Phylogeny-corrected identification of microbial gene families relevant to human gut colonization
Abstract
The mechanisms by which different microbes colonize the healthy human gut versus other body sites, the gut in disease states, or other environments remain largely unknown. Identifying microbial genes influencing fitness in the gut could lead to new ways to engineer probiotics or disrupt pathogenesis. We approach this problem by measuring the statistical association between a species having a gene and the probability that the species is present in the gut microbiome. The challenge is that closely related species tend to be jointly present or absent in the microbiome and also share many genes, only a subset of which are involved in gut adaptation. We show that this phylogenetic correlation indeed leads to many false discoveries and propose phylogenetic linear regression as a powerful solution. To apply this method across the bacterial tree of life, where most species have not been experimentally phenotyped, we use metagenomes from hundreds of people to quantify each species’ prevalence in and specificity for the gut microbiome. This analysis reveals thousands of genes potentially involved in adaptation to the gut across species, including many novel candidates as well as processes known to contribute to fitness of gut bacteria, such as acid tolerance in Bacteroidetes andmore »
- Authors:
-
[1];
- Gladstone Inst. of Data Science and Biotechnology, San Francisco, CA (United States)
- Gladstone Inst. of Data Science and Biotechnology, San Francisco, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Institute and Environmental Genomics and Systems Biology Division
- Gladstone Inst. of Data Science and Biotechnology, San Francisco, CA (United States); Univ. of California, San Francisco, CA (United States). Quantitative Biology Inst. and Inst. for Computational Health Sciences. Inst. for Human Genetics. Dept. of Epidemiology and Biostatistics; Chan-Zuckerberg Biohub, San Francisco, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1627256
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Computational Biology (Online)
- Additional Journal Information:
- Journal Name: PLoS Computational Biology (Online); Journal Volume: 14; Journal Issue: 8; Journal ID: ISSN 1553-7358
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Mathematical & Computational Biology
Citation Formats
Bradley, Patrick H., Nayfach, Stephen, and Pollard, Katherine S. Phylogeny-corrected identification of microbial gene families relevant to human gut colonization. United States: N. p., 2018.
Web. doi:10.1371/journal.pcbi.1006242.
Bradley, Patrick H., Nayfach, Stephen, & Pollard, Katherine S. Phylogeny-corrected identification of microbial gene families relevant to human gut colonization. United States. https://doi.org/10.1371/journal.pcbi.1006242
Bradley, Patrick H., Nayfach, Stephen, and Pollard, Katherine S. Thu .
"Phylogeny-corrected identification of microbial gene families relevant to human gut colonization". United States. https://doi.org/10.1371/journal.pcbi.1006242. https://www.osti.gov/servlets/purl/1627256.
@article{osti_1627256,
title = {Phylogeny-corrected identification of microbial gene families relevant to human gut colonization},
author = {Bradley, Patrick H. and Nayfach, Stephen and Pollard, Katherine S.},
abstractNote = {The mechanisms by which different microbes colonize the healthy human gut versus other body sites, the gut in disease states, or other environments remain largely unknown. Identifying microbial genes influencing fitness in the gut could lead to new ways to engineer probiotics or disrupt pathogenesis. We approach this problem by measuring the statistical association between a species having a gene and the probability that the species is present in the gut microbiome. The challenge is that closely related species tend to be jointly present or absent in the microbiome and also share many genes, only a subset of which are involved in gut adaptation. We show that this phylogenetic correlation indeed leads to many false discoveries and propose phylogenetic linear regression as a powerful solution. To apply this method across the bacterial tree of life, where most species have not been experimentally phenotyped, we use metagenomes from hundreds of people to quantify each species’ prevalence in and specificity for the gut microbiome. This analysis reveals thousands of genes potentially involved in adaptation to the gut across species, including many novel candidates as well as processes known to contribute to fitness of gut bacteria, such as acid tolerance in Bacteroidetes and sporulation in Firmicutes. We also find microbial genes associated with a preference for the gut over other body sites, which are significantly enriched for genes linked to fitness in an in vivo competition experiment. Finally, we identify gene families associated with higher prevalence in patients with Crohn’s disease, including Proteobacterial genes involved in conjugation and fimbria regulation, processes previously linked to inflammation. These gene targets may represent new avenues for modulating host colonization and disease. Our strategy of combining metagenomics with phylogenetic modeling is general and can be used to identify genes associated with adaptation to any environment.},
doi = {10.1371/journal.pcbi.1006242},
journal = {PLoS Computational Biology (Online)},
number = 8,
volume = 14,
place = {United States},
year = {Thu Aug 09 00:00:00 EDT 2018},
month = {Thu Aug 09 00:00:00 EDT 2018}
}
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Fig 1: Failing to account for tree structure results in an elevated false positive rate. Continuous phenotypes and binary genotypes were simulated across the trees for the four phyla under consideration. A-D show results for the null of no true phenotype-genotype correlation. A-B) Histogram of $p$-values for simulated phenotypes andmore »
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Works referenced in this record:
Interaction of gut microbiota with bile acid metabolism and its influence on disease states
journal, November 2016
- Staley, Christopher; Weingarden, Alexa R.; Khoruts, Alexander
- Applied Microbiology and Biotechnology, Vol. 101, Issue 1
A microbial symbiosis factor prevents intestinal inflammatory disease
journal, May 2008
- Mazmanian, Sarkis K.; Round, June L.; Kasper, Dennis L.
