Microbial interactions for nutrient acquisition in soil: Miners, scavengers, and carriers

Abstract

Microbial interactions in soil are hidden, as they occur stealthily in a ‘dark box’. This greatly limits our understanding of microbial functions. Here, soil microorganisms were classified into three broad functional groups, namely miners, scavengers and carriers, to disentangle the intricate microbial labor division and interactions for nutrient acquisition. Miners, such as saprotrophic microorganisms, N2-fixing and phosphate-solubilizing bacteria, and ectomycorrhizal (ECM) fungi, first decompose or mobilize not directly bioavailable organic or inorganic substances through hydrolysis, oxidation and/or mineralization. Scavengers, arbuscular mycorrhizal (AM) fungi as a typical example, explore and efficiently take up nutrients with assistance of host plants, but cannot access nutrients stored in organic matter or minerals. Carriers with filamentous growth such as ECM, AM and saprotrophic fungi transport nutrients and unicellular bacteria to new locations exploiting a large soil volume for nutrients. These three groups build ‘division of labor’ and interaction networks, which reduce the metabolic burden, increase substrate utilization efficiency, and ultimately increase nutrient acquisition in the rhizosphere, detritusphere, and bulk soil. Notably, such grouping of soil microorganisms based on functions is flexible, and a particular microorganism can be versatile. Flexibility in ecological functions and consequence of interactions is necessary to respond to shifting soil nutrient content, organic matter availability, and edaphic conditions. Nevertheless, such broad grouping is conducive to condense functional diversity and allows a better understanding of mutualistic interactions among microbial groups, contributing to hotspot formation and disappearance, nutrient mobilization and delivery to roots. A combination of laboratory studies on pairwise interactions, experiments using synthetic microbial communities with network analysis and imaging techniques is essential to unravel tangled webs of microbial associations. In summary, the interactions among microbial groups classified based on their interconnected ecological processes as miners, scavengers and carriers are important to uncover the true functional roles of microorganisms in terrestrial ecosystems.