Salmonella-Mediated Inflammation Eliminates Competitors for Fructose-Asparagine in the Gut

Infect Immun. 2018 Apr 23;86(5):e00945-17. doi: 10.1128/IAI.00945-17. Print 2018 May.

Abstract

Salmonella enterica elicits intestinal inflammation to gain access to nutrients. One of these nutrients is fructose-asparagine (F-Asn). The availability of F-Asn to Salmonella during infection is dependent upon Salmonella pathogenicity islands 1 and 2, which in turn are required to provoke inflammation. Here, we determined that F-Asn is present in mouse chow at approximately 400 pmol/mg (dry weight). F-Asn is also present in the intestinal tract of germfree mice at 2,700 pmol/mg (dry weight) and in the intestinal tract of conventional mice at 9 to 28 pmol/mg. These findings suggest that the mouse intestinal microbiota consumes F-Asn. We utilized heavy-labeled precursors of F-Asn to monitor its formation in the intestine, in the presence or absence of inflammation, and none was observed. Finally, we determined that some members of the class Clostridia encode F-Asn utilization pathways and that they are eliminated from highly inflamed Salmonella-infected mice. Collectively, our studies identify the source of F-Asn as the diet and that Salmonella-mediated inflammation is required to eliminate competitors and allow the pathogen nearly exclusive access to this nutrient.

Keywords: Amadori products; Clostridium; Maillard reaction; Salmonella; fructosamines; fructose-asparagine; gut inflammation; inflammation.

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
  • Asparagine / metabolism*
  • Fructose / metabolism*
  • Gastrointestinal Microbiome / immunology*
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Salmonella Infections, Animal / immunology*
  • Salmonella Infections, Animal / metabolism*
  • Salmonella Infections, Animal / pathology
  • Salmonella enterica / immunology*
  • Salmonella enterica / metabolism*
  • Salmonella enterica / pathogenicity

Substances

  • Fructose
  • Asparagine