Carbon Use Efficiency In Soil Research Articles

The size and diversity of microbes determine carbon use efficiency in soil.

Soil is home to a multitude of microorganisms from all three domains of life. These organisms and their interactions are crucial in driving the cycling of soil carbon. One key indicator of this process is Microbial Carbon Use Efficiency (CUE), which shows how microbes influence soil carbon storage through their biomass production. Although CUE varies among different microorganisms, there have been few studies that directly examine how biotic factors influence CUE. One such factor could be body size, which can impact microbial growth rates and interactions in soil, thereby influencing CUE. Despite this, evidence demonstrating a direct causal connection between microbial biodiversity and CUE is still scarce. To address these knowledge gaps, we conducted an experiment where we manipulated microbial body size and biodiversity through size-selective filtering. Our findings show that manipulating the structure of the microbial community can reduce CUE by approximately 65%. When we restricted the maximum body size of the microbial community, we observed a reduction in bacterial diversity and functional potential, which in turn lowered the community's CUE. Interestingly, when we included large body size micro-eukarya in the soil, it shifted the soil carbon cycling, increasing CUE by approximately 50% and the soil carbon to nitrogen ratio by about 25%. Our metrics of microbial diversity and community structure were able to explain 36%-50% of the variation in CUE. This highlights the importance of microbial traits, community structure and trophic interactions in mediating soil carbon cycling.

Active microbial population dynamics and life strategies drive the enhanced carbon use efficiency in high-organic matter soils.

Microbial carbon use efficiency (CUE) is a critical parameter that controls carbon storage in soil, but many uncertainties remain concerning adaptations of microbial communities to long-term fertilization that impact CUE. Based on H218O quantitative stable isotope probing coupled with metagenomic sequencing, we disentangled the roles of active microbial population dynamics and life strategies for CUE in soils after a long-term (35 years) mineral or organic fertilization. We found that the soils rich in organic matter supported high microbial CUE, indicating a more efficient microbial biomass formation and a greater carbon sequestration potential. Organic fertilizers supported active microbial communities characterized by high diversity and a relative increase in net growth rate, as well as an anabolic-biased carbon cycling, which likely explains the observed enhanced CUE. Overall, these results highlight the role of population dynamics and life strategies in understanding and predicting microbial CUE and sequestration in soil.IMPORTANCEMicrobial CUE is a major determinant of global soil organic carbon storage. Understanding the microbial processes underlying CUE can help to maintain soil sustainable productivity and mitigate climate change. Our findings indicated that active microbial communities, adapted to long-term organic fertilization, exhibited a relative increase in net growth rate and a preference for anabolic carbon cycling when compared to those subjected to chemical fertilization. These shifts in population dynamics and life strategies led the active microbes to allocate more carbon to biomass production rather than cellular respiration. Consequently, the more fertile soils may harbor a greater microbially mediated carbon sequestration potential. This finding is of great importance for manipulating microorganisms to increase soil C sequestration.

Role of an arbuscular mycorrhizal fungus in vegetation restoration as indicated by bacterial diversity and microbial metabolic limitation in soil underlying moss biocrusts

Arbuscular mycorrhizal (AM) fungi contribute to the revegetation of degraded ecosystems such as coal mining areas and may indirectly affect the development of biological soil crusts (biocrusts). However, bacterial diversity and microbial nutrient cycling in the soil underlying biocrusts are seldom considered when assessing ecological restoration effects. Bacterial community composition was quantified and compared using 16S rRNA gene sequencing, metabolic limitation of microbes via extracellular enzymatic stoichiometry and their association with carbon use efficiency (CUE) in soil underlying moss biocrusts in vegetated areas inoculated with an AM fungus or uninoculated and in uninoculated unvegetated areas. The AM fungal inoculum significantly influenced bacterial community composition and diversity, extracellular enzyme activities and CUE in soil underlying moss biocrusts mainly by affecting soil nutrients. Correlation analysis revealed that Actinobacteria, Armatimonadetes, Bacteroidetes, Chlorobi, Cyanobacteria, Saccharibacteria, and Verrucomicrobia were positively correlated with soil nutrients carbon (C), nitrogen (N) and phosphorus (P). A vector analysis of extracellular enzyme activity indicates that soil microbial communities underlying moss biocrusts were limited by P but microbial communities in areas inoculated with the AM fungus had the lowest relative P limitation. The alleviation of microbial P limitation increased the microbial CUE and bacterial phylum community and alpha diversity, leading to an increase in subsoil C content underlying moss biocrusts. This indicates that microbial communities in soil underlying moss biocrusts under in restoration areas containing the AM fungus were more stable under environmental stress, and the inclusion of AM fungal inoculation may be recommended as the preferred option for ecosystem restoration in arid and semi-arid coal mining areas.

