Cooking shapes the structure and function of the gut microbiome

Carmody, Rachel N.; Bisanz, Jordan E.; Bowen, Benjamin P.; Maurice, Corinne F.; Lyalina, Svetlana; Louie, Katherine B.; Treen, Daniel; Chadaideh, Katia S.; Maini Rekdal, Vayu; Bess, Elizabeth N.; Spanogiannopoulos, Peter; Ang, Qi Yan; Bauer, Kylynda C.; Balon, Thomas W.; Pollard, Katherine S.; Northen, Trent R.; Turnbaugh, Peter J.

doi:10.1038/s41564-019-0569-4

Title: Cooking shapes the structure and function of the gut microbiome

Journal Article · 30 September 2019 · Nature Microbiology

DOI: https://doi.org/10.1038/s41564-019-0569-4 · OSTI ID:1615285

^[1];

^[2]; Bowen, Benjamin P. ^[3];

^[4]; Lyalina, Svetlana ^[2]; Louie, Katherine B. ^[3];

^[3]; Chadaideh, Katia S. ^[5]; Maini Rekdal, Vayu ^[5];

^[2]; Spanogiannopoulos, Peter ^[2]; Ang, Qi Yan ^[2]; Bauer, Kylynda C. ^[5]; Balon, Thomas W. ^[6];

^[7];

^[3];

^[8]

Univ. of California, San Francisco, CA (United States); Harvard Univ., Cambridge, MA (United States)
Univ. of California, San Francisco, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Harvard Univ., Cambridge, MA (United States); McGill Univ., Montreal, QC (Canada). Microbiome and Disease Tolerance Centre
Harvard Univ., Cambridge, MA (United States)
Boston Univ., MA (United States)
Univ. of California, San Francisco, CA (United States). Gladstone Inst.
Univ. of California, San Francisco, CA (United States); Harvard Univ., Cambridge, MA (United States); Chan Zuckerberg Biohub, San Francisco, CA (United States)

Diet is a critical determinant of variation in gut microbial structure and function, outweighing even host genetics. Numerous microbiome studies have compared diets with divergent ingredients but the everyday practice of cooking remains understudied. Here in this paper, we show that a plant diet served raw versus cooked reshapes the murine gut microbiome, with effects attributable to improvements in starch digestibility and degradation of plant-derived compounds. Shifts in the gut microbiota modulated host energy status, applied across multiple starch-rich plants, and were detectable in humans. Thus, diet-driven host–microbial interactions depend on the food as well as its form. Because cooking is human-specific, ubiquitous and ancient, our results prompt the hypothesis that humans and our microbiomes co-evolved under unique cooking-related pressures.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Institutes of Health (NIH); Boston Nutrition Obesity Research Center; Leakey Foundation; G.W. Hooper Foundation; Harvard Dean’s Competitive Fund for Promising Scholarship; William F. Milton Fund; the Defense Advanced Research Projects Agency (DARPA); Natural Sciences and Engineering Research Council of Canada; UCSF

