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

• Published in: Nature communications Vol. 16; no. 1; pp. 7286 - 16
• Main Authors: Schultes, Sina R., Rüger, Lioba, Niedeggen, Daniela, Freudenthal, Jule, Frindte, Katharina, Becker, Maximilian F., Metzner, Ralf, Pflugfelder, Daniel, Chlubek, Antonia, Hinz, Carsten, van Dusschoten, Dagmar, Bauke, Sara L., Bonkowski, Michael, Watt, Michelle, Koller, Robert, Knief, Claudia
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 07.08.2025; Nature Publishing Group; Nature Portfolio
• Subjects: 45/71; 45/77; 631/158/855; 631/326/2565/2134; 631/449/1736; 704/47/4113; Bacteria - classification; Bacteria - genetics; Bacteria - metabolism; Carbon; Carbon - metabolism; Carbon 13; Carbon Isotopes - metabolism; Community structure; Corn; Food chains; Food webs; Fungi - metabolism; Heterogeneity; Humanities and Social Sciences; Isotopic tracers; Labeling; Localization; Magnetic resonance imaging; Microbiomes; Microbiota; Microbiota - physiology; Microorganisms; multidisciplinary; Pattern formation; Phenotyping; Photosynthesis - physiology; Plant roots; Plant Roots - metabolism; Plant Roots - microbiology; Positron emission; Positron emission tomography; Predators; Rhizosphere; Rhizosphere microorganisms; Roots; Science; Science (multidisciplinary); Soil - chemistry; Soil Microbiology; Spatial discrimination; Spatial heterogeneity; Spatial variations; Zea mays - metabolism; Zea mays - microbiology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-025-62550-y

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 11 C tracer-based positron emission tomography combined with magnetic resonance imaging reveals high spatial heterogeneity with highest 11 C-signal accumulations at root tips and differences between root types. Strong correlations exist between root internal carbon allocation and rhizodeposition as evident from 13 CO 2 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 13 C-labeled rhizodeposits are responsive to photosynthate distribution with differences in 13 C-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 13 C-labeling of diverse bacterial and protistan predators, especially at root bases, resulting in characteristic spatiotemporal patterns in the rhizosphere microbiome. The combination of isotopic tracers with root phenotyping reveals specific patterns in photosynthate allocation. These patterns are reflected in rhizodeposition and result in spatially distinct microbiomes within the plant root system.