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Soils store more carbon than other terrestrial ecosystems1,2. How soil organic carbon (SOC) forms and persists remains uncertain1,3, which makes it challenging to understand how it will respond to climatic change3,4. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss5-7. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways4,6,8-11, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes12,13. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved7,14,15. 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.

Quantifying the impact of drought on microbial processes and its consequences for soil carbon cycling is hindered by the lack of underlying mechanistic understanding. Therefore, there is a need to scale up the physiological response to changing water status from individual soil microbes to collective communities across different ecosystems. Here we propose the use of a framework that incorporates trait-based ecology to link drought-impacted microbial processes to rates of soil carbon decomposition and stabilisation. We briefly synthesise existing knowledge on the effects of drought on microbial physiology at the individual to community scale, before integrating this understanding within a framework incorporating life-history strategy, ecological strategy and biochemistry. This framework highlights a dynamic allocation to high yield (Y), resource acquisition (A) and stress tolerance (S) pathways as environmental conditions change. Y-A-S strategies represent sets of traits that tend to correlate due to physiological or evolutionary trade-offs. This framework enables assessment of microbial processes along two key environmental gradients of water and resource availability, both of which are constrained by drought. The variable chemistry of biomass and necromass produced under different physiological strategies in response to drying–rewetting impacts organic matter decomposition and stabilisation in soils, and should also be considered when quantifying soil carbon balance. We highlight that diversion of resources away from microbial growth can alter soil organic matter chemistry and its persistence depending on the kind of microbial compounds produced. To advance such a framework, we highlight avenues of research that would enable the further identification and quantification of traits linked to Y-A-S strategies and the physiological outcomes at the community level under drought and rewetting, and conclude by hypothesising how ecosystem-level changes might feedback on to the soil carbon cycle. A scalable understanding of microbial drought-response mechanisms affecting soil carbon cycling will transform the way microbial physiology is represented in ecosystem studies. Read the free Plain Language Summary for this article on the Journal blog.

Microbial physiology may be critical for projecting future changes in soil carbon. Still, predicting the ecosystem implications of microbial processes remains a challenge. We argue that this challenge can be met by identifying microbial life history strategies based on their phenotypic characteristics, or traits, and representing these strategies in models simulating different environmental conditions. By adapting several theories from macroecology, we define microbial high yield (Y), resource acquisition (A), and stress tolerance (S) strategies. Using multi-omics and carbon stable isotope probing tools, we empirically validated our Y-A-S framework by studying variations in community traits along gradients of resource availability and abiotic conditions arising from anthropogenic change. Across a Britain-wide land use intensity gradient, we used isotope tracing and metaproteomics to show that microbial resource acquisition and stress tolerance traits trade off with growth yield measured as carbon use efficiency. Reduced community growth yield with intensification was linked to decreased microbial biomass and increased biomass-specific respiration which subsequently translated into lower organic carbon storage in such soil systems. We concluded that less-intensive management practices have more potential for carbon storage through increased microbial growth yield by greater channelling of substrates into biomass synthesis. In Californian grass and shrub ecosystems, we used metatranscriptomics and metabolomics to infer traits of in situ microbial communities on plant leaf litter in response to long-term drought. This experimental set-up provided gradients of resource availability and water stress. We observed that drought causes greater microbial allocation to stress tolerance. The most discernable physiological adaptations to drought in litter communities were production or uptake of compatible solutes like trehalose and ectoine as well as inorganic ions to maintain cellular osmotic balance. Grass communities also increased expression of genes for synthesis of capsular and extracellular polymeric substances possibly as a mechanism to retain water. These results showed a clear functional response to drought in grass litter communities with greater allocation to survival relative to growth that reduced decomposition under drought. In contrast, communities on chemically complex shrub litter had smaller differences in gene expression and metabolite profiles in response to drought, suggesting that the drought stress response is constrained by litter chemistry which also reduces decomposition rates. Overall, our findings suggest trade-offs between drought stress tolerance, resource acquisition and growth yield in communities across different ecosystems. These empirical studies demonstrate how trade-offs in key microbial traits can have consequences on soil carbon decomposition and storage. We recommend the use of our Y-A-S framework in experimental and modelling studies to mechanistically link microbial communities to system-level processes.