- Nature, Vol. 453, Issue 7195
Bacteroides reticulotermitis sp. nov., isolated from the gut of a subterranean termite (Reticulitermes speratus)
journal, April 2012
- Sakamoto, M.; Ohkuma, M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2
Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009
- Richter, Michael; Rosselló-Móra, Ramon
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
The European Nucleotide Archive
journal, October 2010
- Leinonen, R.; Akhtar, R.; Birney, E.
- Nucleic Acids Research, Vol. 39, Issue Database
High-throughput ANI Analysis of 90K Prokaryotic Genomes Reveals Clear Species Boundaries
posted_content, October 2017
- Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M.
Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers
journal, July 2009
- Peng, Luying; Li, Zhong-Rong; Green, Robert S.
- The Journal of Nutrition, Vol. 139, Issue 9
Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation
journal, May 2016
- Browne, Hilary P.; Forster, Samuel C.; Anonye, Blessing O.
- Nature, Vol. 533, Issue 7604
Metagenome-wide association studies: fine-mining the microbiome
journal, July 2016
- Wang, Jun; Jia, Huijue
- Nature Reviews Microbiology, Vol. 14, Issue 8
Fusobacterium nucleatum Potentiates Intestinal Tumorigenesis and Modulates the Tumor-Immune Microenvironment
journal, August 2013
- Kostic, Aleksandar D.; Chun, Eunyoung; Robertson, Lauren
- Cell Host & Microbe, Vol. 14, Issue 2
LsrF, a coenzyme A-dependent thiolase, catalyzes the terminal step in processing the quorum sensing signal autoinducer-2
journal, September 2014
- Marques, João C.; Oh, Il Kyu; Ly, Daniel C.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 39
Transient Inability to Manage Proteobacteria Promotes Chronic Gut Inflammation in TLR5-Deficient Mice
journal, August 2012
- Carvalho, Frederic A.; Koren, Omry; Goodrich, Julia K.
- Cell Host & Microbe, Vol. 12, Issue 2
Glutamate decarboxylase-dependent acid resistance in orally acquired bacteria: function, distribution and biomedical implications of the gadBC operon: Role of gadBC operon in orally acquired bacteria
journal, September 2012
- De Biase, Daniela; Pennacchietti, Eugenia
- Molecular Microbiology, Vol. 86, Issue 4
Functional Genomics Approach to the Identification of Virulence Genes Involved in Edwardsiella tarda Pathogenesis
journal, March 2003
- Srinivasa Rao, Putanae S.; Lim, Tit Meng; Leung, Ka Yin
- Infection and Immunity, Vol. 71, Issue 3
Carnitine in bacterial physiology and metabolism
journal, June 2015
- Wargo, Matthew J.; Meadows, Jamie A.
- Microbiology, Vol. 161, Issue 6
Changes in microbial ecology after fecal microbiota transplantation for recurrent C. difficile infection affected by underlying inflammatory bowel disease
journal, May 2017
- Khanna, Sahil; Vazquez-Baeza, Yoshiki; González, Antonio
- Microbiome, Vol. 5, Issue 1
Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis
journal, January 2014
- Fernandes, Andrew D.; Reid, Jennifer NS; Macklaim, Jean M.
