Higher Carbon Use Efficiency Research Articles

Changes in microbial physiology and carbon-use efficiency upon improving soil habitat conditions in conservation farming systems

The interplay between soil microbial anabolism and metabolism has recently been postulated as an important lever for carbon sequestration in soils. Theoretical considerations suggest that high microbial growth rates and a high carbon-use efficiency (CUE) are associated with increased soil organic carbon (SOC) build-up in arable soils. Nature-oriented conservation agricultural practices are believed to facilitate this microbial-driven process of SOC accrual; a practical validation of this postulation is however missing. Against this background, we evaluated the effect of agricultural management and site-specific soil chemical and physical properties on microbial physiology (i.e., respiration, bacterial and fungal growth rates, and microbial biomass turnover) and CUE by an on-farm comparison of conventional farming, conservation farming and unmanaged reference soil systems (i.e., adjacent field margins) at twenty-one sites across three soil depths. We show that a change in agricultural management towards soil health regeneration has a significant impact on microbial physiology. Bacterial growth, respiration and microbial biomass turnover increased from conventional farming towards conservation farming systems to reference soils. The opposite trend however was found for fungal growth and microbial CUE, with highest values observed in conventional farming systems. This clearly contradicts the prevailing idea that higher microbial CUE in conservation farming systems may be associated with higher SOC contents. Our results further show that soil physical and chemical parameters such as soil pH, texture and dissolved carbon compounds strongly predict microbial CUE. In line with these results, functional pore domains showed specific optima for microbial growth and CUE. For example, a high share of small pore domains hampered fungal growth and reduced microbial CUE but facilitated microbial biomass turnover at the same time. Thus, we suggest that – superimposed upon agricultural management effects – habitat structural conditions and microbial carbon limitation mainly shape microbial physiology and CUE in arable soil systems.

Long-term integrated crop-livestock grazing stimulates soil ecosystem carbon flux, increasing subsoil carbon storage in California perennial agroecosystems

The strategic use of ruminant grazing in perennial cropland is steadily increasing throughout Mediterranean perennial agroecosystems. Integrated sheep-vineyard (ISV) management, where small ruminant livestock graze on understory vegetation, is viewed by some practitioners as a feasible transition opportunity to facilitate less petrochemically intensive vineyard understory management. However, our knowledge of soil carbon dynamics associated with grazing in perennial integrated crop-livestock (ICL) agroecosystems is notably limited, especially within Mediterranean climate contexts. Here, we use a series of on-farm paired surveys to assess soil ecosystem habitat and resource conditions related to SOC flux and storage in vineyards utilizing sheep-integration (ISV) and conventional understory management techniques (CONV). Our results show that long-term grazing increased the quantity of active, labile, and soluble carbon (C) within ISV soils, with much higher quantities of microbial biomass carbon (MBC). Vineyard soils with sheep grazing also showed increases in phospholipid fatty acid (PLFA) biomarkers, particularly amongst core functional groups related to decomposition. Soil microbial communities under ISV had higher C mineralization rates as well as higher carbon use-efficiency, as indicated by less CO2-C respired relative to the size of the MBC pool. Whereas inorganic soil nitrogen (N) and phosphorous (P) were also higher under ISV, microbial communities showed distinct metabolic investment strategies related to nutrient acquisition, with lower P-cycling enzyme activity and higher N-cycling enzyme activity. Additionally, ISV resulted in an increase in subsoil SOC storage, including higher quantities of physicochemical stabilization in the mineral-associated organic carbon (MAOC) pool of the deepest measured subsoil layer (30–45 cm). We observed no differences in soil structure indicators between treatments nor differences in the carbon fractions associated with four distinct aggregate size categories. We propose a framework to explain observed shifts in SOC dynamics of perennial ICL systems that include i) deposition of C and nutrient inputs with higher lability and solubility; ii) ruminant-induced decoupling of C from N and P, resulting in increased nutrient bioavailability; and iii) altered soil microbial metabolic strategies with more efficient biomass accumulation. These findings show strong potential of strategically applied ICL grazing to enhance soil functioning and increase SOC storage in Mediterranean perennial agroecosystems.