Different Response of Soil Microbial Carbon Use Efficiency in Compound of Feldspathic Sandstone and Sand

The stoichiometry of efficient soil microbial carbon use is a sensitive index for measuring changes in soil quality and plays a crucial role in research on ecological stoichiometry in the soil nutrient cycle. To further understand the effect of feldspathic sandstone and sand compound ratios on microbial carbon use efficiency (CUE), we simulated the field conditions of the feldspathic sandstone-sand compound layer in the Mu Us sandy land and analyzed the soil C:N:P ratio, microbial biomass, extracellular enzyme activity, and microbial carbon use efficiency in soils with different compound ratios. The results demonstrated that an increase in the feldspathic sandstone content had insignificant effects on the soil C:N:P ratio. The maximum values for microbial biomass nitrogen (MBN) and microbial biomass phosphorus (MBP) were observed at compound ratios of 1:5 and 1:2, respectively. Calculations of microbial carbon use efficiency and vector analysis revealed that the microbial carbon use efficiency increased as the feldspathic sandstone content increased, P limitation existed in all compound soils, and soil with a 1:1 compound ratio may be substantially less limited. In conclusion, our research indicated that adding feldspathic sandstone to sand improved soil quality, and the compound ratio affected soil microorganisms; nevertheless, it did not significantly change soil nutrient restriction. Our study provides a theoretical basis for the development and utilization of desert land resources.

Nitrogen addition to soil affects microbial carbon use efficiency: Meta-analysis of similarities and differences in 13 C and 18 O approaches.

The carbon use efficiency (CUE) of soil microorganisms is a critical parameter for the first step of organic carbon (C) transformation by and incorporation into microbial biomass and shapes C cycling in terrestrial ecosystems. As C and nitrogen (N) cycles interact closely and N availability affects microbial metabolism, N addition to soil may shift the microbial CUE. We conducted a meta-analysis (100 data pairs) to generalize information about the microbial CUE response to N addition in soil based on the two most common CUE estimation approaches: (i) 13 C-labelled substrate addition (13 C-substrate) and (ii) 18 O-labelled water addition (18 O-H2 O). The mean microbial CUE in soils across all biomes and approaches was 0.37. The effects of N addition on CUE, however, were depended on the approach: CUE decreased by 12% if measured by the 13 C-substrate approach, while CUE increased by 11% if measured by the 18 O-H2 O approach. These differences in the microbial CUE response depending on the estimation approach are explained by the divergent reactions of microbial growth to N addition: N addition decreases the 13 C incorporation into microbial biomass (this parameter is in the numerator by CUE calculation based on the 13 C-substrate approach). In contrast, N addition slightly increases (although statistically insignificant) the microbial growth rate (in the numerator of the CUE calculation when assessed by the 18 O-H2 O approach), significantly raising the CUE. We explained these N addition effects based on CUE regulation mechanisms at the metabolic, cell, community, and ecosystem levels. Consequently, the differences in the microbial responses (microbial growth, respiration, C incorporation, community composition, and dormant or active states) between the 13 C-substrate and 18 O-H2 O approaches need to be considered. Thus, these two CUE estimation approaches should be compared to understand microbially mediated C and nutrient dynamics under increasing anthropogenic N input and other global change effects.

