How is microbial carbon use efficiency distributed throughout the soil pore network?

Microbial carbon use efficiency (CUE) is a fundamental metric in understanding carbon (C) dynamics in ecosystems, particularly in soils. CUE quantifies the balance between the carbon microorganisms assimilate into their biomass and the carbon they lose as CO₂ through respiration, thus providing insights into the accumulation and loss of soil organic matter (SOM). Despite its importance, traditional measurements of CUE often fail to account for the significant variations in microenvironmental conditions within soils, which are known to strongly influence microbial activity. Soil microbial communities inhabit a complex three-dimensional pore network, where the physical structure of the soil, particularly pore size and connectivity, shapes microhabitats and constrains microbial distribution, resource access, and activity. Aerobic bacteria and fungi dominate larger pores, whereas micropores can host both aerobic and anaerobic microbes. These spatial and functional heterogeneities are further influenced by agricultural practices, such as tillage, which alter pore size distribution and connectivity. We measured CUE across different pore sizes using short incubation times, minimizing the confounding effects of carbon recycling. To overcome the limitations of single-substrate studies and better capture the functional diversity of microbial communities, we employed a mixture of six ¹³C-labeled substrates. We evaluated the effect of different agricultural management systems and pore sizes on respiration and CUE, providing new insights into the interplay between soil physical structure and microbial carbon dynamics.

Our findings indicate that higher respiration rates in larger pores are linked to their lower CUE, driven by the prevalence of fast-growing copiotrophic communities. These microbes rapidly utilize carbon during periods of resource availability but exhibit lower efficiency in carbon use due to the favorable environmental conditions, such as greater aeration and nutrient mobility. In contrast, smaller pores host oligotrophic microbes adapted to resource-limited environments, which maximize carbon recycling and exhibit higher CUE due to constrained nutrient availability and reduced mineralization. We also demonstrate that agricultural practices significantly influence CUE by shaping nutrient dynamics, microbial community composition, and pore connectivity. For instance, grassland systems have favoured microbial communities adapted to stable resource availability and with higher CUE. These findings underscore the importance of tailoring management practices to optimize soil structure, enhance carbon retention, and mitigate greenhouse gas emissions.