Elemental iron protects gut microbiota against oxygen-induced dysbiosis

PLoS One. 2024 Feb 27;19(2):e0298592. doi: 10.1371/journal.pone.0298592. eCollection 2024.

Abstract

Gut dysbiosis induced by oxygen and reactive oxygen species may be related to the development of inflammation, resulting in metabolic syndrome and associated-conditions in the gut. Here we show that elemental iron can serve as an antioxidant and reverse the oxygen-induced dysbiosis. Fecal samples from three healthy donors were fermented with elemental iron and/or oxygen. 16S rRNA analysis revealed that elemental iron reversed the oxygen-induced disruption of Shannon index diversity of the gut microbiota.The bacteria lacking enzymatic antioxidant systems also increased after iron treatment. Inter-individual differences, which corresponded to iron oxidation patterns, were observed for the tested donors. Gut bacteria responding to oxygen and iron treatments were identified as guilds, among which, Escherichia-Shigella was promoted by oxygen and depressed by elemental iron, while changes in bacteria such as Bifidobacterium, Blautia, Eubacterium, Ruminococcaceae, Flavonifractor, Oscillibacter, and Lachnospiraceae were reversed by elemental iron after oxygen treatment. Short-chain fatty acid production was inhibited by oxygen and this effect was partially reversed by elemental iron. These results suggested that elemental iron can regulate the oxygen/ROS state and protect the gut microbiota from oxidative stress.

MeSH terms

  • Antioxidants / metabolism
  • Bacteria / genetics
  • Dysbiosis / chemically induced
  • Dysbiosis / microbiology
  • Gastrointestinal Microbiome*
  • Humans
  • Iron / metabolism
  • Lactobacillales* / genetics
  • Oxygen / metabolism
  • RNA, Ribosomal, 16S / genetics
  • RNA, Ribosomal, 16S / metabolism

Substances

  • Oxygen
  • Antioxidants
  • Iron
  • RNA, Ribosomal, 16S

Grants and funding

This work was supported by the U.S.-Israel Binational Agricultural Research and Development Fund (BARD) (Vaadia-BARD Postdoctoral Fellowship Proposal No. Fl-580-2018 to I.O.), the NIH / NCCIH Postdoctoral Training Grant (5T32AT004094 to J.B.Z.), and by NIH / ODS / NCCIH Botanical Center Grant (P50 AT002776 to I.R.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.