Synergy of saprotrophs with mycorrhiza for litter decomposition and hotspot formation depends on nutrient availability in the rhizosphere

Plants acquire and recycle nutrients from soil organic matter, and these dynamics depend on a highly diverse array of microorganisms in the rhizosphere. Although functions of many microbial groups have been identified, how different groups interact to affect biogeochemical processes is still poorly understood. We investigated the interactive effects of saprotrophs and arbuscular mycorrhizal fungi (AMF) on Medicago sativa litter decomposition and spatial distribution of enzyme activity in the rhizosphere in nutrient poor and rich soils, using compartmented microcosms designed for zymography. In nutrient poor soils, co-inoculation of saprotrophic bacteria (Alcaligenes faecalis) or fungi (Phanerochaete chrysosporium) with AMF (Rhizophagus irregularis) resulted in faster litter decomposition and greater hotspot areas of enzymes in the rhizosphere compared to mono-inoculations. These positive effects were stronger in the interaction of AMF with saprotrophic bacteria than that with saprotrophic fungi. The synergy of saprotrophic bacteria with AMF for litter decomposition and enzymatic hotspot formation was weaker in nutrient rich soils than that in nutrient poor soils. In contrast, in nutrient rich soils, co-inoculation of saprotrophic fungi with AMF reduced litter decomposition. A partial least squares path modeling (PLS-PM) analysis indicated that faster litter decomposition and larger enzymatic hotspots increased overall plant growth. These findings suggest the existence of important synergistic relationships between these two microbial guilds for plant growth in nutrient poor soils. Specifically, AMF accelerated litter mineralization by increasing saprotrophic biomass and enzyme activities (i.e., nitrate reductase, urease and cellulase). At the same time, saprotrophs increased AMF colonization rate, which increased the hotspot areas of enzyme activities. These hotspots, in turn, broadened the nutrient mobilization zone around the roots - in the rhizosphere. Consequently, the synergistic interactions between saprotrophs and AMF for litter decomposition and the formation of enzymatic hotspots may be an important mechanism for promoting plant fitness under low soil nutrient availability. © 2021 Elsevier B.V.