Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans

Michael L. Patnode; Zachary W. Beller; Nathan D. Han; Jiye Cheng; Samantha L. Peters; Nicolas Terrapon; Bernard Henrissat; Sophie Le Gall; Luc Saulnier; David K. Hayashi; Alexandra Meynier; Sophie Vinoy; Richard J. Giannone; Robert L. Hettich; Jeffrey I. Gordon

doi:10.1016/j.cell.2019.08.011

Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans

Michael L. Patnode, Zachary W. Beller, Nathan D. Han, Jiye Cheng, Samantha L. Peters, Nicolas Terrapon, Bernard Henrissat, Sophie Le Gall, Luc Saulnier, David K. Hayashi, Alexandra Meynier, Sophie Vinoy, Richard J. Giannone, Robert L. Hettich, Jeffrey I. Gordon

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

225 Scopus citations

Abstract

Development of microbiota-directed foods (MDFs) that selectively increase the abundance of beneficial human gut microbes, and their expressed functions, requires knowledge of both the bioactive components of MDFs and the mechanisms underlying microbe-microbe interactions. Here, gnotobiotic mice were colonized with a defined consortium of human-gut-derived bacterial strains and fed different combinations of 34 food-grade fibers added to a representative low-fiber diet consumed in the United States. Bioactive carbohydrates in fiber preparations targeting particular Bacteroides species were identified using community-wide quantitative proteomic analyses of bacterial gene expression coupled with forward genetic screens. Deliberate manipulation of community membership combined with administration of retrievable artificial food particles, consisting of paramagnetic microscopic beads coated with dietary polysaccharides, disclosed the contributions of targeted species to fiber degradation. Our approach, including the use of bead-based biosensors, defines nutrient-harvesting strategies that underlie, as well as alleviate, competition between Bacteroides and control the selectivity of MDF components.

Original language	English
Pages (from-to)	59-73.e13
Journal	Cell
Volume	179
Issue number	1
DOIs	https://doi.org/10.1016/j.cell.2019.08.011
State	Published - Sep 19 2019

Funding

We thank David O’Donnell, Maria Karlsson, Marty Meier, Justin Serugo, Sabrina Wagoner, Janaki Lelwala-Guruge, and J. Hoisington-López for superb technical assistance, Brigitte Laillet and Marie-Jeanne Crépeau for technical assistance in fiber characterization, and Michael Barratt, Darryl Wesener, and Jennifer Bando for helpful discussions. Pierre Aymard, Dominic Vellucci, and Luca Dimartino sourced fibers, processed freeze-dried diets, and assisted with proximate analysis of fibers. This work was supported by grants from the NIH ( DK070977 , DK078669 , and F32DK107158 ), Mondelez International , and the US Department of Energy ( DE-SC0015662 ).

Keywords

biosensors
community ecology
interspecies competition
microbiota-directed foods
polysaccharide utilization

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10.1016/j.cell.2019.08.011

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Patnode, M. L., Beller, Z. W., Han, N. D., Cheng, J., Peters, S. L., Terrapon, N., Henrissat, B., Le Gall, S., Saulnier, L., Hayashi, D. K., Meynier, A., Vinoy, S., Giannone, R. J., Hettich, R. L., & Gordon, J. I. (2019). Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans. Cell, 179(1), 59-73.e13. https://doi.org/10.1016/j.cell.2019.08.011

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title = "Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans",

abstract = "Development of microbiota-directed foods (MDFs) that selectively increase the abundance of beneficial human gut microbes, and their expressed functions, requires knowledge of both the bioactive components of MDFs and the mechanisms underlying microbe-microbe interactions. Here, gnotobiotic mice were colonized with a defined consortium of human-gut-derived bacterial strains and fed different combinations of 34 food-grade fibers added to a representative low-fiber diet consumed in the United States. Bioactive carbohydrates in fiber preparations targeting particular Bacteroides species were identified using community-wide quantitative proteomic analyses of bacterial gene expression coupled with forward genetic screens. Deliberate manipulation of community membership combined with administration of retrievable artificial food particles, consisting of paramagnetic microscopic beads coated with dietary polysaccharides, disclosed the contributions of targeted species to fiber degradation. Our approach, including the use of bead-based biosensors, defines nutrient-harvesting strategies that underlie, as well as alleviate, competition between Bacteroides and control the selectivity of MDF components.",

keywords = "biosensors, community ecology, interspecies competition, microbiota-directed foods, polysaccharide utilization",

author = "Patnode, {Michael L.} and Beller, {Zachary W.} and Han, {Nathan D.} and Jiye Cheng and Peters, {Samantha L.} and Nicolas Terrapon and Bernard Henrissat and {Le Gall}, Sophie and Luc Saulnier and Hayashi, {David K.} and Alexandra Meynier and Sophie Vinoy and Giannone, {Richard J.} and Hettich, {Robert L.} and Gordon, {Jeffrey I.}",

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year = "2019",

month = sep,

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doi = "10.1016/j.cell.2019.08.011",

language = "English",

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Patnode, ML, Beller, ZW, Han, ND, Cheng, J, Peters, SL, Terrapon, N, Henrissat, B, Le Gall, S, Saulnier, L, Hayashi, DK, Meynier, A, Vinoy, S, Giannone, RJ , Hettich, RL & Gordon, JI 2019, 'Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans', Cell, vol. 179, no. 1, pp. 59-73.e13. https://doi.org/10.1016/j.cell.2019.08.011

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AU - Patnode, Michael L.

AU - Beller, Zachary W.

AU - Han, Nathan D.

AU - Cheng, Jiye

AU - Peters, Samantha L.

AU - Terrapon, Nicolas

AU - Henrissat, Bernard

AU - Le Gall, Sophie

AU - Saulnier, Luc

AU - Hayashi, David K.

AU - Meynier, Alexandra

AU - Vinoy, Sophie

AU - Giannone, Richard J.

AU - Hettich, Robert L.

AU - Gordon, Jeffrey I.

PY - 2019/9/19

Y1 - 2019/9/19

N2 - Development of microbiota-directed foods (MDFs) that selectively increase the abundance of beneficial human gut microbes, and their expressed functions, requires knowledge of both the bioactive components of MDFs and the mechanisms underlying microbe-microbe interactions. Here, gnotobiotic mice were colonized with a defined consortium of human-gut-derived bacterial strains and fed different combinations of 34 food-grade fibers added to a representative low-fiber diet consumed in the United States. Bioactive carbohydrates in fiber preparations targeting particular Bacteroides species were identified using community-wide quantitative proteomic analyses of bacterial gene expression coupled with forward genetic screens. Deliberate manipulation of community membership combined with administration of retrievable artificial food particles, consisting of paramagnetic microscopic beads coated with dietary polysaccharides, disclosed the contributions of targeted species to fiber degradation. Our approach, including the use of bead-based biosensors, defines nutrient-harvesting strategies that underlie, as well as alleviate, competition between Bacteroides and control the selectivity of MDF components.

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KW - community ecology

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Interspecies Competition Impacts Targeted Manipulation of Human Gut Bacteria by Fiber-Derived Glycans

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