Abstract
Plant roots are major transmitters of atmospheric carbon into soil. The rhizosphere, the soil volume around living roots influenced by root activities, represents hotspots for organic carbon inputs, microbial activity, and carbon turnover. Rhizosphere processes remain poorly understood and the observation of key mechanisms for carbon transfer and protection in intact rhizosphere microenvironments are challenging. We deciphered the fate of photosynthesis-derived organic carbon (OC) in intact wheat rhizosphere, combining stable isotope labeling at field scale with high-resolution 3D-imaging. We used nano-scale secondary ion mass spectrometry and focus ion beam-scanning electron microscopy to generate insights into rhizosphere processes at nanometer scale. In immature wheat roots, the carbon circulated through the apoplastic pathway, via cell walls, from the stele to the cortex. The carbon was transferred to substantial microbial communuties, mainly represented by bacteria surrounding peripheral root cells. Iron oxides formed bridges between roots and bigger mineral particles, such as quartz, and surrounded bacteria in microaggregates close to the root surface. Some microaggregates were also intimately associated with the fungal hyphae surface. Based on these results, we propose a conceptual model depicting the fate of carbon at biogeochemical interfaces in the rhizosphere, at the forefront of growing roots. We observed complex interplays between vectors (roots, fungi, bacteria), transferring plant-derived OC into root-free soil and stabilizing agents (iron oxides, root and microorganism products), potentially protecting plant-derived OC within microaggregates in the rhizosphere.
Highlights
Soils harbor a huge fraction of the global terrestrial carbon (C) pool
We focused on rhizosphere processes and assumed autotrophic microorganisms to be negligible compared to heterotrophic ones (Kuzyakov and Larionova, 2005)
We were able to detect the round shape of microorganisms with an approximate diameter of 1 μm and high nitrogen content reflected by the 12C14N clearly indicating its microbial origin
Summary
Soils harbor a huge fraction of the global terrestrial carbon (C) pool. While belowground C transfer by plants represents a major pathway of atmospheric C into the soil, soils represent a major source of atmospheric C. Microorganisms inhabiting the rhizosphere represent a major sink for plant-derived C and foster the development of soil microstructures (Liang and Balser, 2011; Kallenbach et al, 2016; Lehmann et al, 2017) These microorganisms include arbuscular mycorrhizal (AM) fungi, soil fungi that form symbiotic associations with the majority of land plants, including wheat (Van der Heijden et al, 1998; Dickie et al, 2013). Rhizosphere processes have a determinant impact on the global soil C pool that is still not fully understood (Schmidt et al, 2011; Pett-Ridge and Firestone, 2017) Enhancing rhizosphere processes, such as C transfer from roots to microorganisms and soil, can increase soil C storage (White et al, 2013; Lange et al, 2015), one of the challenges of the Twenty-firstt century to mitigate climate change (Lal, 2004; Lehmann, 2007)
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