Microbial carbon use efficiency of glucose varies with soil clay content: A meta-analysis

Soil organic matter (SOM) decomposition and stabilisation are largely affected by microbial carbon use efficiency (CUE), which is defined as the proportion of substrate carbon (C) uptake that microbes use for growth. Microbial CUE varies due to substrate quality and availability differences, but this may also depend on soil properties, such as pH, soil organic C (SOC) and clay content. We conducted a meta-analysis using data from 26 publications and analysed 272 CUE observations to investigate whether the substrate type has a distinct effect on microbial CUE and how CUE varies with the amount of substrate application and soil factors (pH, SOC, and clay content). We observed large variations in the CUE among different substrates, but we could not discern clear associations with substrate complexity, nitrogen, and energy content. Most of the studies used glucose as the substrate. The CUE of glucose significantly increased with decreasing amount of substrate applied and increasing clay content. We further observed a significant increase in glucose CUE with increased soil pH and decreased SOC content, although these relationships were relatively weak. Overall, our findings suggest the possibility of rapid adsorption of glucose or microbial products derived from glucose, which would then reduce substrate availability to microbes and increase CUE. The combined effects of greater adsorption and higher CUE with increased clay content would therefore result in more C stabilisation. We emphasise the need for including rapid adsorption of substrates and their microbial products when investigating substrate-specific microbial CUE.

Long-Term Tillage and Irrigation Management Practices: Impact on Carbon Budgeting and Energy Dynamics under Rice–Wheat Rotation of Indian Mid-Himalayan Region

In modern agriculture, reducing the carbon footprint and emission of greenhouse gases with greater energy efficiency are major issues for achieving the sustainability of agricultural production systems. To address this issue, a long-term field experiment was established from 2001 through 2016 with two contrasting tillage practices (ZT: zero tillage; CT: conventional tillage) and four irrigation schedules {I-1: pre-sowing (PS), I-2: PS + crown root initiation (CRI), I-3: PS + CRI + panicle initiation (PI)/flowering (FL), and I-4: PS + CRI + PI/FL + grain filling (GF)}. The grain yield of rice, wheat and the rice–wheat system was increased significantly by 23.6, 39.5 and 32.8%, respectively, with irrigation at four stages (I-4) compared to a single stage (I-1). Energy appraisal results exhibited that 17.2% higher energy was consumed under CT as compared to ZT (25,894 MJ ha−1). Fertilizer application consumed the highest energy (46.5–54.5%), followed by irrigation (8.83–19.5%), and the lowest energy consumption was associated with winnowing, packing and transport (2.07–2.43%) operations. The total energy output of the rice–wheat system did not change significantly among contrast tillage, but higher energy was obtained under CT (214,603 MJ ha−1) as compared to ZT (209,728 MJ ha−1). ZT practice improved the energy use efficiency (EUE), energy productivity (Ep) and energy profitability (Eprof) by 16.6, 21.0 and 16.6%, respectively, over CT. The EUE, SE (specific energy), Ep, net energy return (NER) and Eprof were enhanced by 17.1, 16.6, 21.0, 36.5 and 20.6%, respectively, with irrigation at four stages (I-4) compared to a single stage (I-1). Zero tillage plots reflected a 8.24% higher carbon use efficiency (CUE) and a 9.0% lower carbon footprint than CT plots. Among irrigation schedules, application of I-4 showed a 8.13% higher CUE and a 9.0% lower carbon footprint over single irrigation (I-1). This investigation indicated that ZT with irrigation at four stages (I-4) was the most sustainable option for improving the EUE and CUE with minimal GHGs emissions from the rice–wheat cropping system of Indian mid-Himalayan regions.

Pyrogenic conversion of rice straw and wood to biochar increases aromaticity and carbon accumulation in soil

