Pesticides are widely used in agriculture despite their negative impact on ecosystems and human health. Biogeochemical modeling facilitates the mechanistic understanding of microbial controls on pesticide turnover in soils. We propose to inform models of coupled microbial dynamics and pesticide turnover with measurements of the abundance and expression of functional genes. To assess the advantages of informing models with genetic data, we developed a novel “gene-centric” model and compared model variants of differing structural complexity against a standard biomass-based model. The models were calibrated and validated using data from two batch experiments in which the degradation of the pesticides dichlorophenoxyacetic acid (2,4-D) and 2-methyl-4-chlorophenoxyacetic acid (MCPA) were observed in soil. When calibrating against data on pesticide mineralization, the gene-centric and biomass-based models performed equally well. However, accounting for pesticide-triggered gene regulation allows improved performance in capturing microbial dynamics and in predicting pesticide mineralization. This novel modeling approach also reveals a hysteretic relationship between pesticide degradation rates and gene expression, implying that the biodegradation performance in soils cannot be directly assessed by measuring the expression of functional genes. Our gene-centric model provides an effective approach for exploiting molecular biology data to simulate pesticide degradation in soils.

Pesticide persistence in soils is a widespread environmental concern in agro-ecosystems. One particularly persistent pesticide is atrazine, which continues to be found in soils and groundwater in the EU despite having been banned since 2004. A range of physical and biological barriers, such as sorption and mass-transfer into bacterial cells, might limit atrazine degradation in soils. These effects have been observed in experiments and models working with simplified systems. We build on that work by developing a biogeochemical model of the degradation process. We extended existing engineered system models by including refined representations of mass-transfer processes across the cell membrane as well as thermodynamic growth constraints. We estimated model parameters by calibration with data on atrazine degradation, metabolite (hydroxyatrazine) formation, biomass, and isotope fractionation from a set of controlled retentostat/chemostat experiments. We then produced site-specific model predictions for arable topsoil and compared them with field observations of residual atrazine concentrations. We found that the model overestimated long-term atrazine biodegradation in soils, indicating that this process is likely not limited by bioavailability or energetic constraints of microbial growth. However, sorption-limited bioavailability, could explain the long-term fate and persistence of the main degradation metabolite hydroxyatrazine. Future studies should seek alternative controls that drive the observed atrazine persistence in soil. This work helps to bridge the gap between engineered and natural systems, allowing us to use laboratory setups to gain insight into real environmental systems.

Microbial pesticide degraders are heterogeneously distributed in soil. Their spatial aggregation at the millimeter scale reduces the frequency of degrader–pesticide encounter and can introduce transport limitations to pesticide degradation. We simulated reactive pesticide transport in soil to investigate the fate of the widely used herbicide 4-chloro-2-methylphenoxyacetic acid (MCPA) in response to differently aggregated distributions of degrading microbes. Four scenarios were defined covering millimeter scale heterogeneity from homogeneous (pseudo-1D) to extremely heterogeneous degrader distributions and two precipitation scenarios with either continuous light rain or heavy rain events. Leaching from subsoils did not occur in any scenario. Within the topsoil, increasing spatial heterogeneity of microbial degraders reduced macroscopic degradation rates, increased MCPA leaching, and prolonged the persistence of residual MCPA. In heterogeneous scenarios, pesticide degradation was limited by the spatial separation of degrader and pesticide, which was quantified by the spatial covariance between MCPA and degraders. Heavy rain events temporarily lifted these transport constraints in heterogeneous scenarios and increased degradation rates. Our results indicate that the mild millimeter scale spatial heterogeneity of degraders typical for arable topsoil will have negligible consequences for the fate of MCPA, but strong clustering of degraders can delay pesticide degradation.

Contamination of soils with pesticides and their metabolites is a global environmental threat. Deciphering the complex process chains involved in pesticide degradation is a prerequisite for finding effective solution strategies. This study applies prospective optimal design (OD) of experiments to identify laboratory sampling strategies that allow model-based discrimination of atrazine (AT) degradation pathways. We simulated virtual AT degradation experiments with a first-order model that reflects a simple reaction chain of complete AT degradation. We added a set of Monod-based model variants that consider more complex AT degradation pathways. Then, we applied an extended constraint-based parameter search algorithm that produces Monte-Carlo ensembles of realistic model outputs, in line with published experimental data.Differences between-model ensembles were quantified with Bayesian model analysis using an energy distance metric. AT degradation pathways following first-order reaction chains could be clearly distinguished from those predicted with Monod-based models. As expected, including measurements of specific