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1615285

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 12 Vol. 4; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Viability states of bacteria-Specific mechanisms of selected probes Sträuber, Heike; Müller, Susann Cytometry Part A, Vol. 77A, Issue 7 https://doi.org/10.1002/cyto.a.20920	journal	May 2010
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
Optimization and testing of mass spectral library search algorithms for compound identification Stein, Stephen E.; Scott, Donald R. Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 9 https://doi.org/10.1016/1044-0305(94)87009-8	journal	September 1994
Xenobiotics Shape the Physiology and Gene Expression of the Active Human Gut Microbiome Maurice, Corinne Ferrier; Haiser, Henry Joseph; Turnbaugh, Peter James Cell, Vol. 152, Issue 1-2 https://doi.org/10.1016/j.cell.2012.10.052	journal	January 2013
Diet Dominates Host Genotype in Shaping the Murine Gut Microbiota Carmody, Rachel N.; Gerber, Georg K.; Luevano, Jesus M. Cell Host & Microbe, Vol. 17, Issue 1 https://doi.org/10.1016/j.chom.2014.11.010	journal	January 2015
Gut Commensal E. coli Proteins Activate Host Satiety Pathways following Nutrient-Induced Bacterial Growth Breton, Jonathan; Tennoune, Naouel; Lucas, Nicolas Cell Metabolism, Vol. 23, Issue 2 https://doi.org/10.1016/j.cmet.2015.10.017	journal	February 2016
p-Coumaric acid kills bacteria through dual damage mechanisms Lou, Zaixiang; Wang, Hongxin; Rao, Shengqi Food Control, Vol. 25, Issue 2 https://doi.org/10.1016/j.foodcont.2011.11.022	journal	June 2012
Dealing with the unknown: Metabolomics and Metabolite Atlases Bowen, Benjamin P.; Northen, Trent R. Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9 https://doi.org/10.1016/j.jasms.2010.04.003	journal	September 2010
The energetic significance of cooking Carmody, Rachel N.; Wrangham, Richard W. Journal of Human Evolution, Vol. 57, Issue 4 https://doi.org/10.1016/j.jhevol.2009.02.011	journal	October 2009
Toward ‘Omic Scale Metabolite Profiling: A Dual Separation–Mass Spectrometry Approach for Coverage of Lipid and Central Carbon Metabolism Ivanisevic, Julijana; Zhu, Zheng-Jiang; Plate, Lars Analytical Chemistry, Vol. 85, Issue 14 https://doi.org/10.1021/ac401140h	journal	July 2013
Defining and Detecting Complex Peak Relationships in Mass Spectral Data: The Mz.unity Algorithm Mahieu, Nathaniel G.; Spalding, Jonathan L.; Gelman, Susan J. Analytical Chemistry, Vol. 88, Issue 18 https://doi.org/10.1021/acs.analchem.6b01702	journal	August 2016
Effect of Food Thermal Processing on the Composition of the Gut Microbiota Pérez-Burillo, Sergio; Pastoriza, Silvia; Jiménez-Hernández, Nuria Journal of Agricultural and Food Chemistry, Vol. 66, Issue 43 https://doi.org/10.1021/acs.jafc.8b04077	journal	October 2018
Analysis of the Human Adult Urinary Metabolome Variations with Age, Body Mass Index, and Gender by Implementing a Comprehensive Workflow for Univariate and OPLS Statistical Analyses Thévenot, Etienne A.; Roux, Aurélie; Xu, Ying Journal of Proteome Research, Vol. 14, Issue 8 https://doi.org/10.1021/acs.jproteome.5b00354	journal	June 2015
Determination of Pharmacologically Active Ingredients in Sweet Potato ( Ipomoea batatas L.) by Capillary Electrophoresis with Electrochemical Detection Guan, Yueqing; Wu, Ting; Lin, Miao Journal of Agricultural and Food Chemistry, Vol. 54, Issue 1 https://doi.org/10.1021/jf0508347	journal	January 2006
Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon Ze, Xiaolei; Duncan, Sylvia H.; Louis, Petra The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.4	journal	February 2012
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Antibiotics in early life alter the murine colonic microbiome and adiposity Cho, Ilseung; Yamanishi, Shingo; Cox, Laura Nature, Vol. 488, Issue 7413 https://doi.org/10.1038/nature11400	journal	August 2012
Diet rapidly and reproducibly alters the human gut microbiome David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N. Nature, Vol. 505, Issue 7484 https://doi.org/10.1038/nature12820	journal	December 2013
