Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity

Chemical stabilization of microbial-derived products such as extracellular
enzymes (EE) onto mineral surfaces has gained attention as a possibly
important mechanism leading to the persistence of soil organic carbon
(SOC). While the controls on EE activities and their stabilization in the
surface soil are reasonably well-understood, how these activities change
with soil depth and possibly diverge from those at the soil surface due to
distinct physical, chemical, and biotic conditions remains unclear. We
assessed EE activity to a depth of 1 m (10 cm increments) in 19 soil
profiles across the Critical Zone Observatory Network, which represents a
wide range of climates, soil orders, and vegetation types. For all EEs,
activities per mass soil correlated positively with microbial biomass (MB)
and SOC, all of which decreased logarithmically with depth (p <
0.05). Across all sites, over half of the potential soil EE activities per
mass soil consistently occurred below 20 cm for all measured EEs.
Activities per unit MB or SOC were substantially higher at depth (soils
below 20 cm accounted for 80% of whole-profile EE activity), suggesting an
accumulation of stabilized (i.e., mineral sorbed) EEs in subsoil horizons.
The pronounced enzyme stabilization in subsurface horizons was
corroborated by mixed-effects models that showed a significant, positive
relationship between clay concentration and MB-normalized EE activities in
the subsoil. Furthermore, the negative relationships between soil C, N,
and P and C-, N-, and P-acquiring EEs found in the surface soil decoupled
at 20 cm, which could have also been caused by EE stabilization. This
finding suggests that EEs may not reflect soil nutrient availabilities at
depth. Taken together, our results suggest that deeper soil horizons hold
a significant reservoir of EEs, and that the controls of subsoil EEs
differ from their surface soil counterparts.