Host lifestyle affects human microbiota on daily timescales

BackgroundDisturbance to human microbiota may underlie several pathologies. Yet, we lack a comprehensive understanding of how lifestyle affects the dynamics of human-associated microbial communities.ResultsHere, we link over 10,000 longitudinal measurements of human wellness and action to the daily gut and salivary microbiota dynamics of two individuals over the course of one year. These time series show overall microbial communities to be stable for months. However, rare events in each subjects’ life rapidly and broadly impacted microbiota dynamics. Travel from the developed to the developing world in one subject led to a nearly two-fold increase in the Bacteroidetes to Firmicutes ratio, which reversed upon return. Enteric infection in the other subject resulted in the permanent decline of most gut bacterial taxa, which were replaced by genetically similar species. Still, even during periods of overall community stability, the dynamics of select microbial taxa could be associated with specific host behaviors. Most prominently, changes in host fiber intake positively correlated with next-day abundance changes among 15% of gut microbiota members.ConclusionsOur findings suggest that although human-associated microbial communities are generally stable, they can be quickly and profoundly altered by common human actions and experiences.

[1]  H. Harmsen,et al.  Cultured Representatives of Two Major Phylogroups of Human Colonic Faecalibacterium prausnitzii Can Utilize Pectin, Uronic Acids, and Host-Derived Substrates for Growth , 2011, Applied and Environmental Microbiology.

[2]  Adelchi Azzalini,et al.  The R Package bild for the Analysis of Binary Longitudinal Data , 2012 .

[3]  R. Baker Reassessment of Some Fruit and Vegetable Pectin Levels , 1997 .

[4]  R. Knight,et al.  The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice , 2009, Science Translational Medicine.

[5]  R. Knight,et al.  Moving pictures of the human microbiome , 2011, Genome Biology.

[6]  J. Clemente,et al.  Human gut microbiome viewed across age and geography , 2012, Nature.

[7]  S. Humphrey,et al.  A review of saliva: normal composition, flow, and function. , 2001, The Journal of prosthetic dentistry.

[8]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[9]  Rob J Hyndman,et al.  Automatic Time Series Forecasting: The forecast Package for R , 2008 .

[10]  Andrew P. Martin Phylogenetic Approaches for Describing and Comparing the Diversity of Microbial Communities , 2002, Applied and Environmental Microbiology.

[11]  Zaid Abdo,et al.  Temporal Dynamics of the Human Vaginal Microbiota , 2012, Science Translational Medicine.

[12]  Korbinian Strimmer,et al.  fdrtool: a versatile R package for estimating local and tail area-based false discovery rates , 2008, Bioinform..

[13]  H. Flint,et al.  Reduced Dietary Intake of Carbohydrates by Obese Subjects Results in Decreased Concentrations of Butyrate and Butyrate-Producing Bacteria in Feces , 2006, Applied and Environmental Microbiology.

[14]  J. Neu,et al.  Succession of microbial consortia in the developing infant gut microbiome , 2011 .

[15]  Ann V Rowlands,et al.  Saliva flow rate, total protein concentration and osmolality as potential markers of whole body hydration status during progressive acute dehydration in humans. , 2004, Archives of oral biology.

[16]  S. Massart,et al.  Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa , 2010, Proceedings of the National Academy of Sciences.

[17]  G. Dougan,et al.  Salmonella enterica Serovar Typhimurium Exploits Inflammation to Compete with the Intestinal Microbiota , 2007, PLoS biology.

[18]  D. Haydon,et al.  Alternative stable states in ecology , 2003 .

[19]  J. Parkhill,et al.  Dominant and diet-responsive groups of bacteria within the human colonic microbiota , 2011, The ISME Journal.

[20]  M Cardinal,et al.  On the application of integer-valued time series models for the analysis of disease incidence. , 1999, Statistics in medicine.

[21]  Jonathan A. Eisen,et al.  Human gut microbiome adopts an alternative state following small bowel transplantation , 2009, Proceedings of the National Academy of Sciences.

