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Soils store more carbon than other terrestrial ecosystems 1,2 . How soil organic carbon (SOC) forms and persists remains uncertain 1,3 , which makes it challenging to understand how it will respond to climatic change 3,4 . It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss 5-7 . Although microorganisms affect the accumulation and loss of soil organic matter through many pathways 4,6,8-11 , microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes 12,13 . Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved 7,14,15 . 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., (© 2023. The Author(s).)

Soil microorganisms act as gatekeepers for soil-atmosphere carbon exchange by balancing the accumulation and release of soil organic matter. However, poor understanding of the mechanisms responsible hinders the development of effective land management strategies to enhance soil carbon storage. Here we empirically test the link between microbial ecophysiological traits and topsoil carbon content across geographically distributed soils and land use contrasts. We discovered distinct pH controls on microbial mechanisms of carbon accumulation. Land use intensification in low-pH soils that increased the pH above a threshold (~6.2) leads to carbon loss through increased decomposition, following alleviation of acid retardation of microbial growth. However, loss of carbon with intensification in near-neutral pH soils was linked to decreased microbial biomass and reduced growth efficiency that was, in turn, related to trade-offs with stress alleviation and resource acquisition. Thus, less-intensive management practices in near-neutral pH soils have more potential for carbon storage through increased microbial growth efficiency, whereas in acidic soils, microbial growth is a bigger constraint on decomposition rates.

Environmental factors relating to soil pH are important regulators of bacterial taxonomic biodiversity, yet it remains unclear if such drivers affect community functional potential. To address this, we applied whole-genome metagenomics to eight geographically distributed soils at opposing ends of a landscape soil pH gradient (where "low-pH" is ~pH 4.3 and "high-pH" is ~pH 8.3) and evaluated functional differences with respect to functionally annotated genes. First, differences in taxonomic and functional diversity between the two pH categories were assessed with respect to alpha diversity (mean sample richness) and gamma diversity (total richness pooled for each pH category). Low-pH soils, also exhibiting higher organic matter and moisture, consistently had lower taxonomic alpha and gamma diversity, but this was not apparent in assessments of functional alpha and gamma diversity. However, coherent changes in the relative abundances of annotated genes between low- and high-pH soils were identified; with strong multivariate clustering of samples according to pH independent of geography. Assessment of indicator genes revealed that the acidic organic-rich soils possessed a greater abundance of cation efflux pumps, C and N direct fixation systems, and fermentation pathways, indicating adaptations to both acidity and anaerobiosis. Conversely, high-pH soils possessed more direct transporter-mediated mechanisms for organic C and N substrate acquisition. These findings highlight the distinctive physiological adaptations required for bacteria to survive in soils of various nutrient availability and edaphic conditions and more generally indicate that bacterial functional versatility with respect to functional gene annotations may not be constrained by taxonomy. IMPORTANCE Over a set of soil samples spanning Britain, the widely reported reductions in bacterial taxonomic richness at low pH were found not to be accompanied by significant reductions in the richness of functional genes. However, consistent changes in the abundance of related functional genes were observed, characteristic of differential ecological and nutrient acquisition strategies between high-pH mineral soils and low-pH organic anaerobic soils. Our assessment at opposing ends of a soil gradient encapsulates the limits of functional diversity in temperate climates and identifies key pathways that may serve as indicators for soil element cycling and C storage processes in other soil systems. To this end, we make available a data set identifying functional indicators of the different soils; as well as raw sequences, which given the geographic scale of our sampling should be of value in future studies assessing novel genetic diversity of a wide range of soil functional attributes., (Copyright © 2017 Malik et al.)

Plant diversity strongly influences ecosystem functions and services, such as soil carbon storage. However, the mechanisms underlying the positive plant diversity effects on soil carbon storage are poorly understood. We explored this relationship using long-term data from a grassland biodiversity experiment (The Jena Experiment) and radiocarbon ((14)C) modelling. Here we show that higher plant diversity increases rhizosphere carbon inputs into the microbial community resulting in both increased microbial activity and carbon storage. Increases in soil carbon were related to the enhanced accumulation of recently fixed carbon in high-diversity plots, while plant diversity had less pronounced effects on the decomposition rate of existing carbon. The present study shows that elevated carbon storage at high plant diversity is a direct function of the soil microbial community, indicating that the increase in carbon storage is mainly limited by the integration of new carbon into soil and less by the decomposition of existing soil carbon.

