Photosynthate distribution determines spatial patterns in the rhizosphere microbiota of the maize root system

Abstract

Abstract The spatial variation and underlying mechanisms of pattern formation in the rhizosphere microbiome are not well understood. We demonstrate that specific patterns in the distribution of recently fixed carbon within the plant root system influence the spatial organization of the rhizosphere microbiota. Non-invasive analysis of carbon allocation in the maize root system by 11C tracer-based positron emission tomography combined with magnetic resonance imaging reveals high spatial heterogeneity with highest 11C-signal accumulations at root tips and differences between root types. Strong correlations exist between root internal carbon allocation and rhizodeposition as evident from 13CO2 labeling. These patterns are reflected in the bacterial, fungal and protistan community structure in rhizosphere soil with differences depending on root structure and related spatial heterogeneities in carbon allocation. Especially the active consumers of 13C-labeled rhizodeposits are responsive to photosynthate distribution with differences in 13C-labeling according to their spatial localization within the root system. Thus, root photosynthate allocation supports distinct habitats in the plant root system and is a key determinant of microbial food web development, evident from 13C-labeling of diverse bacterial and protistan predators, especially at root bases, resulting in characteristic spatiotemporal patterns in the rhizosphere microbiome.