Bioremediation of a Common Product of Food Processing by a Human Gut Bacterium

Ashley R. Wolf; Darryl A. Wesener; Jiye Cheng; Alexandra N. Houston-Ludlam; Zachary W. Beller; Matthew C. Hibberd; Richard J. Giannone; Samantha L. Peters; Robert L. Hettich; Semen A. Leyn; Dmitry A. Rodionov; Andrei L. Osterman; Jeffrey I. Gordon

doi:10.1016/j.chom.2019.09.001

Bioremediation of a Common Product of Food Processing by a Human Gut Bacterium

Ashley R. Wolf, Darryl A. Wesener, Jiye Cheng, Alexandra N. Houston-Ludlam, Zachary W. Beller, Matthew C. Hibberd, Richard J. Giannone, Samantha L. Peters, Robert L. Hettich, Semen A. Leyn, Dmitry A. Rodionov, Andrei L. Osterman, Jeffrey I. Gordon

Research output: Contribution to journal › Article › peer-review

41 Scopus citations

Abstract

Dramatic increases in processed food consumption represent a global health threat. Maillard reaction products (MRPs), which are common in processed foods, form upon heat-induced reaction of amino acids with reducing sugars and include advanced glycation end products with deleterious health effects. To examine how processed foods affect the microbiota, we fed gnotobiotic mice, colonized with 54 phylogenetically diverse human gut bacterial strains, defined sugar-rich diets containing whey as the protein source or a matched amino acid mixture. Whey or ϵ-fructoselysine, an MRP in whey and many processed foods, selectively increases Collinsella intestinalis absolute abundance and induces Collinsella expression of genomic loci directing import and metabolism of ϵ-fructoselysine to innocuous products. This locus is repressed by glucose in C. aerofaciens, whose abundance decreases with whey, but is not repressed in C. intestinalis. Identifying gut organisms responding to and degrading potentially harmful processed food components has implications for food science, microbiome science, and public health.

Original language	English
Pages (from-to)	463-477.e8
Journal	Cell Host and Microbe
Volume	26
Issue number	4
DOIs	https://doi.org/10.1016/j.chom.2019.09.001
State	Published - Oct 9 2019

Funding

We thank D. O’Donnell, M. Karlsson, J. Serugo, and S. Wagoner for their assistance with gnotobiotic mouse husbandry; B. Mickelson (Envigo Co.) for her guidance in designing experimental diets; M. Meier, J. Hoisington-Lopez, and M. Crosby for technical assistance with library preparation and sequencing; J. Lelwala-Guruge for advice on anaerobic culturing; V. Kung for assistance with intestinal sample collection; and members of the Gordon laboratory for many helpful discussions. We are grateful to J. Janetka for generously providing resources to support synthesis of fructoselysine. This work was supported by NIH grants DK70977 , DK078669 , and DK30292 and by a postdoctoral fellowship to A.R.W ( American Diabetes Association , United States, grant 1-16-PDF-125 ). D.A.W. is a Damon Runyon Fellow supported by the Damon Runyon Cancer Research Foundation , United States ( DRG-2303-17 ). D.A.R. and S.A.L. were supported by the Russian Science Foundation (grant 19-14-00305 ). We thank D. O'Donnell, M. Karlsson, J. Serugo, and S. Wagoner for their assistance with gnotobiotic mouse husbandry; B. Mickelson (Envigo Co.) for her guidance in designing experimental diets; M. Meier, J. Hoisington-Lopez, and M. Crosby for technical assistance with library preparation and sequencing; J. Lelwala-Guruge for advice on anaerobic culturing; V. Kung for assistance with intestinal sample collection; and members of the Gordon laboratory for many helpful discussions. We are grateful to J. Janetka for generously providing resources to support synthesis of fructoselysine. This work was supported by NIH grants DK70977, DK078669, and DK30292 and by a postdoctoral fellowship to A.R.W (American Diabetes Association, United States, grant 1-16-PDF-125). D.A.W. is a Damon Runyon Fellow supported by the Damon Runyon Cancer Research Foundation, United States (DRG-2303-17). D.A.R. and S.A.L. were supported by the Russian Science Foundation (grant 19-14-00305). A.R.W. and J.I.G. conceived the project and designed the experiments. A.R.W. performed the experiments and analyzed the data. D.A.W. synthesized fructoselysine and provided input on experimental design and data analysis. J.C. performed mass spectrometry and analyzed the data. A.N.H.-L. assisted with the experiment shown in Figure 4A. Z.W.B. analyzed the homology of loci in Figure 4D. D.A.R. and S.A.L. analyzed FrlR regulators and reconstructed their regulons. D.A.R. and A.L.O. reconstructed metabolic pathways in the analyzed community strains. R.J.G. S.L.P. and R.L.H. performed mass spectrometry on whey protein isolate and analyzed the resulting data. M.C.H. wrote portions of the analysis pipeline and advised on experimental design and data analysis. A.R.W. and J.I.G. wrote the paper with helpful input from D.A.W. J.I.G. is a co-founder of Matatu Inc. a company characterizing the role of diet-by-microbiota interactions in animal health. The other authors declare no competing interests.

Keywords

Collinsella species
Maillard reaction products
gnotobiotic mice
human gut microbiome
processed foods
transcriptional and metabolic regulation

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10.1016/j.chom.2019.09.001

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Wolf, A. R., Wesener, D. A., Cheng, J., Houston-Ludlam, A. N., Beller, Z. W., Hibberd, M. C., Giannone, R. J., Peters, S. L., Hettich, R. L., Leyn, S. A., Rodionov, D. A., Osterman, A. L., & Gordon, J. I. (2019). Bioremediation of a Common Product of Food Processing by a Human Gut Bacterium. Cell Host and Microbe, 26(4), 463-477.e8. https://doi.org/10.1016/j.chom.2019.09.001

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Bioremediation of a Common Product of Food Processing by a Human Gut Bacterium

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