Thinning Can Reduce Losses in Carbon Use Efficiency and Carbon Stocks in Managed Forests Under Warmer Climate
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54 ENVIRONMENTAL SCIENCES↗
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Emerging multiscale insights on microbial carbon use efficiency in the land carbon cycle
Microbial carbon use efficiency (CUE) affects the fate and storage of carbon in terrestrial ecosystems, but its global importance remains uncertain. Accurately modeling and predicting CUE on a global scale is challenging due to inconsistencies in measurement techniques and the complex interactions of climatic, edaphic, and biological factors across scales. The link between microbial CUE and soil organic carbon relies on the stabilization of microbial necromass within soil aggregates or its association with minerals, necessitating an integration of microbial and stabilization processes in modeling approaches. In this perspective, we propose a comprehensive framework that integrates diverse data sources, ranging from genomic information to traditional soil carbon assessments, to refine carbon cycle models by incorporating variations in CUE, thereby enhancing our understanding of the microbial contribution to carbon cycling.
54 ENVIRONMENTAL SCIENCES↗
Clarifying the interpretation of carbon use efficiency in soil through methods comparison
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Geyer, Kevin M. (ORCID:0000000252182745)↗
Stoichiometry of microbial carbon use efficiency in soils
The carbon use efficiency (CUE) of microbial communities partitions the flow of C from primary producers to the atmosphere, decomposer food webs, and soil C stores. CUE, usually defined as the ratio of growth to assimilation, is a critical parameter in ecosystem models, but is seldom measured directly in soils because of the methodological difficulty of measuring in situ rates of microbial growth and respiration. Alternatively, CUE can be estimated indirectly from the elemental stoichiometry of organic matter and microbial biomass, and the ratios of C to nutrient-acquiring ecoenzymatic activities. In this paper, we used this approach to estimate and compare microbial CUE in >2000 soils from a broad range of ecosystems. Mean CUE based on C:N stoichiometry was 0.269 ± 0.110 (mean ± SD). A parallel calculation based on C:P stoichiometry yielded a mean CUE estimate of 0.252 ± 0.125. The mean values and frequency distributions were similar to those from aquatic ecosystems, also calculated from stoichiometric models, and to those calculated from direct measurements of bacterial and fungal growth and respiration. CUE was directly related to microbial biomass C with a scaling exponent of 0.304 (95% CI 0.237–0.371) and inversely related to microbial biomass P with a scaling exponent of -0.234 (95% CI -0.289 to -0.179). Relative to CUE, biomass specific turnover time increased with a scaling exponent of 0.509 (95% CI 0.467–0.551). CUE increased weakly with mean annual temperature. CUE declined with increasing soil pH reaching a minimum at pH 7.0, then increased again as soil pH approached 9.0, a pattern consistent with pH trends in the ratio of fungal : bacteria abundance and growth. Structural equation models that related geographic variables to CUE component variables showed the strongest connections for paths linking latitude and pH to β-glucosidase activity and soil C:N:P ratios. Finally, the integration of stoichiometric and metabolic models provides a quantitative description of the functional organization of soil microbial communities that can improve the representation of CUE in microbial process and ecosystem simulation models.
54 ENVIRONMENTAL SCIENCES↗
Microbial carbon use efficiency promotes global soil carbon storage
Soils store more carbon than other terrestrial ecosystems. How soil organic carbon (SOC) forms and persists remains uncertain, which makes it challenging to understand how it will respond to climatic change. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved. Here we examine the relationship between CUE and the preservation of SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis. We find that CUE is at least four times as important as other evaluated factors, such as carbon input, decomposition or vertical transport, in determining SOC storage and its spatial variation across the globe. In addition, CUE shows a positive correlation with SOC content. Our findings point to microbial CUE as a major determinant of global SOC storage. Understanding the microbial processes underlying CUE and their environmental dependence may help the prediction of SOC feedback to a changing climate.
