Changes in Microbiome Confer Multigenerational Host Resistance after Sub-toxic Pesticide Exposure

The gut is a first point of contact with ingested xenobiotics, where chemicals are metabolized directly by the host or microbiota. Atrazine is a widely used pesticide, but the role of the microbiome metabolism of this xenobiotic and the impact on host responses is unclear. We exposed successive generations of the wasp Nasonia vitripennis to subtoxic levels of atrazine and observed changes in the structure and function of the gut microbiome that conveyed atrazine resistance. This microbiome-mediated resistance was maternally inherited and increased over successive generations, while also heightening the rate of host genome selection. The rare gut bacteria Serratia marcescens and Pseudomonas protegens contributed to atrazine metabolism. Both of these bacteria contain genes that are linked to atrazine degradation and were sufficient to confer resistance in experimental wasp populations. Thus, pesticide exposure causes functional, inherited changes in the microbiome that should be considered when assessing xenobiotic exposure and as potential countermeasures to toxicity. [Display omitted] •Atrazine exposure leads to changes in host microbiota that are vertically transmitted•Atrazine is toxic to the hymenopteran model Nasonia at very high doses•Specific gut bacteria metabolize atrazine and are enriched after atrazine exposure•Multi-generational exposure causes host genome divergence Wang et al. demonstrate low-level toxicity of atrazine in Nasonia wasps. A single, sub-toxic exposure causes changes in the gut microbiota that are transmitted to the next generation. Populations that are exposed every generation become resistant to high-level exposure, with atrazine resistance conferred by metabolic capabilities of at least two rare bacteria.