[22]  E. Mardis,et al.  An obesity-associated gut microbiome with increased capacity for energy harvest , 2006, Nature.

[23]  Otto X. Cordero,et al.  Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations , 2012, Proceedings of the National Academy of Sciences.

[24]  A. Viale,et al.  Profound Alterations of Intestinal Microbiota following a Single Dose of Clindamycin Results in Sustained Susceptibility to Clostridium difficile-Induced Colitis , 2011, Infection and Immunity.

[25]  Achim Zeileis,et al.  Diagnostic Checking in Regression Relationships , 2015 .

[26]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[27]  R. Knight,et al.  Bacterial Community Variation in Human Body Habitats Across Space and Time , 2009, Science.

[28]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[29]  D. Relman,et al.  The Application of Ecological Theory Toward an Understanding of the Human Microbiome , 2012, Science.

[30]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[31]  Y. Belkaid,et al.  Acute Gastrointestinal Infection Induces Long-Lived Microbiota-Specific T Cell Responses , 2012, Science.

[32]  P. A. Blight The Analysis of Time Series: An Introduction , 1991 .

[33]  Yunwei Wang,et al.  Dietary fat-induced taurocholic acid production promotes pathobiont and colitis in IL-10−/− mice , 2012, Nature.

[34]  B. Bohannan,et al.  Phylogenetic clustering and overdispersion in bacterial communities. , 2006, Ecology.

[35]  G R Gibson,et al.  Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. , 1995, Gastroenterology.

[36]  D. Dickey,et al.  Testing for unit roots in autoregressive-moving average models of unknown order , 1984 .

[37]  F. Bushman,et al.  Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes , 2011, Science.

[38]  P. Turnbaugh,et al.  Microbial ecology: Human gut microbes associated with obesity , 2006, Nature.

[39]  Jeffrey Heer,et al.  Sizing the horizon: the effects of chart size and layering on the graphical perception of time series visualizations , 2009, CHI.

[40]  D. Relman,et al.  Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation , 2010, Proceedings of the National Academy of Sciences.

[41]  R. Knight,et al.  PyCogent: a toolkit for making sense from sequence , 2007, Genome Biology.

[42]  J. Clemente,et al.  The Long-Term Stability of the Human Gut Microbiota , 2013 .

[43]  Lawrence A. David,et al.  Diet rapidly and reproducibly alters the human gut microbiome , 2013, Nature.

[44]  Skipper Seabold,et al.  Statsmodels: Econometric and Statistical Modeling with Python , 2010, SciPy.

[45]  J. Doré,et al.  Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients , 2008, Proceedings of the National Academy of Sciences.

[46]  A. Biesbrock,et al.  Treatment outcomes of dental flossing in twins: molecular analysis of the interproximal microflora. , 2008, Journal of periodontology.

[47]  Les Dethlefsen,et al.  The Pervasive Effects of an Antibiotic on the Human Gut Microbiota, as Revealed by Deep 16S rRNA Sequencing , 2008, PLoS biology.

[48]  E. Zoetendal,et al.  Temperature Gradient Gel Electrophoresis Analysis of 16S rRNA from Human Fecal Samples Reveals Stable and Host-Specific Communities of Active Bacteria , 1998, Applied and Environmental Microbiology.

[49]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[50]  Jonathan Friedman,et al.  Inferring Correlation Networks from Genomic Survey Data , 2012, PLoS Comput. Biol..

[51]  43 Dietary Fat-Induced Taurocholic Acid Production Promotes Pathobiont and Colitis in IL-10-/- Mice , 2012 .

[52]  C. Granger,et al.  Spurious regressions in econometrics , 1974 .

[53]  John Aitchison,et al.  The Statistical Analysis of Compositional Data , 1986 .

[54]  Anders F. Andersson,et al.  Short-Term Antibiotic Treatment Has Differing Long-Term Impacts on the Human Throat and Gut Microbiome , 2010, PloS one.

[55]  M. Blaser,et al.  Antibiotics in early life alter the murine colonic microbiome and adiposity , 2012, Nature.