Diffusion-limited iron transformations in artificial soil aggregates: The impact of small-scale heterogeneity on cycling of redox-sensitive elements

Structured soils are typically heterogeneous composites of chemical and biological constituents within an intricate physical framework, which has variable geometry, composition and stability expressed over spatial scales of several orders of magnitude. In such settings, solutes move preferentially (by advection) through macropores and slowly (by diffusion) into intra-aggregate micropores, which promotes the establishment of redox gradients at the aggregate scale. Consequently, in such structured environments characterized by mass transfer limitation and redox gradients within soil aggregates, metals distribution can be strongly localized and the interrelated transport and biogeochemical processes control the fate of redox-sensitive contaminants and metals. Iron (hydr)oxides are particularly ubiquitous in soils and sediments and hence exert a pronounced effect on the fate and transport of nutrients and contaminants. As they are subject to both biotic and abiotic redox transformations, iron cycling depends on a tight interplay between hydrodynamic transport, and (bio)geochemical reactions depending on substrate distribution and microbial activity patterns. In this study, we present an experimental/modelling approach aimed at a qualitative and quantitative understanding of bioreductive processes at the microscale, and between advective and diffusive domains. Artificial soil aggregates, representing systems of intermediate complexity, were used to study the coupling of physical, chemical, and biological processes affecting iron oxides transformations, under environmentally relevant geometries. We used novel aggregate-based reaction flow cell experiments and reactive transport modeling to determine mass transfer and biogeochemical redox controls on the cycling of iron ranging from micropore- to aggregate-scales. Aggregates were made of ferrihydrite coated-sand and inoculated with Shewanella putrefaciens. Lactate was added in the input solution. Chemical gradients, spatial distribution of bacteria, and solid phase constituents were determined, to quantify magnitude, as well as temporal and spatial heterogeneity in biotransformation rates of iron. After 9 days of reaction, a slight and uniform transformation of ferrihydrite results in approximately 10% (mol Fe) of goethite and 10% (mol Fe) magnetite. While this distribution remains steady within the outer portion of the aggregate, toward the aggregate center, goethite becomes the dominant product (60% (mol Fe)) after 36 days of reaction. Due to the localized buildup of both Fe(II) and bicarbonate, up to 15% (mol Fe) siderite also results within aggregate centers while no magnetite was detected. Our results demonstrate the large variation in biotransformation of iron within soil aggregates characterized by a transition between advective and diffusive transport domains. They illustrate the importance of small-scale chemical conditions, dynamics of bioreductive processes at the microscale, and the microbial dynamics in situ for assessing bulk elemental cycling.