Drought represents a significant stress to microorganisms and is known to reduce microbial activity and organic matter decomposition in Mediterranean ecosystems. However, we lack a detailed understanding of the drought stress response of microbial decomposers. Here we present metatranscriptomic and metabolomic data on the physiological response of in situ microbial communities on plant litter to long-term drought in Californian grass and shrub ecosystems. We hypothesised that drought causes greater microbial allocation to stress tolerance relative to growth pathways. In grass litter, communities from the decade-long ambient and reduced precipitation treatments had distinct taxonomic and functional profiles. The most discernable physiological signatures of drought were production or uptake of compatible solutes to maintain cellular osmotic balance, and synthesis of capsular and extracellular polymeric substances as a mechanism to retain water. The results show a clear functional response to drought in grass litter communities with greater allocation to survival relative to growth that could affect decomposition under drought. In contrast, communities on chemically more diverse and complex shrub litter had smaller physiological differences in response to long-term drought but higher investment in resource acquisition traits across precipitation treatments, suggesting that the functional response to drought is constrained by substrate quality. Our findings suggest, for the first time in a field setting, a trade off between microbial drought stress tolerance, resource acquisition and growth traits in plant litter microbial communities.

Microbial physiology may be critical for projecting future changes in soil carbon. Still, predicting the ecosystem implications of microbial processes remains a challenge. We argue that this challenge can be met by identifying microbial life history strategies based on their phenotypic characteristics, or traits, and representing these strategies in models simulating different environmental conditions. By adapting several theories from macroecology, we define microbial high yield (Y), resource acquisition (A), and stress tolerance (S) strategies. Using multi-omics and carbon stable isotope probing tools, we empirically validated our Y-A-S framework by studying variations in community traits along gradients of resource availability and abiotic conditions arising from anthropogenic change. Across a Britain-wide land use intensity gradient, we used isotope tracing and metaproteomics to show that microbial resource acquisition and stress tolerance traits trade off with growth yield measured as carbon use efficiency. Reduced community growth yield with intensification was linked to decreased microbial biomass and increased biomass-specific respiration which subsequently translated into lower organic carbon storage in such soil systems. We concluded that less-intensive management practices have more potential for carbon storage through increased microbial growth yield by greater channelling of substrates into biomass synthesis. In Californian grass and shrub ecosystems, we used metatranscriptomics and metabolomics to infer traits of in situ microbial communities on plant leaf litter in response to long-term drought. This experimental set-up provided gradients of resource availability and water stress. We observed that drought causes greater microbial allocation to stress tolerance. The most discernable physiological adaptations to drought in litter communities were production or uptake of compatible solutes like trehalose and ectoine as well as inorganic ions to maintain cellular osmotic balance. Grass communities also increased expression of genes for synthesis of capsular and extracellular polymeric substances possibly as a mechanism to retain water. These results showed a clear functional response to drought in grass litter communities with greater allocation to survival relative to growth that reduced decomposition under drought. In contrast, communities on chemically complex shrub litter had smaller differences in gene expression and metabolite profiles in response to drought, suggesting that the drought stress response is constrained by litter chemistry which also reduces decomposition rates. Overall, our findings suggest trade-offs between drought stress tolerance, resource acquisition and growth yield in communities across different ecosystems. These empirical studies demonstrate how trade-offs in key microbial traits can have consequences on soil carbon decomposition and storage. We recommend the use of our Y-A-S framework in experimental and modelling studies to mechanistically link microbial communities to system-level processes.

Resource acquisition and growth yield are fundamental microbial traits that affect biogeochemical processes and have consequences for ecosystem functioning. However, there is a lack of empirical observations linking these traits. Using a landscape-scale survey of temperate near-neutral pH soils, we show tradeoffs in key community-level parameters linked to these traits. Increased investment into extracellular enzymes estimated using specific potential enzyme activity was associated with reduced growth yield obtained using carbon use efficiency measures from stable isotope tracing. Reduction in growth yield was linked more to carbon than nitrogen acquisition highlighting smaller stoichiometric than energetic constraints on community metabolism in examined soils.