RESUMEN
Understanding of how soil organic matter (SOM) chemistry is altered in a changing climate has advanced considerably; however, most SOM components remain unidentified, impeding the ability to characterize a major fraction of organic matter and predict what types of molecules, and from which sources, will persist in soil. We present a novel approach to better characterize SOM extracts by integrating information from three types of analyses, and we deploy this method to characterize decaying root-detritus soil microcosms subjected to either drought or normal conditions. To observe broad differences in composition, we employed direct infusion Fourier-transform ion cyclotron resonance mass spectrometry (DI-FT-ICR MS). We complemented this with liquid chromatography tandem mass spectrometry (LC-MS/MS) to identify components by library matching. Since libraries contain only a small fraction of SOM components, we also used fragment spectral cosine similarity scores to relate unknowns and library matches through molecular networks. This integrated approach allowed us to corroborate DI-FT-ICR MS molecular formulas using library matches, which included fungal metabolites and related polyphenolic compounds. We also inferred structures of unknowns from molecular networks and improved LC-MS/MS annotation rates from â¼5 to 35% by considering DI-FT-ICR MS molecular formula assignments. Under drought conditions, we found greater relative amounts of lignin-like vs condensed aromatic polyphenol formulas and lower average nominal oxidation state of carbon, suggesting reduced decomposition of SOM and/or microbes under stress. Our integrated approach provides a framework for enhanced annotation of SOM components that is more comprehensive than performing individual data analyses in parallel.
RESUMEN
Mineral-associated soil organic matter (MAOM) is the largest, slowest cycling pool of carbon (C) in the terrestrial biosphere. MAOM is primarily derived from plant and microbial sources, yet the relative contributions of these two sources to MAOM remain unresolved. Resolving this issue is essential for managing and modeling soil carbon responses to environmental change. Microbial biomarkers, particularly amino sugars, are the primary method used to estimate microbial versus plant contributions to MAOM, despite systematic biases associated with these estimates. There is a clear need for independent lines of evidence to help determine the relative importance of plant versus microbial contributions to MAOM. Here, we synthesized 288 datasets of C/N ratios for MAOM, particulate organic matter (POM), and microbial biomass across the soils of forests, grasslands, and croplands. Microbial biomass is the source of microbial residues that form MAOM, whereas the POM pool is the direct precursor of plant residues that form MAOM. We then used a stoichiometric approach-based on two-pool, isotope-mixing models-to estimate the proportional contribution of plant residue (POM) versus microbial sources to the MAOM pool. Depending on the assumptions underlying our approach, microbial inputs accounted for between 34% and 47% of the MAOM pool, whereas plant residues contributed 53%-66%. Our results therefore challenge the existing hypothesis that microbial contributions are the dominant constituents of MAOM. We conclude that biogeochemical theory and models should account for multiple pathways of MAOM formation, and that multiple independent lines of evidence are required to resolve where and when plant versus microbial contributions are dominant in MAOM formation.
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Minerales , Suelo , Suelo/química , Bosques , Carbono , Biomasa , Plantas , Microbiología del SueloRESUMEN
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.
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Carbono , Suelo , Suelo/química , Carbono/metabolismo , Microbiología del Suelo , Plantas/metabolismo , Minerales/químicaRESUMEN
Soil microorganisms shape global element cycles in life and death. Living soil microorganisms are a major engine of terrestrial biogeochemistry, driving the turnover of soil organic matter - Earth's largest terrestrial carbon pool and the primary source of plant nutrients. Their metabolic functions are influenced by ecological interactions with other soil microbial populations, soil fauna and plants, and the surrounding soil environment. Remnants of dead microbial cells serve as fuel for these biogeochemical engines because their chemical constituents persist as soil organic matter. This non-living microbial biomass accretes over time in soil, forming one of the largest pools of organic matter on the planet. In this Review, we discuss how the biogeochemical cycling of organic matter depends on both living and dead soil microorganisms, their functional traits, and their interactions with the soil matrix and other organisms. With recent omics advances, many of the traits that frame microbial population dynamics and their ecophysiological adaptations can be deciphered directly from assembled genomes or patterns of gene or protein expression. Thus, it is now possible to leverage a trait-based understanding of microbial life and death within improved biogeochemical models and to better predict ecosystem functioning under new climate regimes.
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Microbiota , Suelo , Biomasa , Carbono/metabolismo , Ecosistema , Plantas/metabolismo , Microbiología del SueloRESUMEN
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.