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Global metabolic profiling procedures for urine using UPLC–MS Want, Elizabeth J.; Wilson, Ian D.; Gika, Helen Nature Protocols, Vol. 5, Issue 6 https://doi.org/10.1038/nprot.2010.50	journal	May 2010
Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry Dunn, Warwick B.; Broadhurst, David; Begley, Paul Nature Protocols, Vol. 6, Issue 7 https://doi.org/10.1038/nprot.2011.335	journal	June 2011
Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-63196-0	journal	April 2020
Potential use of molecular and structural characterization of the gut bacterial community for postmortem interval estimation in Sprague Dawley rats Li, Huan; Zhang, Siruo; Liu, Ruina Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-020-80633-2	journal	January 2021
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Energetic consequences of thermal and nonthermal food processing Carmody, R. N.; Weintraub, G. S.; Wrangham, R. W. Proceedings of the National Academy of Sciences, Vol. 108, Issue 48 https://doi.org/10.1073/pnas.1112128108	journal	November 2011
Rapid changes in the gut microbiome during human evolution Moeller, Andrew H.; Li, Yingying; Mpoudi Ngole, Eitel Proceedings of the National Academy of Sciences, Vol. 111, Issue 46 https://doi.org/10.1073/pnas.1419136111	journal	November 2014
Antibacterial Activity and Mode of Action of Ferulic and Gallic Acids Against Pathogenic Bacteria Borges, Anabela; Ferreira, Carla; Saavedra, Maria J. Microbial Drug Resistance, Vol. 19, Issue 4 https://doi.org/10.1089/mdr.2012.0244	journal	August 2013
Factors affecting the rate of hydrolysis of starch in food Snow, P.; O'Dea, K. The American Journal of Clinical Nutrition, Vol. 34, Issue 12 https://doi.org/10.1093/ajcn/34.12.2721	journal	December 1981
MZmine: toolbox for processing and visualization of mass spectrometry based molecular profile data Katajamaa, M.; Miettinen, J.; Oresic, M. Bioinformatics, Vol. 22, Issue 5 https://doi.org/10.1093/bioinformatics/btk039	journal	January 2006
Picante: R tools for integrating phylogenies and ecology Kembel, S. W.; Cowan, P. D.; Helmus, M. R. Bioinformatics, Vol. 26, Issue 11 https://doi.org/10.1093/bioinformatics/btq166	journal	April 2010
ROAST: rotation gene set tests for complex microarray experiments Wu, Di; Lim, Elgene; Vaillant, François Bioinformatics, Vol. 26, Issue 17 https://doi.org/10.1093/bioinformatics/btq401	journal	July 2010
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
MetaQuery: a web server for rapid annotation and quantitative analysis of specific genes in the human gut microbiome Nayfach, Stephen; Fischbach, Michael A.; Pollard, Katherine S. Bioinformatics, Vol. 31, Issue 20 https://doi.org/10.1093/bioinformatics/btv382	journal	June 2015
Genetic Evidence of Human Adaptation to a Cooked Diet Carmody, Rachel N.; Dannemann, Michael; Briggs, Adrian W. Genome Biology and Evolution, Vol. 8, Issue 4 https://doi.org/10.1093/gbe/evw059	journal	March 2016
KEGG for linking genomes to life and the environment Kanehisa, M.; Araki, M.; Goto, S. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm882	journal	December 2007
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Nucleic Acids Research, Vol. 43, Issue 7 https://doi.org/10.1093/nar/gkv007	journal	January 2015
A comparative study of the cytometric characteristics of High and Low nucleic-acid bacterioplankton cells from different aquatic ecosystems Bouvier, Thierry; del Giorgio, Paul A.; Gasol, Josep M. Environmental Microbiology, Vol. 9, Issue 8 https://doi.org/10.1111/j.1462-2920.2007.01321.x	journal	August 2007
Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies Alves, M. J.; Ferreira, I. C. F. R.; Froufe, H. J. C. Journal of Applied Microbiology, Vol. 115, Issue 2 https://doi.org/10.1111/jam.12196	journal	May 2013
Metabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5 Vijay-Kumar, M.; Aitken, J. D.; Carvalho, F. A. Science, Vol. 328, Issue 5975 https://doi.org/10.1126/science.1179721	journal	March 2010
Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans Muegge, B. D.; Kuczynski, J.; Knights, D. Science, Vol. 332, Issue 6032 https://doi.org/10.1126/science.1198719	journal	May 2011
