Water flow drives small scale biogeography of pesticides and bacterial pesticide degraders - A microcosm study using 2,4-D as a model compound

Abstract Complex interactions between biodegradation and mass transfer of organic compounds drive the fate of pesticides in soil ecosystems. We hypothesized that, at the small-scale, co-location of degraders and pollutants in soils may be a prerequisite for efficient biodegradation of these chemicals. In non-co-localized micro-environments, however, diffusive and advective solute transport as well as active transport of microbial degraders towards their corresponding substrate may improve the accessibility of microbial substrates. The objective of this study was to test whether water flow can accelerate microbial pesticide degradation by facilitating the encounter of spatially separated pesticides and bacterial degraders at the millimeter scale. Combining natural and sterilized soil aggregates, we built soil cores with different spatial localizations of the pesticide 2,4-dichlorophenoxyacetic acid (2,4-D) and microbial degraders: (i) homogeneous distribution of microorganisms and 2,4-D throughout the soil core, (ii) co-localized microorganisms and 2,4-D in a mm 3 soil location, and iii) separated microorganisms and 2,4-D in two mm 3 soil locations spaced 1 cm apart. Following the fate of 14 C labelled 2,4-D (mineralization, extractable and non-extractable residues) as well as the abundance of bacterial 2,4-D degraders harboring the tfdA gene over an incubation period of 24 days, we observed decreased biodegradation of 2,4-D with increasing spatial separation between substrate and bacterial degraders. We found evidence that advection is a key process controlling the accessibility of 2,4-D and pesticide degraders. Advective solute transport induced leaching of about 50% of the initially applied 2,4-D regardless of initial spatial distribution patterns. Simultaneously, advective transport of 2,4-D and bacterial degraders triggered their re-encounter and compensated for the leaching-induced separation of initially co-localized microorganisms and 2,4-D. This resulted in effective biodegradation of 2,4-D, comparable to the homogeneous treatment. Similarly, advective transport processes brought substrate and degraders into contact if both were initially separated. Thus, advection more effectively removed bioaccessibility limitations to pesticide degradation than diffusive transport alone. These results emphasize the importance of considering spatial microbial ecology as well as biogeophysics at the mm scale to better understand the fate of pesticides at larger scales in soil.