Productivity-driven decoupling of microbial carbon use efficiency and respiration across global soils

ECOLOGY Productivity-driven decoupling of microbial carbon use efficiency and respiration across global soils

Despite extensive research on soil microbial carbon use efficiency, its linkage to actual soil carbon storage remains ambiguous. A key uncertainty is that use efficiency estimates from short-term labeling incubations assume a linear negative relationship with respiration rates, overlooking nonlinear interactions and long-term microbial acclimation. Here, we use a stoichiometry-based approach to estimate use efficiency, which links soil resource availability to microbial demand and captures microbial adaptability under resource constraints. We synthesized one thousand ninety-four paired observations of use efficiency and heterotrophic respiration rate across natural ecosystems and found a nonlinear relationship between them governed by ecosystem productivity. In low-productivity arid and cold regions, use efficiency declined with increasing respiration, whereas in productive tropical and temperate regions, use efficiency stabilized at a low level (zero point two seven plus or minus zero point one one) as respiration exceeded three hundred forty plus or minus ten point eight grams of carbon per square meter per year. This shift reflects microbial trade-offs between carbon assimilation and stoichiometric homeostasis, revealing a decoupling of microbial growth from respiration that limits the capacity of productive ecosystems to store additional soil carbon.

INTRODUCTION

Soil microbial carbon assimilation and heterotrophic respiration are two basic microbial metabolic processes that collectively control organic carbon retention in soils. When the total microbial carbon uptake remains constant, higher assimilation for growth combined with lower respiration indicates more efficient biomass production, which enhances soil organic carbon retention. Culture-based studies, from strains to community levels, have shown that microbial growth efficiency is more stable than respiration under changing environmental conditions. Recent global assessments further suggest that warming accelerates respiration but does not have a clear or consistent effect on microbial growth.

These differential responses imply a decoupling between microbial carbon assimilation efficiency, commonly described as microbial carbon use efficiency, and respiration under specific environmental constraints. This decoupling challenges the long-held assumption that

Use efficiency uniformly declines with increasing respiration, even though use efficiency definitions vary among measurement approaches. It may also represent a key source of uncertainty in linking use efficiency to soil carbon storage and dynamics. Under nutrient-limited conditions, particularly low nitrogen and phosphorus availability, microorganisms may sustain growth by investing in energetically expensive enzyme production and efficient nutrient recycling, which increases carbon efflux while maintaining biomass production, thereby decoupling use efficiency from respiration. Nevertheless, this potential decoupling has been neither empirically tested across natural ecosystems nor understood in terms of the potential mechanisms involved.

This knowledge gap is likely attributable to three main reasons. First, most existing studies assume a linear negative relationship between use efficiency and respiration because widely used approaches, such as those based on carbon thirteen/carbon fourteen-labeled substrates and oxygen eighteen-labeled water, calculate use efficiency from pulse respiration and thus inherently generate a negative correlation between the two. However, this approach overlooks mounting evidence for widespread nonlinear relationships in soil carbon cycling across ecosystems. Second, respiration measurements used for estimating use efficiency are generally conducted on disturbed soils under short-term laboratory incubations, which reflect immediate metabolic responses to added substrates, rather than long-term microbial adaptability. Moreover, changes in the availability of one resource (e.g., carbon) can trigger cascading metabolic responses to other resources through priming effects and nutrient mining. These processes could obscure trade-offs between microbial carbon assimilation and the maintenance of stoichiometric homeostasis in natural ecosystems. Third, there is a lack of simultaneous, independent measurements of use efficiency and respiration across a range of natural ecosystems, limiting our ability to assess their relationship across environmental gradients.

To explore the potential decoupling between use efficiency and respiration, we compiled a global dataset of one thousand ninety-four paired, independently derived observations of use efficiency and respiration across natural ecosystems. Specifically, we estimated use efficiency using a culture-independent stoichiometric model, which accounts for microbial enzyme allocation strategies to minimize elemental imbalances between soil resource supply and microbial growth demand. The estimated use efficiency reflects in situ microbial traits, with higher values indicating more efficient carbon utilization relative to nutrient acquisition. To obtain corresponding respiration values, we matched the geographic coordinates (latitude and longitude) of each use efficiency observation with average annual respiration from the latest global Soil Respiration Database, which characterizes long-term patterns of microbial respiration. We hypothesize that use efficiency is negatively correlated with respiration under low carbon availability (e.g., low plant-derived carbon inputs), as organisms encounter a trade-off between carbon assimilation and respiratory loss. However, use efficiency and respiration could decouple under low nutrient conditions because of increased carbon expenditure to acquire and recycle limiting nutrients, particularly nitrogen and phosphorus, to maintain stoichiometric homeostasis. To test this hypothesis, we examined the relationship between use efficiency and respiration across global ecosystems and evaluated the environmental drivers with nine variables representing temperature, water, carbon, and nutrient availability.