Estimating microbial carbon use efficiency in soil: Isotope-based and enzyme-based methods measure fundamentally different aspects of microbial resource use

How carbon partitions between microbial biomass and CO2 (carbon use efficiency, CUE) is key in all soil carbon cycling models. Traditional methods to estimate CUE focus on the physiological partitioning of specific substrates, typically labeled with isotopes. However, an alternative approach (Sinsabaugh et al., 2016) is based on community-level resource capture using assays of extracellular enzymes; although this uses the same name (CUE), it measures something distinctly different from the isotopic methods. Rather, it assesses how microbes shift resource use in response to substrate stoichiometry.

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).

Heavy and wet: The consequences of violating assumptions of measuring soil microbial growth efficiency using the 18O water method

Soils store more carbon than the biosphere and atmosphere combined, and the efficiency to which soil microorganisms allocate carbon to growth rather than respiration is increasingly considered a proxy for the soil capacity to store carbon. This carbon use efficiency (CUE) is measured via different methods, and more recently, the 18O-H2O method has been embraced as a significant improvement for measuring CUE of soil microbial communities. Based on extrapolating 18O incorporation into DNA to new biomass, this measurement makes various implicit assumptions about the microbial community at hand. Here we conducted a literature review to evaluate how viable these assumptions are and then developed a mathematical model to test how violating them affects estimates of the growth component of CUE in soil. We applied this model to previously collected data from two kinds of soil microbial communities. By changing one parameter at a time, we confirmed our previous observation that CUE was reduced by fungal removal. Our results also show that depending on the microbial community composition, there can be substantial discrepancies between estimated and true microbial growth. Of the numerous implicit assumptions that might be violated, not accounting for the contribution of sources of oxygen other than extracellular water to DNA leads to a consistent underestimation of CUE. We present a framework that allows researchers to evaluate how their experimental conditions may influence their 18O-H2O-based CUE measurements and suggest the parameters that need further constraining to more accurately quantify growth and CUE.

Land-use alters the temperature response of microbial carbon-use efficiency in soils – a consumption-based approach

Soil organic carbon (SOC) is a substantial source of atmospheric CO2, but also a large cause of uncertainties in Earth-system models. A principal control on soil CO2 release is the carbon-use efficiency (CUE) of microbial communities, which partitions the carbon (C) allocation between biosynthetic stabilization and CO2 respiration during SOC decomposition. In Earth-system models, CUE is commonly considered as a constant, although it should be susceptible to environmental factors such as temperature. We explored CUE across a set of land-uses and temperatures, and we show the hitherto neglected phenomenon that land-use can alter the temperature response of CUE. In arable soils, CUE was constant over a temperature range between 5 and 20 °C, but it decreased with temperature in ley farming, grassland, and forest soils at temperatures above 12.5 °C. The decrease in CUE was strongest for forest soils. Implementing our findings into a soil-C model revealed substantial differences in projected SOC losses: Assuming an increase of mean annual temperature of 2 or 4 °C, soils were projected to lose up to 6 or 15% of their current SOC, respectively, until they reach a new steady-state. These projections varied among land-uses. Our findings confront the current representation of CUE in global C models and challenges C sequestration strategies based on land-use changes, because land-uses such as e.g. forest ecosystems with current high C storage may lose substantially more C than agricultural soils due to strong declines of CUE.

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.

Clarifying the interpretation of carbon use efficiency in soil through methods comparison