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Carbono , Minerales/química , Compuestos Orgánicos , Plantas/metabolismo , Suelo/química , Adsorción , Biodegradación Ambiental , Carbono/química , Carbono/metabolismo , Ciclo del Carbono , Compuestos Orgánicos/química , Compuestos Orgánicos/metabolismo , Microbiología del SueloRESUMEN
Soil organic carbon (SOC) is primarily formed from plant inputs, but the relative carbon (C) contributions from living root inputs (i.e. rhizodeposits) vs litter inputs (i.e. root + shoot litter) are poorly understood. Recent theory suggests that living root inputs exert a disproportionate influence on SOC formation, but few field studies have explicitly tested this by separately tracking living root vs litter inputs as they move through the soil food web and into distinct SOC pools. We used a manipulative field experiment with an annual C4 grass in a forest understory to differentially track its living root vs litter inputs into the soil and to assess net SOC formation over multiple years. We show that living root inputs are 2-13 times more efficient than litter inputs in forming both slow-cycling, mineral-associated SOC as well as fast-cycling, particulate organic C. Furthermore, we demonstrate that living root inputs are more efficiently anabolized by the soil microbial community en route to the mineral-associated SOC pool (dubbed 'the in vivo microbial turnover pathway'). Overall, our findings provide support for the primacy of living root inputs in forming SOC. However, we also highlight the possibility of nonadditive effects of living root and litter inputs, which may deplete SOC pools despite greater SOC formation rates.
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Carbono , Raíces de Plantas/metabolismo , Brotes de la Planta/metabolismo , Microbiología del Suelo , Suelo/química , Animales , Ciclo del Carbono , Connecticut , Cadena Alimentaria , Bosques , Especies Introducidas , Minerales , Raíces de Plantas/química , Brotes de la Planta/química , Poaceae , ÁrbolesRESUMEN
Environmental conditions exert strong controls on the activity of saprotrophic microbes, yet abiotic factors often fail to adequately predict wood decomposition rates across broad spatial scales. Given that species interactions can have significant positive and negative effects on wood-decay fungal activity, one possibility is that biotic processes serve as the primary controls on community function, with abiotic controls emerging only after species associations are accounted for. Here we explore this hypothesis in a factorial field warming- and nitrogen-addition experiment by examining relationships among wood decomposition rates, fungal activity, and fungal community structure. We show that functional outcomes and community structure are largely unrelated to abiotic conditions, with microsite and plot-level abiotic variables explaining at most 19% of the total variability in decomposition and fungal activity, and 2% of the variability in richness and evenness. In contrast, taxonomic richness, evenness, and species associations (i.e., co-occurrence patterns) exhibited strong relationships with community function, accounting for 52% of the variation in decomposition rates and 73% in fungal activity. A greater proportion of positive vs. negative species associations in a community was linked to strong declines in decomposition rates and richness. Evenness emerged as a key mediator between richness and function, with highly even communities exhibiting a positive richness-function relationship and uneven communities exhibiting a negative or null response. These results suggest that community-assembly processes and species interactions are important controls on the function of wood-decay fungal communities, ultimately overwhelming substantial differences in abiotic conditions.
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Micobioma , Biodiversidad , Hongos , Nitrógeno , Madera/microbiologíaRESUMEN
Invasive species frequently co-occur with other disturbances, which can impact the same ecosystem functions as the invader. Yet invasion studies rarely control for the presence of these other disturbances, although their overlapping effects may influence the direction and magnitude of impacts attributed to the invader alone. Here, we ask whether controlling for the presence of a co-occurring disturbance, as well as the time since disturbance, yields different values of an invader's ecosystem effects than when these factors remain unaddressed. We used a chronosequence of six forest stands at a single site: five logged stands that each contained paired invaded-uninvaded plots of the forest understory invasive grass Microstegium vimineum, as well as one unlogged and uninvaded control stand. By controlling for the presence of both logging and invasion, we untangled the effects of each through time. We found that the co-occurring disturbance of logging can dramatically alter the measured effects of M. vimineum by amplifying, dampening, negating, or entirely reversing the direction of the invader's impacts. During its period of peak impact, logging amplified the invader's positive effect on the size of the soil microbial biomass pool by 24%, reduced the invader's positive effect on soil water holding capacity by 5%, negated the invader's positive effect on the particulate organic matter carbon pool (from a 9% increase to no significant effect), and reversed the direction of the invader's impact on net nitrogen mineralization rate from a 51% increase to a 52% decrease. Furthermore, the influence of logging on the invader's impacts was not static, but dynamic through time. The results from our site therefore demonstrate that failure to account for the impacts of a co-occurring disturbance, as well as the time since disturbance, can result in flawed inference about the nature of an invader's effects. Future research should determine how widespread such flawed inference might be among other invasive species and across different environmental contexts. To help guide such research, we describe a general framework for disentangling the overlapping effects of invasions and co-occurring disturbances through time.