Soil pores created by diverse plant communities drive microbial community composition and processes with ecosystem consequences

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.