- Microbiome, Vol. 2, Issue 1
Innate and Adaptive Immunity Cooperate Flexibly to Maintain Host-Microbiota Mutualism
journal, July 2009
- Slack, E.; Hapfelmeier, S.; Stecher, B.
- Science, Vol. 325, Issue 5940
Enterobacteriaceae Act in Concert with the Gut Microbiota to Induce Spontaneous and Maternally Transmitted Colitis
journal, September 2010
- Garrett, Wendy S.; Gallini, Carey A.; Yatsunenko, Tanya
- Cell Host & Microbe, Vol. 8, Issue 3
fitdistrplus : An R Package for Fitting Distributions
journal, January 2015
- Delignette-Muller, Marie Laure; Dutang, Christophe
- Journal of Statistical Software, Vol. 64, Issue 4
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011
- Revell, Liam J.
- Methods in Ecology and Evolution, Vol. 3, Issue 2
Correlation detection strategies in microbial data sets vary widely in sensitivity and precision
journal, February 2016
- Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine
- The ISME Journal, Vol. 10, Issue 7
MCMCpack : Markov Chain Monte Carlo in R
journal, January 2011
- Martin, Andrew D.; Quinn, Kevin M.; Park, Jong Hee
- Journal of Statistical Software, Vol. 42, Issue 9
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
journal, September 2005
- Subramanian, A.; Tamayo, P.; Mootha, V. K.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550
Assessment and Selection of Competing Models for Zero-Inflated Microbiome Data
journal, July 2015
- Xu, Lizhen; Paterson, Andrew D.; Turpin, Williams
- PLOS ONE, Vol. 10, Issue 7
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile
journal, January 2013
- van Nood, Els; Vrieze, Anne; Nieuwdorp, Max
- New England Journal of Medicine, Vol. 368, Issue 5
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid
journal, April 2001
- Cotter, Paul D.; Gahan, Cormac G. M.; Hill, Colin
- Molecular Microbiology, Vol. 40, Issue 2
Manipulation of the Quorum Sensing Signal AI-2 Affects the Antibiotic-Treated Gut Microbiota
journal, March 2015
- Thompson, Jessica Ann; Oliveira, Rita Almeida; Djukovic, Ana
- Cell Reports, Vol. 10, Issue 11
Immunization with a heat-killed preparation of the environmental bacterium Mycobacterium vaccae promotes stress resilience in mice
journal, May 2016
- Reber, Stefan O.; Siebler, Philip H.; Donner, Nina C.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 22
Past and future species definitions for Bacteria and Archaea
journal, June 2015
- Rosselló-Móra, Ramon; Amann, Rudolf
- Systematic and Applied Microbiology, Vol. 38, Issue 4
GEIGER: investigating evolutionary radiations
journal, November 2007
- Harmon, L. J.; Weir, J. T.; Brock, C. D.
- Bioinformatics, Vol. 24, Issue 1
A general framework for association analysis of microbial communities on a taxonomic tree
journal, December 2016
- Tang, Zheng-Zheng; Chen, Guanhua; Alekseyenko, Alexander V.
- Bioinformatics
Generalized linear mixed models for phylogenetic analyses of community structure
journal, August 2011
- Ives, Anthony R.; Helmus, Matthew R.
- Ecological Monographs, Vol. 81, Issue 3
Genomic features of bacterial adaptation to
plants
journal, December 2017
- Levy, Asaf; Salas Gonzalez, Isai; Mittelviefhaus, Maximilian
- Nature Genetics, Vol. 50, Issue 1
The Treatment-Naive Microbiome in New-Onset Crohn’s Disease
journal, March 2014
- Gevers, Dirk; Kugathasan, Subra; Denson, Lee A.
- Cell Host & Microbe, Vol. 15, Issue 3
Proteobacteria: microbial signature of dysbiosis in gut microbiota
journal, September 2015
- Shin, Na-Ri; Whon, Tae Woong; Bae, Jin-Woo
- Trends in Biotechnology, Vol. 33, Issue 9
An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography
journal, October 2016
- Nayfach, Stephen; Rodriguez-Mueller, Beltran; Garud, Nandita
- Genome Research, Vol. 26, Issue 11
Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species
journal, December 2010
- Atarashi, K.; Tanoue, T.; Shima, T.