63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTAN↗
Testing the relationship between carbon-use efficiency and soil carbon formation in rhizosphere and detritusphere microbial communities
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Biological and medical sciences, Chemistry - Isoto↗
Soil carbon formation is promoted by saturation deficit and existing mineral-associated carbon, not by microbial carbon-use efficiency
Mineral-associated organic carbon (MAOC) is the largest terrestrial pool of organic carbon, yet controls on its formation remain unresolved. Existing MAOC is thought to preclude additional C storage on minerals, but this perspective is difficult to reconcile with observations that MAOC stacks in multilayers, suggesting that existing MAOC could promote greater C retention. Here, in a manipulative experiment using 118 soils from 15 agricultural sites across the United States, we show that MAOC formation is promoted by both existing MAOC and its counterpart—MAOC saturation deficit. The positive effect of existing MAOC on the formation of new MAOC persists after accounting for soil physicochemical properties that covary with MAOC. In contrast with current theory, we found that MAOC formation was not clearly influenced by microbial carbon-use efficiency (CUE). Our findings demonstrate that existing MAOC and saturation deficit, not microbial CUE, are key to determining new MAOC formation in agricultural soils.
King, Alison E. [Colorado State Univ., Fort Collin↗
Modeling adaptation of carbon use efficiency in microbial communities
In new microbial-biogeochemical models, microbial carbon use efficiency (CUE) is often assumed to decline with increasing temperature. Under this assumption, soil carbon losses under warming are small because microbial biomass declines. Yet there is also empirical evidence that CUE may adapt (i.e., become less sensitive) to warming, thereby mitigating negative effects on microbial biomass. To analyze potential mechanisms of CUE adaptation, I used two theoretical models to implement a tradeoff between microbial uptake rate and CUE. This rate-yield tradeoff is based on thermodynamic principles and suggests that microbes with greater investment in resource acquisition should have lower CUE. Microbial communities or individuals could adapt to warming by reducing investment in enzymes and uptake machinery. Consistent with this idea, a simple analytical model predicted that adaptation can offset 50% of the warming-induced decline in CUE. To assess the ecosystem implications of the rate-yield tradeoff, I quantified CUE adaptation in a spatially-structured simulation model with 100 microbial taxa and 12 soil carbon substrates. This model predicted much lower CUE adaptation, likely due to additional physiological and ecological constraints on microbes. In particular, specific resource acquisition traits are needed to maintain stoichiometric balance, and taxa with high CUE and low enzyme investment rely on low-yield, high-enzyme neighbors to catalyze substrate degradation. In contrast to published microbial models, simulations with greater CUE adaptation also showed greater carbon storage under warming. This pattern occurred because microbial communities with stronger CUE adaptation produced fewer degradative enzymes, despite increases in biomass. Thus, the rate-yield tradeoff prevents CUE adaptation from driving ecosystem carbon loss under climate warming.
59 BASIC BIOLOGICAL SCIENCES↗
Reduced carbon use efficiency and increased microbial turnover with soil warming
Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial-enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades-long field observations, contrast with values obtained from short-term laboratory experiments. We also show that long-term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion-derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of <1.0% on average (1 st and 3 rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadal datasets. This approach can potentially be applied in broader spatiotemporal scales to improve long-term projections of soil C feedbacks to climate warming.
54 ENVIRONMENTAL SCIENCES↗
Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production
Summary The carbon use efficiency of plants ( CUE a ) and microorganisms ( CUE h ) determines rates of biomass turnover and soil carbon sequestration. We evaluated the hypothesis that CUE a and CUE h counterbalance at a large scale, stabilizing microbial growth (μ) as a fraction of gross primary production ( GPP ). Collating data from published studies, we correlated annual CUE a , estimated from satellite imagery, with locally determined soil CUE h for 100 globally distributed sites. Ecosystem CUE e , the ratio of net ecosystem production ( NEP ) to GPP , was estimated for each site using published models. At the ecosystem scale, CUE a and CUE h were inversely related. At the global scale, the apparent temperature sensitivity of CUE h with respect to mean annual temperature ( MAT ) was similar for organic and mineral soils (0.029°C −1 ). CUE a and CUE e were inversely related to MAT , with apparent sensitivities of −0.009 and −0.032°C −1 , respectively. These trends constrain the ratio μ : GPP (= (CUE a × CUE h )/(1 − CUE e )) with respect to MAT by counterbalancing the apparent temperature sensitivities of the component processes. At the ecosystem scale, the counterbalance is effected by modulating soil organic matter stocks. The results suggest that a μ : GPP value of c . 0.13 is a homeostatic steady state for ecosystem carbon fluxes at a large scale.
