering in the critical zone and primed decomposition of SOM. Intensified mineral weathering and rock-derived nutrient release are generally coupled with primed SOM decomposition resulting from “triggered” microbial activity. Fluxes of organic matter products decomposed via priming are linearly correlated with weathering congruency. Weathering congruency influences the formation of organo-mineral associations, thereby modulating the accessibility of organic matter to microbial decomposers and, thus, the priming effect. Our study links weathering with primed SOM decomposition, which plays a key role in controlling soil C dynamics in space and time. These connections represent fundamental links between long-term lithogenic element cycling (= weathering) and rapid turnover of carbon and nutrients (= priming) in soil.

     
    more » « less
  4. Abstract

    In dryland soils, spatiotemporal variation in surface soils (0–10 cm) plays an important role in the function of the “critical zone” that extends from canopy to groundwater. Understanding connections between soil microbes and biogeochemical cycling in surface soils requires repeated multivariate measurements of nutrients, microbial abundance, and microbial function. We examined these processes in resource islands and interspaces over a two‐month period at a Chihuahuan Desert bajada shrubland site. We collected soil inProsopis glandulosa(honey mesquite),Larrea tridentata(creosote bush), and unvegetated (interspace) areas to measure soil nutrient concentrations, microbial biomass, and potential soil enzyme activity. We monitored the dynamics of these belowground processes as soil conditions dried and then rewetted due to rainfall. Most measured variables, including inorganic nutrients, microbial biomass, and soil enzyme activities, were greater under shrubs during both wet and dry periods, with the highest magnitudes under mesquite followed by creosote bush and then interspace. One exception was nitrate, which was highly variable and did not show resource island patterns. Temporally, rainfall pulses were associated with substantial changes in soil nutrient concentrations, though resource island patterns remained consistent during all phases of the soil moisture pulse. Microbial biomass was more consistent than nutrients, decreasing only when soils were driest. Potential enzyme activities were even more consistent and did not decline in dry periods, potentially helping to stimulate observed pulses in CO2efflux following rain events observed at a co‐located eddy flux tower. These results indicate a critical zone with organic matter cycling patterns consistently elevated in shrub resource islands (which varied by shrub species), high decomposition potential that limits soil organic matter accumulation across the landscape, and nitrate fluxes that are decoupled from the organic matter pathways.

     
    more » « less
  5. Abstract

    Nitrogen (N) deposition increases soil carbon (C) storage by reducing microbial activity. These effects vary in soil beneath trees that associate with arbuscular (AM) and ectomycorrhizal (ECM) fungi. Variation in carbon C and N uptake traits among microbes may explain differences in soil nutrient cycling between mycorrhizal associations in response to high N loads, a mechanism not previously examined due to methodological limitations. Here, we used quantitative Stable Isotope Probing (qSIP) to measure bacterial C and N assimilation rates from an added organic compound, which we conceptualize as functional traits. As such, we applied a trait‐based approach to explore whether variation in assimilation rates of bacterial taxa can inform shifts in soil function under chronic N deposition. We show taxon‐specific and community‐wide declines of bacterial C and N uptake under chronic N deposition in both AM and ECM soils. N deposition‐induced reductions in microbial activity were mirrored by declines in soil organic matter mineralization rates in AM but not ECM soils. Our findings suggest C and N uptake traits of bacterial communities can predict C cycling feedbacks to N deposition in AM soils, but additional data, for instance on the traits of fungi, may be needed to connect microbial traits with soil C and N cycling in ECM systems. Our study also highlights the potential of employing qSIP in conjunction with trait‐based analytical approaches to inform how ecological processes of microbial communities influence soil functioning.

     
    more » « less