An integrated host-microbiome response to atrazine exposure mediates toxicity in Drosophila

James B. Brown*, Sasha A. Langley, Antoine M. Snijders, Kenneth H. Wan, Siti Nur Sarah Morris, Benjamin W. Booth, William W. Fisher, Ann S. Hammonds, Soo Park, Richard Weiszmann, Charles Yu, Jennifer A. Kirwan, Ralf J.M. Weber, Mark R. Viant, Jian Hua Mao, Susan E. Celniker

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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Abstract

The gut microbiome produces vitamins, nutrients, and neurotransmitters, and helps to modulate the host immune system—and also plays a major role in the metabolism of many exogenous compounds, including drugs and chemical toxicants. However, the extent to which specific microbial species or communities modulate hazard upon exposure to chemicals remains largely opaque. Focusing on the effects of collateral dietary exposure to the widely used herbicide atrazine, we applied integrated omics and phenotypic screening to assess the role of the gut microbiome in modulating host resilience in Drosophila melanogaster. Transcriptional and metabolic responses to these compounds are sex-specific and depend strongly on the presence of the commensal microbiome. Sequencing the genomes of all abundant microbes in the fly gut revealed an enzymatic pathway responsible for atrazine detoxification unique to Acetobacter tropicalis. We find that Acetobacter tropicalis alone, in gnotobiotic animals, is sufficient to rescue increased atrazine toxicity to wild-type, conventionally reared levels. This work points toward the derivation of biotic strategies to improve host resilience to environmental chemical exposures, and illustrates the power of integrative omics to identify pathways responsible for adverse health outcomes.

Original languageEnglish
Article number1324
JournalCommunications Biology
Volume4
Issue number1
DOIs
Publication statusPublished - 24 Nov 2021

Bibliographical note

Funding Information:
We thank members of the BDGP for their input. We thank the National Center for Genome Resources for PacBio sequencing of the fly microbes. We thank the UC Berkeley Fly Food Facility (Alison Killilea, Loida Pineda, and Sara Sosa) for fly food. We thank Martin Jones and Judith Ngere (University of Birmingham, UK) for assisting with the metabolomics data collection. We thank the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions. This work was supported by the Laboratory Directed Research and Development Program of Lawrence Berkeley National Laboratory under U.S. Department of Energy Contract No. DE-AC02-05CH11231. Additional support was provided by NIEHS: R01ES031322 to AMS.

ASJC Scopus subject areas

  • Medicine (miscellaneous)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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