Transcription of macromolecular N degrading genes provides a window into organic nitrogen decomposition in soil

Abstract Background Nitrogen (N) is commonly limiting in soil in part because most N is present in macromolecular organic compounds and not directly available to plants. Using extracellular enzymes, the soil microbial community present near roots (rhizosphere) is largely responsible for transforming organic substrates, which yields nitrogen in forms that are plant-available. Microbial genetic potential (genes) and the cycling of inorganic nitrogen pools have been extensively documented and widely explored in rhizospere soil. But there is scarce information on microbial gene expression for macromolecular nitrogen decomposition and how it relates in space and time to life stages of plant roots. Here we use a suite of time-resolved metatranscriptomes from rhizosphere and bulk soil to follow bacterial and fungal extracellular protease and chitinase expression during rhizosphere aging. We also explore the effect of adding plant root litter as a distinct source of macromolecular carbon and nitrogen. Results Expression of extracellular proteases in rhizosphere soil increased with plant growth in the absence of litter, whereas chitinase (chit1) was highly upregulated in the detritusphere. Structural groups of proteases were dominated by serineproteases, despite the higher abundance of metalloproteases previously observed in soil and aquatic systems. Extracellular proteases of Betaprotebacteria were more highly expressed in the rhizosphere, whereas those of Deltaroteobacteria and Fungi responded strongly to the presence of litter. We identified distinct functional guilds of taxa specializing in decomposition of proteins in the rhizosphere, detritusphere and in the vicinity of aging roots. We also identify a sub-guild that appears to specialize in protein decomposition in the presence of growing roots as well as litter that increases its activity in aging rhizosphere soil, which may be particularly N limited. Taxonomic membership of these guilds partially overlapped with functional guilds identified by carbon decomposing enzymes, making up multifunctional guilds. Conclusions We found organic N decomposers have distinct spatiotemporal preferences that are selected during plant growth. Rhizosphere microbes which could potentially benefit plants by degrading macromolecular nitrogen were not comparatively active in bulk soil, even in the presence of root litter, implying that they are enhanced near plant roots and less competitive in bulk soils.