A history of repeated antibiotic usage leads to microbiota-dependent mucus defects

Gut Microbes. 2024 Jan-Dec;16(1):2377570. doi: 10.1080/19490976.2024.2377570. Epub 2024 Jul 21.

Abstract

Recent evidence indicates that repeated antibiotic usage lowers microbial diversity and ultimately changes the gut microbiota community. However, the physiological effects of repeated - but not recent - antibiotic usage on microbiota-mediated mucosal barrier function are largely unknown. By selecting human individuals from the deeply phenotyped Estonian Microbiome Cohort (EstMB), we here utilized human-to-mouse fecal microbiota transplantation to explore long-term impacts of repeated antibiotic use on intestinal mucus function. While a healthy mucus layer protects the intestinal epithelium against infection and inflammation, using ex vivo mucus function analyses of viable colonic tissue explants, we show that microbiota from humans with a history of repeated antibiotic use causes reduced mucus growth rate and increased mucus penetrability compared to healthy controls in the transplanted mice. Moreover, shotgun metagenomic sequencing identified a significantly altered microbiota composition in the antibiotic-shaped microbial community, with known mucus-utilizing bacteria, including Akkermansia muciniphila and Bacteroides fragilis, dominating in the gut. The altered microbiota composition was further characterized by a distinct metabolite profile, which may be caused by differential mucus degradation capacity. Consequently, our proof-of-concept study suggests that long-term antibiotic use in humans can result in an altered microbial community that has reduced capacity to maintain proper mucus function in the gut.

Keywords: Akkermansia; Antibiotics; colonic mucosa; fecal microbiota transplantation; gut microbiome; intestinal barrier; mucus; short-chain fatty acids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Akkermansia
  • Animals
  • Anti-Bacterial Agents* / pharmacology
  • Bacteria* / classification
  • Bacteria* / drug effects
  • Bacteria* / genetics
  • Bacteria* / isolation & purification
  • Bacteria* / metabolism
  • Bacteroides fragilis / drug effects
  • Colon / microbiology
  • Fecal Microbiota Transplantation*
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome* / drug effects
  • Humans
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Mucus* / metabolism
  • Mucus* / microbiology

Substances

  • Anti-Bacterial Agents

Supplementary concepts

  • Akkermansia muciniphila

Grants and funding

This work was supported by the Estonian Research Council grant PUT [#PRG1414 and #1371], the Swedish Research Council [#2018-02095 and #2021-06602], the European Union through the Horizon 2020 research and innovation program [#810645] and MIBEst H2020-WIDESPREAD-2018-2020/GA [#857518] and through the European Regional Development Fund [#MOBEC008] as well as through an EMBO Installation grant (#3573).