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Abstract Delineation of microbial habitats within the soil matrix and characterization of their environments and metabolic processes are crucial to understand soil functioning, yet their experimental identification remains persistently limited. We combined single- and triple-energy X-ray computed microtomography with pore specific allocation of¹³C labeled glucose and subsequent stable isotope probing to demonstrate how long-term disparities in vegetation history modify spatial distribution patterns of soil pore and particulate organic matter drivers of microbial habitats, and to probe bacterial communities populating such habitats. Here we show striking differences between large (30-150 µm Ø) and small (4-10 µm Ø) soil pores in (i) microbial diversity, composition, and life-strategies, (ii) responses to added substrate, (iii) metabolic pathways, and (iv) the processing and fate of labile C. We propose a microbial habitat classification concept based on biogeochemical mechanisms and localization of soil processes and also suggests interventions to mitigate the environmental consequences of agricultural management. 

Summary Plant roots are the main supplier of carbon (C) to the soil, the largest terrestrial C reservoir. Soil pore structure drives root growth, yet how it affects belowground C inputs remains a critical knowledge gap. By combining X‐ray computed tomography with 14 C plant labelling, we identified root–soil contact as a previously unrecognised influence on belowground plant C allocations and on the fate of plant‐derived C in the soil. Greater contact with the surrounding soil, when the growing root encounters a pore structure dominated by small (< 40 μm Ø) pores, results in strong rhizodeposition but in areas of high microbial activity. The root system of Rudbeckia hirta revealed high plasticity and thus maintained high root–soil contact. This led to greater C inputs across a wide range of soil pore structures. The root–soil contact Panicum virgatum , a promising bioenergy feedstock crop, was sensitive to the encountered structure. Pore structure built by a polyculture, for example, restored prairie, can be particularly effective in promoting lateral root growth and thus root–soil contact and associated C benefits. The findings suggest that the interaction of pore structure with roots is an important, previously unrecognised, stimulus of soil C gains. 

Abstract Delineation of microbial habitats within the soil matrix and characterization of their environments are crucial to understand soil functioning and carbon (C) cycling. Yet, experimental identification of microbial communities populating specific micro-habitats and assessments of their biochemical properties have been persistently limited. Here we demonstrate how long-term disparities in vegetation history modify spatial distribution patterns and properties of soil pores and particulate organic matter (POM), and show striking differences in bacterial communities populating pores of contrasting sizes in soils from three vegetation systems on the same soil type: an intensive corn (Zea mays L.) rotation, monoculture switchgrass (Panicum virgatum L.), and restored North American prairie. We combined single- and triple-energy X-ray computed microtomography (µCT) with pore specific allocation of 13 C labeled glucose and subsequent stable isotope probing (¹³C-DNA/RNA-SIP) to show that large (30-150 µm Ø) and small (4-10 µm Ø) soil pores differed in (i) microbial diversity, composition, and life-strategies, (ii) responses to added substrate, (iii) metabolic pathways, and (iv) the processing and fate of labile C. Results demonstrate that soil pores created by different plant communities differ in ways that strongly influence microbial composition and activity, and thus impact ecosystem processes such as decomposition, nitrogen processing, and carbon sequestration. A proposed classification scheme may improve biogeochemical models of soil processes and as well suggest interventions to mitigate the environmental consequences of agricultural management.