Selective retention of extracellular polymeric substances induced by adsorption to and coprecipitation with ferrihydrite

Abstract Recent work shows that microbially-derived compounds constitute a significant fraction of the soil organic matter (OM) pool. These compounds include extracellular polymeric substances (EPS) whose mass can far exceed total microbial cell biomass. Sorption of EPS to soil minerals occurs via adsorption and coprecipitation and contributes to the preservation of OM in the soil environment. Little is known, however, about the sorption mechanisms of EPS and selective retention of different EPS constituents on iron (oxyhydr)oxides, especially during EPS adsorption versus coprecipitation with these reactive soil phases. This study examines how EPS interacts with the ubiquitous soil iron (oxyhydr)oxide ferrihydrite during EPS adsorption and coprecipitation and whether these different EPS-mineral association pathways affect EPS sorption and selective retention, and thus the mobility and fate of microbially-derived OM in the soil environment. We use several complimentary techniques to i) examine EPS-carbon, EPS-nitrogen and EPS-phosphorus sorption and fractionation, ii) visualize spatial relationships between EPS biomolecular classes and ferrihydrite using confocal laser scanning microscopy (CLSM), iii) determine EPS-C speciation and chemical fractionation with ferrihydrite using X-ray photoelectron spectroscopy (XPS) and near-edge X-ray absorption fine structure spectroscopy (NEXAFS), and iv) determine functional group interactions with ferrihydrite using Fourier transform infrared spectroscopy (FTIR) combined with two-dimensional correlation spectroscopy (2D-COS) analysis. Results show that the coprecipitation of EPS does not change the ferrihydrite mineralogy, as the main mineral phase for EPS association, but it substantially increases the particle size of EPS-ferrihydrite. A substantial difference in the EPS mass fraction associated with the ferrihydrite is observed between the adsorption and coprecipitation experiments at an initial molar C/Fe ratio > 1. The EPS-N is relatively enriched during the adsorption process, while more EPS-C and near-complete EPS-P are fixed in the coprecipitation process. XPS results show that the surface of the ferrihydrite formed through EPS adsorption is preferentially enriched with protein-like components, whereas, the surface of the ferrihydrite formed through EPS coprecipitation is enriched with polysaccharide-like components, which is visually confirmed with CLSM images. NEXAFS results reveal that the carboxylic/amide C-containing components are selectively retained during adsorption, with the aliphatic and O-alkyl C-containing components relatively enriched during coprecipitation. 2D-FTIR-COS results indicate that during EPS adsorption on ferrihydrite the P=O functional groups are adsorbed faster than the amide and carboxylate functional groups, while during EPS coprecipitation with ferrihydrite the opposite trend is observed. The findings from this study indicate that the formation pathway of EPS-ferrihydrite associations substantially effects the sorption mechanisms and selective retention of EPS and may thus affect the mobility and fate of microbially-derived carbon (C), nitrogen (N) and phosphorus (P) in soils. These new insights on EPS behavior at the mineral-water interface might be used to evaluate how microbially-derived compounds like EPS are stabilized by iron (oxyhydr)oxides and how EPS-iron (oxyhydr)oxide couplings might affect the reactivity and cycling of OM in natural environments.