Background <p>Foodborne pathogens, including <i>Salmonella enterica</i> serovar Typhimurium (<i>S</i>. Typhimurium), pose a significant threat to both human health and livestock productivity. The pandemic <i>S.</i> Typhimurium ST34 clone acquired a genomic island (SGI-4) conferring high copper resistance, an adaptation relevant in the context of the widespread use of copper sulphate at therapeutic levels in pig farming. We investigated how high dietary copper influences the piglet gut microbiota and <i>Salmonella</i>-microbiota interactions that may explain the global spread of <i>S.</i> Typhimurium ST34.</p> Results <p>An on-farm study combined with faecal shotgun metagenomics revealed that several potential <i>Salmonella</i> competitor species, including <i>Bifidobacterium</i>, <i>Escherichia</i>, and <i>Lactobacillus</i>, were less abundant in piglets on high-copper diets. Anaerobic and aerobic culturing alongside whole genome sequencing of 131 species and copper sulphate susceptibility testing identified copper resistance gene acquisition in selected microbes, particularly within <i>Escherichia</i>. Niche competition assays demonstrated that copper resistance is critical for inter-species competition under high-copper conditions, with <i>Salmonella</i>’s Type VI Secretion System providing a distinct advantage over <i>Escherichia</i> in the copper-modified niche.</p> Conclusions <p>Our findings suggest that copper supplementation alters the piglet gut environment, impacting competitive dynamics between pathogenic and commensal bacteria, likely to influence the zoonotic transmission of pathogens.</p> <p><MediaObject ID="MOESM7"> <VideoObject FileRef="MediaObjects/40168_2025_2322_MOESM7_ESM.mp4" VideoID="7HGfSp5tFGWTF9yHxnok5s"> <Caption Language="En" xml:lang="en"> <CaptionContent> <p>Video Abstract</p> </CaptionContent> </Caption> </VideoObject> </MediaObject></p>

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Copper is an intestinal habitat filter affecting the gut microbiota interactions with Salmonella Typhimurium

  • Rafał Kolenda,
  • Marwa M. Hassan,
  • Ainhoa Arrieta-Gisasola,
  • Abioseh Kamara,
  • Rebecca Ansorge,
  • Katarzyna Sidorczuk,
  • Luke Acton,
  • Gaëtan Thilliez,
  • Dave J. Baker,
  • Michał Burdukiewicz,
  • Mark D. Stares,
  • Hilary P. Browne,
  • Gwenaelle Le Gall,
  • Ricardo C. Torres,
  • Alfredo Chavez-Arroyo,
  • John Garrett,
  • Mark P. Stevens,
  • Trevor D. Lawley,
  • Andreas J. Bäumler,
  • Roberto La Ragione,
  • Falk Hildebrand,
  • Robert A. Kingsley

摘要

Background

Foodborne pathogens, including Salmonella enterica serovar Typhimurium (S. Typhimurium), pose a significant threat to both human health and livestock productivity. The pandemic S. Typhimurium ST34 clone acquired a genomic island (SGI-4) conferring high copper resistance, an adaptation relevant in the context of the widespread use of copper sulphate at therapeutic levels in pig farming. We investigated how high dietary copper influences the piglet gut microbiota and Salmonella-microbiota interactions that may explain the global spread of S. Typhimurium ST34.

Results

An on-farm study combined with faecal shotgun metagenomics revealed that several potential Salmonella competitor species, including Bifidobacterium, Escherichia, and Lactobacillus, were less abundant in piglets on high-copper diets. Anaerobic and aerobic culturing alongside whole genome sequencing of 131 species and copper sulphate susceptibility testing identified copper resistance gene acquisition in selected microbes, particularly within Escherichia. Niche competition assays demonstrated that copper resistance is critical for inter-species competition under high-copper conditions, with Salmonella’s Type VI Secretion System providing a distinct advantage over Escherichia in the copper-modified niche.

Conclusions

Our findings suggest that copper supplementation alters the piglet gut environment, impacting competitive dynamics between pathogenic and commensal bacteria, likely to influence the zoonotic transmission of pathogens.

Video Abstract