Sinsabaugh, Robert L.↗
Microbial diversity drives carbon use efficiency in a model soil
Abstract 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.
54 ENVIRONMENTAL SCIENCES↗
Diverging climate response of corn yield and carbon use efficiency across the U.S.
Abstract In this paper, we developed an open-source package to analyze the overall trend and responses of both carbon use efficiency (CUE) and corn yield to climate factors for the contiguous United States. Our algorithm enables automatic retrieval of remote sensing data through the Google Earth Engine (GEE) and U.S. Department of Agriculture (USDA) agricultural production data at the county level through application programming interface (API). Firstly, we integrated satellite products of net primary productivity and gross primary productivity based on the Moderate Resolution Imaging Spectroradiometer (MODIS) sensor, and climatic variables from the European Centre for Medium-Range Weather Forecasts. Secondly, we calculated CUE and commonly used climate metrics. Thirdly, we investigated the spatial heterogeneity of these variables. We applied a random forest algorithm to identify the key climate drivers of CUE and crop yield, and estimated the responses of CUE and yield to climate variability using the spatial moving window regression across the U.S. Our results show that growing degree days (GDD) has the highest predictive power for both CUE and yield, while extreme degree days (EDD) is the least important explanatory variable. Moreover, we observed that in most areas of the U.S., yield increases or stays the same with higher GDD and precipitation. However, CUE decreases with higher GDD in the north and shows more mixed and fragmented interactions in the south. Notably, there are some exceptions where yield is negatively correlated with precipitation in the Missouri and Mississippi River Valleys. As global warming continues, we anticipate a decrease in CUE throughout the vast northern part of the country, despite the possibility of yield remaining stable or increasing.
54 ENVIRONMENTAL SCIENCES↗
Carbon use efficiency diagnostics in Nannochloropsis salina
We report that carbon dioxide (CO 2 ) can be a significant resource input affecting the cost of algae biomass production on an industrial scale. Improvements in biofuel productivity therefore require characterization of CO 2 use efficiency (CUE). RuBisCO saturation with CO 2 is an important factor influencing biomass productivity. During CO2 fixation by RuBisCO, fractionation of carbon isotopes occurs, with preferential fixation of 12 CO 2 , resulting in assimilation of the lighter isotope in algae. This photosynthetic discrimination (Δ DIC-algae ), approximated by the difference between the δ 13 C of external medium and that of algae, is a function of the proportion of CO 2 fixed relative to supply. Δ DIC-algae has been applied to the study of photosynthesis in algae over the past few decades and we have adopted the tool to characterize improvements in conditions optimized for biofuel productivity, such as controlled photobioreactors. We report the use of Δ DIC-algae as a tool for characterizing CO 2 dynamics and RuBisCO saturation in Nannochloropsis salina CCMP 1776, a benchmark strain in algal biofuels research. We use Δ DIC-algae to describe the conditions under which RuBisCO saturation can be achieved to maximize biomass productivity. Finally, our results suggest that determination of Δ DIC-algae can provide important feedback to support engineering and cultural improvements that can impact carbon use efficiency and biomass productivity.
09 BIOMASS FUELS↗
In situ diversity of metabolism and carbon use efficiency among soil bacteria
The central carbon (C) metabolic network harvests energy to power the cell and feed biosynthesis for growth. In pure cultures, bacteria use some but not all of the network’s major pathways, such as glycolysis and pentose phosphate and Entner-Doudoroff pathways. However, how these pathways are used in microorganisms in intact soil communities is unknown. Here, we analyzed the incorporation of 13 C from glucose isotopomers into phospholipid fatty acids. We showed that groups of Gram-positive and Gram-negative bacteria in an intact agricultural soil used different pathways to metabolize glucose. They also differed in C use efficiency (CUE), the efficiency with which a substrate is used for biosynthesis. Our results provide experimental evidence for diversity among microbes in the organization of their central carbon metabolic network and CUE under in situ conditions. These results have important implications for our understanding of how community composition affects soil C cycling and organic matter formation.