Accurate estimates of microbial carbon use efficiency (CUE) are required to predict how global change will impact microbially-mediated ecosystem functions such as organic matter decomposition. Multiple approaches are currently used to quantify CUE but the extent to which estimates reflect methodological variability is unknown. This limits our ability to apply or cross-compare published CUE values. Here we evaluated the performance of five methods in a single soil under standard conditions. The microbial response to three substrate amendment rates (0.0, 0.05, and 2.0 mg glucose-C g−1 soil) was examined using: 13C and 18O isotope tracing approaches which estimate CUE based on substrate uptake and growth dynamics; calorespirometry which infers growth and CUE from metabolic heat and respiration rates; metabolic flux analysis where CUE is determined as the balance between biosynthesis and respiration using position-specific 13CO2 production of labeled glucose; and stoichiometric modeling which derives CUE from elemental ratios of microbial biomass, substrate, and exoenzyme activity. The CUE estimates we obtained differed by method and substrate concentration, ranging under in situ conditions from <0.4 for the substrate-nonspecific methods that do not use C tracers (18O, stoichiometric modeling) to >0.6 for the substrate-specific methods that trace glucose use (13C method, calorespirometry, metabolic flux analysis). We explore the different aspects of microbial metabolism that each method captures and how this affects the interpretation of CUE estimates. We recommend that users consider the strengths and weaknesses of each method when choosing the technique that will best address their research needs.

Biochar modulates heavy metal toxicity and improves microbial carbon use efficiency in soil

Soil organic carbon is essential to improve soil fertility and ecosystem functioning. Soil microorganisms contribute significantly to the carbon transformation and immobilisation processes. However, microorganisms are sensitive to environmental stresses such as heavy metals. Applying amendments, such as biochar, to contaminated soils can alleviate the metal toxicity and add carbon inputs. In this study, Cd and Pb spiked soils treated with macadamia nutshell biochar (5% w/w) were monitored during a 49days incubation period. Microbial phospholipid fatty acids (PLFAs) were extracted and analysed as biomarkers in order to identify the microbial community composition. Soil properties, metal bioavailability, microbial respiration, and microbial biomass carbon were measured after the incubation period. Microbial carbon use efficiency (CUE) was calculated from the ratio of carbon incorporated into microbial biomass to the carbon mineralised.Total PLFA concentration decreased to a greater extent in metal contaminated soils than uncontaminated soils. Microbial CUE also decreased due to metal toxicity. However, biochar addition alleviated the metal toxicity, and increased total PLFA concentration. Both microbial respiration and biomass carbon increased due to biochar application, and CUE was significantly (p<0.01) higher in biochar treated soils than untreated soils. Heavy metals reduced the microbial carbon sequestration in contaminated soils by negatively influencing the CUE. The improvement of CUE through biochar addition in the contaminated soils could be attributed to the decrease in metal bioavailability, thereby mitigating the biotoxicity to soil microorganisms.

Stoichiometry of microbial carbon use efficiency in soils

AbstractThe 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. We used this approach to estimate and compare microbial CUE in &gt;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. 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.

Using metabolic tracer techniques to assess the impact of tillage and straw management on microbial carbon use efficiency in soil

Tillage practices and straw management can affect soil microbial activities with consequences for soil organic carbon (C) dynamics. Microorganisms metabolize soil organic C and in doing so gain energy and building blocks for biosynthesis, and release CO2 to the atmosphere. Insight into the response of microbial metabolic processes and C use efficiency (CUE; microbial C produced per substrate C utilized) to management practices may therefore help to predict long term changes in soil C stocks. In this study, we assessed the effects of reduced (RT) and conventional tillage (CT) on the microbial central C metabolic network, using soil samples from a 12-year-old field experiment in an Irish winter wheat cropping system. Straw was removed from half of the RT and CT plots after harvest or incorporated into the soil in the other half, resulting in four treatment combinations. We added 1-13C and 2,3-13C pyruvate and 1-13C and U-13C glucose as metabolic tracer isotopomers to composite soil samples taken at two depths (0–15 cm and 15–30 cm) from each of the treatments and used the rate of position-specific respired 13CO2 to parameterize a metabolic model. Model outcomes were then used to calculate CUE of the microbial community. Whereas the composite samples differed in CUE, the changes were small, with values ranging between 0.757 and 0.783 across treatments and soil depth. Increases in CUE were associated with a reduced tricarboxylic acid cycle and reductive pentose phosphate pathway activity and increased consumption of metabolic intermediates for biosynthesis. Our results suggest that RT and straw incorporation do not substantially affect CUE.