Metabolic impact of persistent organic pollutants on gut microbiota

Gut Microbes. 2020 Nov 9;12(1):1-16. doi: 10.1080/19490976.2020.1848209.

Abstract

Emerging evidence supports that exposure to persistent organic pollutants (POPs) can impact the interaction between the gut microbiota and host. Recent efforts have characterized the relationship between gut microbiota and environment pollutants suggesting additional research is needed to understand potential new avenues for toxicity. Here, we systematically examined the direct effects of POPs including 2,3,7,8-tetrachlorodibenzofuran (TCDF), 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), and polychlorinated biphenyls (PCB-123 and PCB-156) on the microbiota using metatranscriptomics and NMR- and mass spectrometry-based metabolomics combined with flow cytometry and growth rate measurements (OD600). This study demonstrated that (1) POPs directly and rapidly affect isolated cecal bacterial global metabolism that is associated with significant decreases in microbial metabolic activity; (2) significant changes in cecal bacterial gene expression related to tricarboxylic acid (TCA) cycle as well as carbon metabolism, carbon fixation, pyruvate metabolism, and protein export were observed following most POP exposure; (3) six individual bacterial species show variation in lipid metabolism in response to POP exposure; and (4) PCB-153 (non-coplanar)has a greater impact on bacteria than PCB-126 (coplanar) at the metabolic and transcriptional levels. These data provide new insights into the direct role of POPs on gut microbiota and begins to establish possible microbial toxicity endpoints which may help to inform risk assessment.

Keywords: NMR; Persistent organic pollutants; flow cytometry; growth rate measurements; gut microbiota; mass spectrometry; metabolomics; metatranscriptomics.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Bacteria / metabolism*
  • Benzofurans / toxicity
  • Carbon / metabolism
  • Cecum / drug effects
  • Cecum / microbiology
  • Citric Acid Cycle / drug effects
  • Gastrointestinal Microbiome / drug effects*
  • Lipid Metabolism / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Persistent Organic Pollutants / toxicity*
  • Polychlorinated Biphenyls / toxicity*
  • Polychlorinated Dibenzodioxins / toxicity*
  • Protein Transport / drug effects
  • Pyruvic Acid / metabolism

Substances

  • Benzofurans
  • Polychlorinated Dibenzodioxins
  • 2,3,3',4,4',5-hexachlorobiphenyl
  • Carbon
  • Pyruvic Acid
  • Polychlorinated Biphenyls
  • 3,4,5,3',4'-pentachlorobiphenyl
  • 2,3,7,8-tetrachlorodibenzofuran
  • 2,4,5,2',4',5'-hexachlorobiphenyl