Linking 3D Soil Structure and Plant-Microbe-Soil Carbon Transfer in the Rhizosphere

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 (OC) 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 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.

Imaging microstructure of the barley rhizosphere: particle packing and root hair influences

“…Barley exudates initially disperse and then gel soil (Naveed et al, 2017a,b), so the observed extension of the packing effect beyond the initial sieved soil size was likely due to aggregation. Root-and microbially derived mucilage are thought to play an important role in aggregate formation in the rhizosphere (Caravaca et al, 2005;Moreno-Esp ındola et al, 2007;Vidal et al, 2018). The mixed phase was assumed to be unaffected by the roots in the present model because of the limiting imaging resolution.…”

“…Water uptake by roots is recognised as a major driver of crack formation through shrinkage of clay particles (Yoshida & Hallett, 2008). Wetting and drying cycles in the rhizosphere are also an important driver of aggregation and rhizosheath formation (Watt et al, 1994;Albalasmeh & Ghezzehei, 2014), with aggregation further enhanced by binding agents in rhizodeposits or released by microbes (Czarnes et al, 2000;Hallett et al, 2009;Vidal et al, 2018). These root exudates may differ significantly in their chemical composition and physical properties depending on the species and among genotypes of the same species (Mwafulirwa et al, 2016;Naveed et al, 2017a,b).…”

“…For instance, Naveed et al (2017a) showed that rhizodeposits from barley roots weakened soil as opposed to rhizodeposits from maize, which stabilised soil. Rhizodeposits are an important carbon source for soil microbiota, including fungi and bacteria, which play an important role in the formation of microaggregates in the rhizosphere (Vidal et al, 2018). Microbial decomposition of root exudates may also reverse the weakening/stabilising effect of rhizodeposits (Naveed et al, 2017a).…”

Root‐induced soil deformation influences Fe, S and P: rhizosphere chemistry investigated using synchrotron XRF and XANES

“…In order to regulate the poorly bioavailable Fe, plants exude phytosiderophores and/or organic acids as to increase its solubility. In a study by Vidal et al (2018), most of the microbial cells were found within microaggregates rich in Fe oxides. For example, barley has been shown to increase the root exudation of organic acids and siderophores three-fold during mild stress (Yang & Crowley, 2000).…”

Phenazine‐1‐carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces

“…For example, methods for the bulk extraction of EPS from soils (Redmile-Gordon et al, 2014) can establish the effects of microbial controls or environmental conditions upon the gross accumulation of EPS in soils over time, but imaging or molecular techniques are necessary to establish the effects of specific stimuli or regulators upon the development of biofilms at root surfaces. In prior studies, imaging techniques such as scanning and transmission electron microscopy (SEM and TEM) and nano-scale secondary-ion mass spectrometry (NanoSIMS) have revealed the distribution of microbial biomass and EPS on soil and root surfaces (Roberson and Firestone, 1992;Chenu, 1993;Dandurand et al, 1997;Watt et al, 2006;Herrmann et al, 2007;Keiluweit et al, 2012;Schurig et al, 2013) and patterns of nutrient uptake and transfer among roots, fungi and bacteria in the rhizosphere (Clode et al, 2009;Jones et al, 2013;Nuccio et al, 2013;Kaiser et al, 2015;Pett-Ridge and Firestone, 2017;Vidal et al, 2018).…”