Open field burning of rice straw besides causing environmental pollution and human health problems results in loss of organic carbon and essential nutrients. Urgent solution is required for management of rice straw in an eco-friendly and sustainable manner. The aim of the present study was to examine the efficiency of direct return of rice straw into the soil versus biochar generated from rice straw, and compare it with wood derived biochar in influencing soil biological processes and potential to accumulate soil organic C (SOC). We studied the effect of pyrogenic conversion of rice straw and wood chips to biochar on changes in chemical composition of feedstock by Fourier Transform Infrared (FTIR) spectroscopy and C and N mineralization kinetics, microbial metabolism, carbon use efficiency (CUE) and soil enzyme activities in a series of laboratory incubation experiments conducted at 25 °C temperature and field capacity moisture. Pyrogenic conversion of feedstock to biochar resulted in increase in C (39.6% to 69.2%) and N (0.4% to 1.65%) contents and lowering of C/N (99 to 28.4) and H/C (1.94 to 0.60) ratios. Charring resulted in decrease in aliphatic and increase in aromatic components. Decomposition of organic substrates was governed by aromaticity and C/N ratio; in 127 days, only 12% of rice straw biochar embodied C was mineralized as against 76% from rice straw. The addition of biochars resulted in soil N priming (120 ± 24 mg N kg−1) whereas straw application resulted in net N immobilization (−13 mg N kg−1). Compared to unpyrogenic straw, the rice straw biochar led to greater microbial growth, lower metabolic quotient, higher CUE (3.3 times) and decreased microbial respiration, with potential to promote SOC accumulation. It was concluded that addition of rice residue generated biochar into soil is more beneficial for soil biological processes and SOC stabilization to stymie climate change than direct return of plant residue into the soil. The results are significant for devising eco-friendly rice residue management practices in the Indo-Gangetic plains.

Microbial carbon use efficiency during plant residue decomposition: Integrating multi-enzyme stoichiometry and C balance approach

Accurate estimation of microbial carbon use efficiency (CUE) in soil is challenged by a high degree of genetic and environmental variability. Different methods vary in their estimates of soil microbial CUE giving the room to select the optimal method for a specific research task, while integrating different methods could improve our understanding of processes controlling CUE variability. Aiming to estimate CUE during plant residue decomposition in different soils, we applied the conventional C-balance method, single C-cycling enzymatic stoichiometry (SCE-STM) and newly proposed “multi”-C-cycling enzymatic stoichiometry (MCE-STM) methods. The STM approach derives CUE from elemental ratios of microbial biomass, substrate, and activities of C and nutrient (e.g. N) acquiring exoenzymes. The extended MCE-STM is a modification of the SCE-STM method, where we used the sum of three C-cycling enzymatic activities (β-glucosidase (BGL), β-D-cellobiohydrolase (BCL), β-xylosidase (BXL)) as proxy for CUE calculation, instead of using a single C-acquiring enzyme (BGL). We hypothesized that MCE-STM provides a more reliable estimation of microbial CUE in soils amended with complex plant residues than the SCE-STM or the C balance approach. The comparison of methods was done in a laboratory incubation experiment, using two soils differing mainly in acidity level mixed with two specimen of plant residues differing in lignin (L) and polyphenol (PP) content. We anticipated a higher microbial CUE in less acidic (pH 5.1) soil amended with higher quality (lower (L + PP)/N) ratio)) plant residues than in more acidic (pH 4.3) soils amended with medium quality (higher (L + PP)/N ratio) plant residues, due to less energy investment in microbial metabolism in the former case. Microbial CUE estimations were completed at 7, 15, 30, 45 and 60 days. Lower CUE values (0.09–0.18) were recorded by MCE-STM as compare to those (0.24–0.47) obtained by C-balance and SCE-STM methods. Irrespective of applied CUE estimation methods, higher CUE was recorded in less acidic (pH 5.1) soil amended with residues of higher quality than the other three combinations. Microorganisms invested more energy to support growth in low pH soil in order to tolerate soil acidity, which, in turn, suppressed N-acquiring enzymatic activity and further decreased CUE. The modification of the MCE-STM method for CUE determination proposed in this work was capable to quantify the combined effect of soil pH and plant residue quality on efficiency of microbial metabolism. It, therefore, can be considered as viable alternative to the original stoichiometric modeling approach (SCE-STM).

Spatial variations and controls of carbon use efficiency in China\u2019s terrestrial ecosystems

Carbon use efficiency (CUE), one of the most important eco-physiological parameters, represents the capacity of plants to transform carbon into new biomass. Understanding the variations and controls of CUE is crucial for regional carbon assessment. Here, we used 15-years of continuous remote sensing data to examine the variations of CUE across broad geographic and climatic gradients in China. The results showed that the vegetation CUE was averaged to 0.54 ± 0.11 with minor interannual variation. However, the CUE greatly varied with geographic gradients and ecosystem types. Forests have a lower CUE than grasslands and croplands. Evergreen needleleaf forests have a higher CUE than other forest types. Climate factors (mean annual temperature (MAT), precipitation (MAP) and the index of water availability (IWA)) dominantly regulated the spatial variations of CUE. The CUE exhibited a linear decrease with enhanced MAT and MAP and a parabolic response to the IWA. Furthermore, the responses of CUE to environmental change varied with individual ecosystem type. In contrast, precipitation exerted strong control on CUE in grassland, while in forest and cropland, the CUE was mainly controlled by the available water. This study identifies the variations and response of CUE to environmental drivers in China, which will be valuable for the regional assessment of carbon cycling dynamics under future climate change.

Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally.

The degree to which climate warming will stimulate soil organic carbon (SOC) losses via heterotrophic respiration remains uncertain, in part because different or even opposite microbial physiology and temperature relationships have been proposed in SOC models. We incorporated competing microbial carbon use efficiency (CUE)-mean annual temperature (MAT) and enzyme kinetic-MAT relationships into SOC models, and compared the simulated mass-specific soil heterotrophic respiration rates with multiple published datasets of measured respiration. The measured data included 110 dryland soils globally distributed and two continental to global-scale cross-biome datasets. Model-data comparisons suggested that a positive CUE-MAT relationship best predicts the measured mass-specific soil heterotrophic respiration rates in soils distributed globally. These results are robust when considering models of increasing complexity and competing mechanisms driving soil heterotrophic respiration-MAT relationships (e.g., carbon substrate availability). Our findings suggest that a warmer climate selects for microbial communities with higher CUE, as opposed to the often hypothesized reductions in CUE by warming based on soil laboratory assays. Our results help to build the impetus for, and confidence in, including microbial mechanisms in soil biogeochemical models used to forecast changes in global soil carbon stocks in response to warming.

Understanding the controls over forest carbon use efficiency on small spatial scales: Effects of forest disturbance and tree diversity

Tropical forests are characterized by their high photosynthetic activity. Results from pantropical studies show that on average only 30% of the products from photosynthesis are allocated to new biomass compared to on average 50% in temperate forest systems. Why those forests have a low carbon use efficiency (CUE) remains unknown. We present a synthesis of studies from two tropical sites with a similar methodological setup allowing the evaluation of the ecophysiological responses of tree communities to diversity effects and forest disturbance. Here we use xylem sap flux derived gross primary productivity (GPP) that was modeled with eddy covariance data for a seven-year-old planted forest with plots of varying tree species diversity in Panama and an old-growth forest with a distinct disturbance gradient in an Amazonian moist lowland forest. Additionally, net primary productivity (NPP) was calculated from inventory data. We found evidence that GPP is relatively stable with forest disturbance but GPP increases with tree species richness. Lowest CUE with only 35% of GPP allocated to growth was present in undisturbed forest patches. Light forest disturbance had a positive effect on CUE and 62% of GPP was allocated to grow new biomass. Monospecific stands had a higher CUE than diverse tree stands. We conclude that two factors are controlling CUE in tropical forests leading to low CUE. First, forest disturbance leads to a higher allocation of carbon towards growth. Second, a great fraction of GPP is used for processes dedicated to species complementarity. This improves the overall performance of diverse forest stands compared to monocultures.

Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry

Microbial decomposers are responsible for the breakdown of organic matter (OM) and thus regulate soil carbon (C) stocks. During the decomposition of OM, microorganisms can use the assimilated C for biomass production or respire it as CO2, and the fraction of growth to total assimilation defines the microbial carbon-use efficiency (CUE). As such, CUE has direct consequences for how microbial decomposers affect the balance of C between atmosphere and soil. We estimated fungal and bacterial growth in C units in microcosm systems with submerged plant litter. We established conversion factors between bacterial and fungal growth to biomass and applied this to a dataset representing 9 different sites in temperate forest soils, temperate agricultural soils, and subarctic forest soils, to estimate growth rates of fungi and bacteria in units of C, to estimate the dominance of the two decomposer groups, and to compare these values to respiration to estimate the microbial CUE. We observed that fungal-to-bacterial growth ratios (F:B) ranged from 0.02 to 0.44, and that the fungal dominance was higher in soils with lower C:N ratio and higher C-quality. We found a negative exponential relationship between the dominance of fungi and the microbial CUE. CUE ranged from 0.03 to 0.30, and values clustered most strongly according to site rather than level of soil N. CUE was higher in soil with high C:N ratio and high C-quality. However, within each land-use type, a high mineral N-content did result in lower F:B and higher resulting CUE. In conclusion, a higher soil C-quality coincided with lower F:B and higher CUE across the surveyed sites, while a higher N availability did not. A higher N availability resulted in higher CUE and lower F:B within each site suggesting that site-specific differences such as the effect of plant community via e.g. plant litter and rhizosphere input, overrode the influence of N-availability.