59 BASIC BIOLOGICAL SCIENCES↗
Nitrogen availability and summer drought, but not N:P imbalance, drive carbon use efficiency of a Mediterranean tree-grass ecosystem
All ecosystems contain both sources and sinks for atmospheric carbon (C). A change in their balance of net and gross ecosystem carbon uptake, ecosystem-scale carbon use efficiency (CUE ECO ), is a change in their ability to buffer climate change. However, anthropogenic nitrogen (N) deposition is increasing N availability, potentially shifting terrestrial ecosystem stoichiometry towards phosphorus (P) limitation. Depending on how gross primary production (GPP, plants alone) and ecosystem respiration (R ECO , plants and heterotrophs) are limited by N, P or associated changes in other biogeochemical cycles, CUE ECO may change. Seasonally, CUE ECO also varies as the multiple processes that control GPP and respiration and their limitations shift in time. We worked in a Mediterranean tree-grass ecosystem (locally called ‘dehesa’) characterized by mild, wet winters and summer droughts. We examined CUE ECO from eddy covariance fluxes over 6 years under control, +N and + NP fertilized treatments on three timescales: annual, seasonal (determined by vegetation phenological phases) and 14-day aggregations. Finer aggregation allowed consideration of responses to specific patterns in vegetation activity and meteorological conditions. We predicted that CUE ECO should be increased by wetter conditions, and successively by N and NP fertilization. Milder and wetter years with proportionally longer growing seasons increased CUE ECO , as did N fertilization, regardless of whether P was added. Using a generalized additive model, whole ecosystem phenological status and water deficit indicators, which both varied with treatment, were the main determinants of 14-day differences in CUE ECO . The direction of water effects depended on the timescale considered and occurred alongside treatment-dependent water depletion. Overall, future regional trends of longer dry summers may push these systems towards lower CUE ECO .
59 BASIC BIOLOGICAL SCIENCES↗
Assessing microbial residues in soil as a potential carbon sink and moderator of carbon use efficiency
Abstract A longstanding assumption of glucose tracing experiments is that all glucose is microbially utilized during short incubations of ≤2 days to become microbial biomass or carbon dioxide. Carbon use efficiency (CUE) estimates have consequently ignored the formation of residues (non-living microbial products) although such materials could represent an important sink of glucose that is prone to stabilization as soil organic matter. We examined the dynamics of microbial residue formation from a short tracer experiment with frequent samplings over 72 h, and conducted a meta-analysis of previously published glucose tracing studies to assess the generality of these experimental results. Both our experiment and meta-analysis indicated 30–34% of amended glucose-C ( 13 C or 14 C) was in the form of residues within the first 6 h of substrate addition. We expand the conventional efficiency calculation to include residues in both the numerator and denominator of efficiency, thereby deriving a novel metric of the potential persistence of glucose-C in soil as living microbial biomass plus residues (‘carbon stabilization efficiency’). This new metric indicates nearly 40% of amended glucose-C persists in soil 180 days after amendment, the majority as non-biomass residues. Starting microbial biomass and clay content emerge as critical factors that positively promote such long term stabilization of labile C. Rapid residue production supports the conclusion that non-growth maintenance activity can illicit high demands for C in soil, perhaps equaling that directed towards growth, and that residues may have an underestimated role in the cycling and sequestration potential of C in soil.
Geyer, Kevin (ORCID:0000000252182745)↗
Microbial carbon use efficiency predicted from genome-scale metabolic models
Abstract 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.
59 BASIC BIOLOGICAL SCIENCES↗
Data from Microbial Carbon Use Efficiency Predicted from Genome-Scale Metabolic Models
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.
Metabolomics↗