Soil dissolved organic carbon (DOC) sources and its seasonal dynamics are poorly known. We aimed to determine the contribution of plant and soil organic matter (SOM) to size classes of DOC in a field experiment with C3 to C4 vegetation change on two soil types through different seasons. Stable isotope ratios of DOC size classes were measured using size exclusion chromatography (SEC) coupled online to liquid chromatography-isotope ratio mass spectrometry (LC-IRMS). SEC resolved DOC into three size classes: very high molecular weight/vHMW (> 10 kDa), high molecular weight/HMW (0.4-10 kDa), and low molecular weight/LMW (< 0.4 kDa). HMW DOC was most abundant in all seasons, soil types, and depths. In contrast, vHMW DOC was only seen postsnowmelt in upper 20 cm and was mainly (87 ± 9%) plant-derived. Through all seasons, HMW and LMW DOC had less than 30% recent plant contribution. Similar size range and source of DOC size classes and soil chloroform fumigation extracts suggest microbial origin of DOC. Thus, microbial SOM recycling is an important process in DOC production. We suggest that DOC molecules get partitioned manifold between soil solution and the mineral matrix (chromatography), thereby getting constantly decomposed, altered, or produced anew by soil microorganisms (reactive transport)., (© 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.)

Aims: We investigated the role of plants and their plant-derived carbon in shaping the microbial community that decomposes substrates and traced the return of nutrients from decomposition back to plant shoots in order to understand the importance of plants for ecosystem element cycling. Methods: We performed a greenhouse experiment having plant communities with and without arbuscular mycorrhizal fungi (AMF) and ingrowth cores that held different 15N labeled substrates. We determined the microbial community structure using molecular sequencing and the net assimilation of plant carbon into soil microorganisms using a 13CO2 pulse and 13C measurements of microbial biomarkers. We determined the return of nitrogen back to the shoots using the 15N signal, which was provided from the decomposition of the substrate added to the ingrowth cores. Results: We observed that the microbial community composition in the ingrowth cores and their net 13C assimilation depended on the presence of AMF and the added substrate. Both plant communities had similar 15N uptake into their shoots, but the net N uptake cost was significantly lower in presence of AMF. In the presence of AMF also lower net N uptake cost was observed for the decomposition of plant-derived and microorganism-derived substrates compared to inorganic nitrogen suggesting that AMF actively controls the decomposer comunity and their carbon demand. Conclusion: Our results identify for the first time a functional overlap of soil microorganisms as identical substrate is decomposed by different microorganisms suggesting functional redundancy of microbial communities. In consequence a better understanding of ecosystem element cycling can only be achieved when the whole plant-microorganism-organic matter-soil continuum is investigated. [ABSTRACT FROM AUTHOR]

Soil carbon cycling and ecosystem functioning can strongly depend on how microbial communities regulate their metabolism and adapt to changing environmental conditions to improve their fitness. Investing in extracellular enzymes is an important strategy for the acquisition of resources, but the principle behind the trade-offs between enzyme production and growth is not entirely clear. Here we show that the enzyme production rate per unit biomass may be regulated in order to maximize the biomass specific growth rate. Based on this optimality hypothesis, we derive mathematical expressions for the biomass specific enzyme production rate and the microbial carbon use efficiency, and verify them with experimental observations. As a result of this analysis, we also find that the optimal enzyme production rate decays hyperbolically with the soil organic carbon content. We then show that integrating the optimal extracellular enzyme production into soil microbial carbon models may change considerably soil carbon projections under global warming, underscoring the need to improve parameterization of microbial processes. [ABSTRACT FROM AUTHOR]

It is well established that soil microorganisms play an important role in respiration of newly fixed plant carbon. Recent results show that they also contribute significantly to soil organic matter (SOM) formation. We hypothesized that different molecular size classes of compounds in soil microbial biomass (SMB) have variable turnover time and in consequence influence SOM formation differentially. Here we used natural differences in carbon stable isotope signatures (δ13C values) after C3–C4 vegetation change to track newly fixed C4 plant carbon into SMB molecular size classes. SMB was obtained by chloroform fumigation extraction (SFE) and δ13C values of its size classes were measured using size exclusion chromatography coupled online to liquid chromatography‒isotope ratio mass spectrometry (SEC–LC–IRMS). Resolved SMB was assigned to 5 size classes of 1800–9800, 800–1800, 380–800, 180–380 and 50–180 Da respectively. The contribution of recent C4 plant carbon to size classes of SMB decreased with increasing molecular weight (MW). It ranged from 77 ± 19% in the lowest MW size class size class to 41 ± 14% in the highest MW size class in a sandy soil and from 59 ± 18% in the lowest MW size class to 8 ± 15% in the highest MW size class in a clayey soil. A decreasing carbon turnover of compounds in SMB extracts along a continuum of molecular size from small to large implies that low molecular weight microbial compounds are rapidly metabolized products that link to fast respiratory carbon fluxes, whereas high molecular weight ones could be products of microbial synthesis like structural compounds that have slower turnover rates and link to slower SOM formation. Our methods help avoid contamination of CFE extracts and the results help explain why SMB turnover is faster in CFE extracts when compared to calculations using membrane lipids (e.g. PLFA-based). [ABSTRACT FROM AUTHOR]