Spatio-temporal feedbacks between soil legacies and the rhizosphere microbiome of maize

The rhizosphere is the narrow layer of soil around roots, where root respiration and rhizodeposits continually restructure the physicochemical conditions, fuelling microbial growth. Bottom-up carbon release operates alongside top-down trophic consumers across interlinked feedback loops: mucilage at growing tips and exudates along older zones trigger bacterial and fungal proliferation, and, subsequently, protist grazers restructure the emerging assemblage. Senescing roots leave behind biological and structural legacies, microbial propagules and empty root channels (biopores), that influence root architecture and rhizosphere microbiomes of subsequent plants. These dual legacies may accelerate beneficial interactions but may also favour host-specific pathogens under continuous monoculture. This thesis first quantified how maize carbon release structures the rhizosphere. Respiration-kinetics assays showed that microbial growth is initiated at 60 % of microbial-biomass carbon for simple sugars but requires 250–630 % for complex rhizodeposits, indicating substrate-specific activation thresholds that confine activity to the immediate root zone. PET-MRI, combined with DNA-SIP, traced photo-synthesised carbon into bacterial, fungal, and protistan communities, revealing discrete hotspots that select for specific sub-communities. A five-year field chronosequence monitored protist succession across two soil textures (sand and loam), while complementary column experiments used the pre-conditioned monoculture field soil to observe a full growth–decay–regrowth cycle, testing how biopore recycling and legacy inocula jointly influence rhizosphere microbial community assembly. Field data demonstrated that continuous maize steadily enriched potentially pathogenic oomycete species as well as heterotrophic Cercozoa, confirming that soil legacy drives microbial succession. Loam promoted an enhanced soil legacy effect by facilitating compositional shifts in protist communities. By contrast, sand exhibited more stochastic and drought-sensitive behaviour. Column imaging revealed that 10 % of biopores were reused by new roots. During regrowth, these recycled biomes shifted from decomposer communities back towards rhizosphere communities, though they hosted microbiomes with elevated beta dispersion. Overall, the results showed that the location of microbial niches is determined by the availability of carbon, while inherited inocula and pore architecture influence the assembly of communities, which is further defined by exudate patterns. The interaction between these factors creates spatiotemporal feedback loops that can maintain the resilience of the maize rhizosphere microbiome or cause it to become vulnerable under continuous monoculture.

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Published
2026-07-25
Primary Topic
Plant-Microbe Interactions and Immunity
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article

Spatio-temporal feedbacks between soil legacies and the rhizosphere microbiome of maize

Daniela Niedeggen
Plant-Microbe Interactions and Immunity
article

Spatio-temporal feedbacks between soil legacies and the rhizosphere microbiome of maize

Daniela Niedeggen
article en

Abstract

The rhizosphere is the narrow layer of soil around roots, where root respiration and rhizodeposits continually restructure the physicochemical conditions, fuelling microbial growth. Bottom-up carbon release operates alongside top-down trophic consumers across interlinked feedback loops: mucilage at growing tips and exudates along older zones trigger bacterial and fungal proliferation, and, subsequently, protist grazers restructure the emerging assemblage. Senescing roots leave behind biological and structural legacies, microbial propagules and empty root channels (biopores), that influence root architecture and rhizosphere microbiomes of subsequent plants. These dual legacies may accelerate beneficial interactions but may also favour host-specific pathogens under continuous monoculture. This thesis first quantified how maize carbon release structures the rhizosphere. Respiration-kinetics assays showed that microbial growth is initiated at 60 % of microbial-biomass carbon for simple sugars but requires 250–630 % for complex rhizodeposits, indicating substrate-specific activation thresholds that confine activity to the immediate root zone. PET-MRI, combined with DNA-SIP, traced photo-synthesised carbon into bacterial, fungal, and protistan communities, revealing discrete hotspots that select for specific sub-communities. A five-year field chronosequence monitored protist succession across two soil textures (sand and loam), while complementary column experiments used the pre-conditioned monoculture field soil to observe a full growth–decay–regrowth cycle, testing how biopore recycling and legacy inocula jointly influence rhizosphere microbial community assembly. Field data demonstrated that continuous maize steadily enriched potentially pathogenic oomycete species as well as heterotrophic Cercozoa, confirming that soil legacy drives microbial succession. Loam promoted an enhanced soil legacy effect by facilitating compositional shifts in protist communities. By contrast, sand exhibited more stochastic and drought-sensitive behaviour. Column imaging revealed that 10 % of biopores were reused by new roots. During regrowth, these recycled biomes shifted from decomposer communities back towards rhizosphere communities, though they hosted microbiomes with elevated beta dispersion. Overall, the results showed that the location of microbial niches is determined by the availability of carbon, while inherited inocula and pore architecture influence the assembly of communities, which is further defined by exudate patterns. The interaction between these factors creates spatiotemporal feedback loops that can maintain the resilience of the maize rhizosphere microbiome or cause it to become vulnerable under continuous monoculture.

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Plant-Microbe Interactions and Immunity
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