The functional role of earthworm mucus during aggregation

• Published in: Journal of plant nutrition and soil science 2024-02, Vol.187 (1), p.63-76
• Main Authors: Guhra, Tom, Wonneberger, Arnold, Stolze, Katharina, Ritschel, Thomas, Totsche, Kai Uwe
• Format: Article
• Language: English
• Subjects: Adsorption; biogenically excreted organic matter; Biopolymers; Bioturbation; bridging agent; Carbon sequestration; electrostatic interactions; Goethite; hetero‐aggregation; homo‐aggregation; Lipids; Lumbricidae; Molecular properties; Molecular structure; Mucus; Oligochaeta; pH controlled; pH effects; Polysaccharides; Protein adsorption; Proteins; Quartz; Saccharides; Separation; separation agent; Soil formation; Soil quality; Soil structure; Soils; Worms
• ISSN: 1436-8730; 1522-2624
• DOI: 10.1002/jpln.202300100

Background Soil organisms influence pedogenesis on a molecular level through the production of biopolymers which interact with soil minerals depending on their molecular properties. Specifically, biopolymers impact structure formation by inhibiting aggregation as a separation agent or promoting aggregation as a bridging agent. Mucus is a biopolymer excreted by earthworms that consists mainly of proteins, polysaccharides, and, to a lesser extent, lipids. However, despite earthworms’ fundamental contribution to soil quality and structuring via bioturbation, the role of mucus in aggregation still has to be unraveled. Aims Our study explores the role of cutaneous earthworm mucus (CEM) of Lumbricus terrestris L. for the formation of organo–mineral associations and aggregates, a sub‐process of pedogenesis. Methods We conducted batch experiments with goethite and CEM at different pH values and varying CEM concentrations to form mucus–goethite associations. Employing the newly formed mucus–goethite associations, we explored the (homo‐/hetero‐)aggregation with quartz particles as a function of the loading of surfaces with mucus‐C and CEM concentrations in solution. Results Our results suggest that the molecular structure of CEM constituents (especially proteins) is sensitive to pH. We found that the adsorption of CEM to goethite depends on pH and concentration. Polysaccharides of CEM adsorbed preferentially under acidic conditions (pH 3) and at low CEM concentration (6 mg mucus‐C L–1). In contrast, stronger adsorption of proteins was observed at higher CEM concentrations (30 mg mucus‐C L–1). In subsequent aggregation experiments, the hetero‐aggregation rate of organo–mineral associations and quartz decreased at low C‐loadings. Conversely, the rate increased at high loadings compared to the CEM‐free reference. Furthermore, electrostatic/steric repulsion (separation agent) inhibited the aggregation between goethite particles at high CEM concentrations in the solution (mineral/mucus ratio of 17). However, at a low CEM supply (mineral/mucus ratio of >83), CEM took the role of a bridging agent. Conclusions The composition, function, and (im‐)mobilization of CEM and corresponding organo–mineral associations in earthworm‐influenced soil structures are shaped by the structure/reactivity of CEM affected by environmental parameters. Formation and aggregation of mucus–mineral associations contribute to nutrient/carbon storage and are involved in the structure formation in soi