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Original article
Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation
  1. Benoit Chassaing1,
  2. Tom Van de Wiele2,
  3. Jana De Bodt2,
  4. Massimo Marzorati2,
  5. Andrew T Gewirtz1
  1. 1Center for Inflammation, Immunity and Infection, Institute for Biomedical Sciences, Georgia State University, Atlanta, Georgia, USA
  2. 2Center of Microbial Ecology and Technology (CMET), Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
  1. Correspondence to Dr Benoit Chassaing, Center for Inflammation, Immunity, and Infection, Institute for Biomedical Sciences, Georgia State University, Atlanta, GA 30312, USA; bchassaing{at}gsu.edu Pr Tom van de Wiele, Center of Microbial Ecology and Technology (CMET), Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

Abstract

Objective The intestinal microbiota plays a central role in the development of many chronic inflammatory diseases including IBD and metabolic syndrome. Administration of substances that alter microbiota composition, including the synthetic dietary emulsifiers polysorbate 80 (P80) and carboxymethylcellulose (CMC), can promote such inflammatory disorders. However, that inflammation itself impacts microbiota composition has obfuscated defining the extent to which these compounds or other substances act directly upon the microbiota versus acting on host parameters that promote inflammation, which subsequently reshapes the microbiota.

Design We examined the direct impact of CMC and P80 on the microbiota using the mucosal simulator of the human intestinal microbial ecosystem (M-SHIME) model that maintains a complex stable human microbiota in the absence of a live host.

Results This approach revealed that both P80 and CMC acted directly upon human microbiota to increase its proinflammatory potential, as revealed by increased levels of bioactive flagellin. The CMC-induced increase in flagellin was rapid (1 day) and driven by altered microbiota gene expression. In contrast, the P80-induced flagellin increase occurred more slowly and was closely associated with altered species composition. Transfer of both emulsifier-treated M-SHIME microbiotas to germ-free recipient mice recapitulated many of the host and microbial alterations observed in mice directly treated with emulsifiers.

Conclusions These results demonstrate a novel paradigm of deconstructing host–microbiota interactions and indicate that the microbiota can be directly impacted by these commonly used food additives, in a manner that subsequently drives intestinal inflammation.

  • INFLAMMATION
  • INTESTINAL MICROBIOLOGY

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Footnotes

  • Contributors Conception and design: BC, TVdW and ATG. Development of methodology: BC, TVdW and ATG. Acquisition of data: BC and JDB. Analysis and interpretation of data: BC, TVdW, JDB, MM and ATG. Writing, review and/or revision of the manuscript: BC and ATG. Study supervision: ATG.

  • Funding This work was supported by NIH grant DK099071 (ATG) and DK083890 (ATG). BC is a recipient of the Career Development Award from the Crohn's and Colitis Foundation of America (CCFA). TVdW is supported by UGent grant BOF2017-GOA-032. MM is supported by a postdoctoral mandate from Research Foundation Flanders (FWO).

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data sharing statement Metatranscriptomic: unprocessed sequencing data are deposited at MG-RAST http://metagenomics.anl.gov/linkin.cgi?project=mgp16059, samples mgs411584, mgs411587, mgs411590, mgs411593, mgs411596, mgs411599, mgs411602, mgs411605, mgs411608, mgs411611, mgs411614, mgs411617, mgs411620, mgs411623, mgs411626, mgs411629, mgs411632, mgs411635, mgs411638, mgs411641, mgs411644, mgs411647, mgs411650, mgs411653. 16S sequencing: unprocessed sequencing data are deposited in the European Nucleotide Archive under accession numbers PRJEB19279 (M-SHIME suspension) and PRJEB19272 (transplant of M-SHIME suspension to germ-free recipient mice).

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