BIOMEDICINE: Medical Consequences of Antibiotic Use in Agriculture Witte, W. Science, Vol. 279, Issue 5353 https://doi.org/10.1126/science.279.5353.996	journal	February 1998
Chemical transformation of xenobiotics by the human gut microbiota Koppel, Nitzan; Maini Rekdal, Vayu; Balskus, Emily P. Science, Vol. 356, Issue 6344 https://doi.org/10.1126/science.aag2770	journal	June 2017
Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania Smits, Samuel A.; Leach, Jeff; Sonnenburg, Erica D. Science, Vol. 357, Issue 6353 https://doi.org/10.1126/science.aan4834	journal	August 2017
The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice Turnbaugh, P. J.; Ridaura, V. K.; Faith, J. J. Science Translational Medicine, Vol. 1, Issue 6 https://doi.org/10.1126/scitranslmed.3000322	journal	November 2009
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Salyers, A. A.; Vercellotti, J. R.; West, S. E. Applied and Environmental Microbiology, Vol. 33, Issue 2 https://doi.org/10.1128/AEM.33.2.319-322.1977	journal	January 1977
Significance of Size and Nucleic Acid Content Heterogeneity as Measured by Flow Cytometry in Natural Planktonic Bacteria Gasol, Josep M.; Zweifel, Ulla Li; Peters, Francesc Applied and Environmental Microbiology, Vol. 65, Issue 10 https://doi.org/10.1128/AEM.65.10.4475-4483.1999	journal	October 1999
Does the High Nucleic Acid Content of Individual Bacterial Cells Allow Us To Discriminate between Active Cells and Inactive Cells in Aquatic Systems? Lebaron, Philippe; Servais, Pierre; Agogué, Helene Applied and Environmental Microbiology, Vol. 67, Issue 4 https://doi.org/10.1128/AEM.67.4.1775-1782.2001	journal	April 2001
Plant Products as Antimicrobial Agents Cowan, Marjorie Murphy Clinical Microbiology Reviews, Vol. 12, Issue 4 https://doi.org/10.1128/CMR.12.4.564	journal	October 1999
Antimicrobial Growth Promoters Used in Animal Feed: Effects of Less Well Known Antibiotics on Gram-Positive Bacteria Butaye, Patrick; Devriese, Luc A.; Haesebrouck, Freddy Clinical Microbiology Reviews, Vol. 16, Issue 2 https://doi.org/10.1128/CMR.16.2.175-188.2003	journal	April 2003
Food Starch Structure Impacts Gut Microbiome Composition Warren, Frederick J.; Fukuma, Naoki M.; Mikkelsen, Deirdre mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/mSphere.00086-18	journal	May 2018
RNA-Seq methods for imperfect samples: development, evaluation and applications Adiconis, Xian; Fan, Lin; DeLuca, David Genome Biology, Vol. 12, Issue S1 https://doi.org/10.1186/1465-6906-12-S1-P1	journal	September 2011
Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis Cui, Peng; Zhang, Shoudong; Ding, Feng Genome Biology, Vol. 15, Issue 1 https://doi.org/10.1186/gb-2014-15-1-r1	journal	January 2014
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
Impaired glucose metabolism and altered gut microbiome despite calorie restriction of ob/ob mice Kashani, Alireza; Brejnrod, Asker Daniel; Jin, Chunyu Animal Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/s42523-019-0007-1	journal	September 2019
Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts Martens, Eric C.; Lowe, Elisabeth C.; Chiang, Herbert PLoS Biology, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pbio.1001221	journal	December 2011
lmerTest Package: Tests in Linear Mixed Effects Models Kuznetsova, Alexandra; Brockhoff, Per B.; Christensen, Rune H. B. Journal of Statistical Software, Vol. 82, Issue 13 https://doi.org/10.18637/jss.v082.i13	journal	January 2017
Comparison of Sequencing Utility Programs Aronesty, Erik The Open Bioinformatics Journal, Vol. 7, Issue 1 https://doi.org/10.2174/1875036201307010001	journal	January 2013
Microbiome Datasets Are Compositional: And This Is Not Optional Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02224	journal	November 2017
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Oxford University Press https://doi.org/10.5167/uzh-155268	text	January 2015
A phylogenetic transform enhances analysis of compositional microbiota data Silverman, Justin D.; Washburne, Alex D.; Mukherjee, Sayan eLife, Vol. 6 https://doi.org/10.7554/eLife.21887	journal	February 2017

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