Sorption of Alanine changes microbial metabolism in addition to availability

Sorption is one of the main processes stabilizing organic matter in soil against microbial mineralization. We hypothesize that besides reduced accessibility for microorganisms and enzymes, changes in microbial metabolism additionally intensify this organic matter stabilization effect of sorption.Position-specifically 14C labeled Alanine was applied to soil as solution or sorbed on sterilized soil to investigate the mechanisms underlying this metabolism related stabilization effect. Sorption decreased initial mineralization of Alanine by ~80% and doubled the duration until the mineralization maxima (14CO2 peak). Almost all Alanine was taken up by microorganisms independent on sorption, and C‐1 was completely (>99%) decarboxylated during glycolysis after one day. Sorption could not prevent microbial utilization of Alanine, but increased the carbon use efficiency (CUE) of sorbed Alanine for 60% compared to Alanine in solution and increased C incorporation in microbial biomass up to four times. The position-specific pattern of 14C in soil and in microbial biomass showed that oxidation of C-2 from sorbed Alanine was strongly lowered compared to free Alanine. Both higher CUE and delayed C-2 mineralization were achieved by a higher C flux towards efficient anabolism, or/and to slower cycling cell components.Limitation of accessibility for microorganisms alone does not explain the stabilizing effect of sorption on organic substances like amino acids and the observed changed position specific pattern. Even though all sorbed Alanine was taken up by microorganisms within 3days, C partitioning towards anabolism, slower microbial turnover and increased CUE increased C retention from sorbed compounds in soil even after microbial uptake. Position-specific labeling clearly showed that LMWOS are stabilized by sorption not as intact molecules, but after microbial metabolization – as released metabolites or microbial biomass. We conclude that the indirect effects of sorption, namely 1) more C partitioned to anabolism, 2) slower decomposition, 3) higher incorporation into microbial biomass and 4) increased carbon use efficiency promote C retention in soil and may be even more important than the direct effect, namely inaccessibility. The finding that stabilization did not significantly impede microbial utilization, but sorption greatly increased carbon use efficiency has major implications for conceptual and numerical representation of organic matter stabilization and losses in soils.

Does declining carbon‐use efficiency explain thermal acclimation of soil respiration with warming?

Enhanced soil respiration in response to global warming may substantially increase atmospheric CO2 concentrations above the anthropogenic contribution, depending on the mechanisms underlying the temperature sensitivity of soil respiration. Here, we compared short-term and seasonal responses of soil respiration to a shifting thermal environment and variable substrate availability via laboratory incubations. To analyze the data from incubations, we implemented a novel process-based model of soil respiration in a hierarchical Bayesian framework. Our process model combined a Michaelis-Menten-type equation of substrate availability and microbial biomass with an Arrhenius-type nonlinear temperature response function. We tested the competing hypotheses that apparent thermal acclimation of soil respiration can be explained by depletion of labile substrates in warmed soils, or that physiological acclimation reduces respiration rates. We demonstrated that short-term apparent acclimation can be induced by substrate depletion, but that decreasing microbial biomass carbon (MBC) is also important, and lower MBC at warmer temperatures is likely due to decreased carbon-use efficiency (CUE). Observed seasonal acclimation of soil respiration was associated with higher CUE and lower basal respiration for summer- vs. winter-collected soils. Whether the observed short-term decrease in CUE or the seasonal acclimation of CUE with increased temperatures dominates the response to long-term warming will have important consequences for soil organic carbon storage.

TEMPERATURE EFFECTS ON PHOTOSYNTHESIS, GROWTH RESPIRATION, AND MAINTENANCE RESPIRATION OF MARIGOLD

TEMPERATURE EFFECTS ON PHOTOSYNTHESIS, GROWTH RESPIRATION, AND MAINTENANCE RESPIRATION OF MARIGOLD