Deep tree roots maintain biogeochemical environments distinct from persistently root-free soils. soil metagenome

Deep roots pump reduced C deep into Earth’s critical zone. Via their growth and this pumping action, they promote biogeochemical environments conducive to soil development by generating acid-forming CO2 and organic acids, and by fostering activities of soil microbes that also produce CO2 and organic acids. Anthropogenic disturbance can transform deeply rooted, terrestrial ecosystems into more shallowly-rooted annual row crop systems, some of which are re-transformed into regenerating ecosystems after relaxation of the disturbance regime. Leveraging replicated plots across the Calhoun Critical Zone Observatory landscape and deep (to 5 m) soil sampling strategies, we tested the hypothesis that the loss of deep roots associated with disturbance of relatively old-growth ecosystems and prevention of deep root establishment for centuries alters root- and microbially-mediated biogeochemical pools and fluxes, even well below the zone of maximum root density. We also hypothesize that any land use effects on these and associated parameters will be evident even after decades of forest regeneration. Root abundance, quantified to ~2 m depth, declined with depth in all plots and was greater in old-growth and ~60 y old regenerating pine forests than in agricultural plots at most depths; between ~30-45 and ~70-80 cm depth, old-growth forest root abundances were statistically greater than in regenerating pine forests. Modeled parameter estimates of root depth distribution functions suggest that root declines with depth were least severe in old-growth forest plots. In spite of these differences in rooting habit across land use histories, soil organic C (SOC) concentrations did not differ across land use. Extractable OC (EOC) also did not vary with land use, though old-growth forest soils exhibited 8.8 and 12.5 times the [EOC] of regenerating forest soils and agricultural soils at 4 to 5 m depth. The proportion of SOC comprised of EOC (EOC/SOC) exhibited a significant interaction effect of landuse and depth interval driven by higher EOC/SOC in old-growth forests (20.0±2.6%) compared to regenerating forests (2.1±1.1) and agricultural soils (1.9±0.9%) at the deepest depth interval. That this effect was observed far deeper than where root abundances exhibited significant differences between forest types hints that deep roots in old-growth, hardwood forests allocate more resources to root exudates than deep roots in regenerating pine forests. At soil depths greater than 20 cm, we observed a significantly greater slope of the relationship between root abundance and [EOC] in old-growth relative to regenerating forests. SOC and EOC 13C revealed the ability of regenerating forests to pump sufficient C belowground to mask any past planting of C4, 13C-enriched crops, but no differences between old-growth and regenerating forests. In contrast, 13C of respired CO2 during ex situ, aerobic incubations indicate that soil microbial communities are sensitive signalers of the origins of organic C substrates even when 13C of those substrates does not appear to differ across forest ages: microbes in regenerating forest soils mineralized SOC with more of a C4 signature than in old-growth forest soils. Soil microbial communities in all plots declined in -diversity with depth; microbial community composition varied with land use history on microbial community composition even at 4-5 m depths, with greater abundances of root-associated bacterial taxa in old-growth systems than in regenerating forests or agricultural soils. Combined, these data suggest that widespread, repeated disturbance regimes that induce deep root mortality can impart top-down, biotic signals deep within Earth’s critical zone, some of which remain evident after even ~60 y of forest regeneration.