Biogels in Soils: Plant Mucilage as a Biofilm Matrix That Shapes the Rhizosphere Microbial Habitat

Abstract

Mucilage is a gelatinous high-molecular-weight substance produced by almost all plants, serving numerous functions for plant and soil. To date, research has mainly focused on hydraulic and physical functions of mucilage in the rhizosphere. Studies on the relevance of mucilage as a microbial habitat are scarce. Extracellular polymeric substances (EPS) are similarly gelatinous high-molecular-weight substances produced by microorganisms. EPS support the establishment of microbial assemblages in soils, mainly through providing a moist environment, a protective barrier, and serving as carbon and nutrient sources. We propose that mucilage shares physical and chemical properties with EPS, functioning similarly as a biofilm matrix covering a large extent of the rhizosphere. Our analyses found no evidence of consistent differences in viscosity and surface tension between EPS and mucilage, these being important physical properties. With regard to chemical composition, polysaccharide, protein, neutral monosaccharide, and uronic acid composition also showed no consistent differences between these biogels. Our analyses and literature review suggest that all major functions known for EPS and required for biofilm formation are also provided by mucilage, offering a protected habitat optimized for nutrient mobilization. Mucilage enables high rhizo-microbial abundance and activity by functioning as carbon and nutrient source. We suggest that the role of mucilage as a biofilm matrix has been underestimated, and should be considered in conceptual models of the rhizosphere.

Soil, climate, and variety impact on quantity and quality of maize root mucilage exudation

“…This viewpoint is bolstered by the observation that mucilage increases the rhizosphere water content and facilitates root water uptake, delaying the onset of hydraulic failure during conditions with high vapor pressure deficit (Ahmed et al 2014;Carminati et al 2010;Naveed et al 2019;Nazari et al 2020). Moreover, mucilage is a potential biofilm matrix and protective habitat for the rhizosphere microbiome, with all mucilage sugars functioning as a potential energy source (Bennett et al 2020;Nazari et al 2022). Thus, another reason for the higher mucilage exudation rate could be the protection and feeding of a beneficial rhizosphere microbiome for promoting survival despite the increased temperature and The German loam soil induced 73.7% greater mucilage exudation than the Kenyan sandy-clay loam did (Fig.…”

“…1). Given that mucilage is released into the soil, microorganisms in the rhizosphere can considerably influence its exudation, but vice versa the presence of mucilage can positively affect microbial growth and abundance (Nazari et al 2022). Thus, the fivefold higher microbial biomass in the German loam soil (493 μg g −1 soil) compared to the Kenyan sandy-clay loam soil (103 μg g −1 soil) likely profits from the provision of this carbon source by the root.…”

“…Other studies demonstrated that microorganisms in the rhizosphere modify the exudation and composition of amino acids, flavonoids, and fatty acids released from the root (Dardanelli et al 2010;Matilla et al 2010;Phillips et al 2004), suggesting that mucilage exudation may also be stimulated by a high microbial abundance in the rhizosphere. Although similar studies have not yet been done on mucilage exudation, it is likely that mucilage plays a key role in the establishment of rhizosphere microbial communities (Nazari et al 2022).…”

“…This underlines the role of mucilage as a carbon source for the rhizosphere microbiome. The potential role of mucilage as a biofilm matrix harboring the rhizosphere microbiome (Nazari et al 2022) further motivates this perspective. However, more studies are required to identify plant-microbial signaling mechanisms that may control root mucilage exudation and composition.…”

“…from Mexico harbors diazotrophic bacteria that fix atmospheric nitrogen and provide 29%-82% of the plant's nitrogen demand (Bennett et al 2020;Van Deynze et al 2018). Mucilage is also a potential biofilm matrix, similar to microbial extracellular polymeric substances (EPS), that shapes the rhizosphere microbial habitat (Benard et al 2019;Nazari et al 2022). Most of these functions are associated with the polysaccharide component of mucilage (Nazari 2021).…”