- Science, Vol. 331, Issue 6015
A phylogenetic method to perform genome-wide association studies in microbes that accounts for population structure and recombination
journal, February 2018
- Collins, Caitlin; Didelot, Xavier
- PLOS Computational Biology, Vol. 14, Issue 2
A core gut microbiome in obese and lean twins
journal, November 2008
- Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya
- Nature, Vol. 457, Issue 7228
The convergence of carbohydrate active gene repertoires in human gut microbes
journal, September 2008
- Lozupone, C. A.; Hamady, M.; Cantarel, B. L.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 39
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis
journal, April 2015
- Yano, Jessica M.; Yu, Kristie; Donaldson, Gregory P.
- Cell, Vol. 161, Issue 2
Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides
journal, October 2015
- Wu, Meng; McNulty, Nathan P.; Rodionov, Dmitry A.
- Science, Vol. 350, Issue 6256
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
SRAdb: query and use public next-generation sequencing data from within R
journal, January 2013
- Zhu, Yuelin; Stephens, Robert M.; Meltzer, Paul S.
- BMC Bioinformatics, Vol. 14, Issue 1
The Human Intestinal Microbiome in Health and Disease
journal, December 2016
- Lynch, Susan V.; Pedersen, Oluf
- New England Journal of Medicine, Vol. 375, Issue 24
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes
journal, September 2005
- Overbeek, R.
- Nucleic Acids Research, Vol. 33, Issue 17
Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection
journal, March 2015
- Weingarden, Alexa; González, Antonio; Vázquez-Baeza, Yoshiki
- Microbiome, Vol. 3, Issue 1
Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation
journal, October 2011
- Zaneveld, Jesse R. R.; Parfrey, Laura Wegener; Van Treuren, Will
- Trends in Microbiology, Vol. 19, Issue 10
Methods for phylogenetic analysis of microbiome data
journal, May 2018
- Washburne, Alex D.; Morton, James T.; Sanders, Jon
- Nature Microbiology, Vol. 3, Issue 6
FIGfams: yet another set of protein families
journal, September 2009
- Meyer, Folker; Overbeek, Ross; Rodriguez, Alex
- Nucleic Acids Research, Vol. 37, Issue 20
A metagenome-wide association study of gut microbiota in type 2 diabetes
journal, September 2012
- Qin, Junjie; Li, Yingrui; Cai, Zhiming
- Nature, Vol. 490, Issue 7418
PATRIC, the bacterial bioinformatics database and analysis resource
journal, November 2013
- Wattam, Alice R.; Abraham, David; Dalay, Oral
- Nucleic Acids Research, Vol. 42, Issue D1
A phylogenetic transform enhances analysis of compositional microbiota data
journal, February 2017
- Silverman, Justin D.; Washburne, Alex D.; Mukherjee, Sayan
- eLife, Vol. 6
Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes
journal, July 2014
- Nielsen, H. Bjørn; Almeida, Mathieu; Juncker, Agnieszka Sierakowska
- Nature Biotechnology, Vol. 32, Issue 8
Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium
journal, July 2016
- Porter, Stephanie S.; Chang, Peter L.; Conow, Christopher A.
- The ISME Journal, Vol. 11, Issue 1
The Prevalence and Geographic Distribution of Crohn’s Disease and Ulcerative Colitis in the United States
journal, December 2007
- Kappelman, Michael D.; Rifas–Shiman, Sheryl L.; Kleinman, Ken
- Clinical Gastroenterology and Hepatology, Vol. 5, Issue 12
Genetic Co-Occurrence Network across Sequenced Microbes
journal, December 2011
- Kim, Pan-Jun; Price, Nathan D.
- PLoS Computational Biology, Vol. 7, Issue 12
AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition
journal, July 2013
- Chassaing, Benoit; Koren, Omry; Carvalho, Frederic A.
- Gut, Vol. 63, Issue 7
Microbiome Datasets Are Compositional: And This Is Not Optional
journal, November 2017
- Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera
- Frontiers in Microbiology, Vol. 8
Pairwise comparisons across species are problematic when analyzing functional genomic data
journal, January 2018
- Dunn, Casey W.; Zapata, Felipe; Munro, Catriona
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 3
Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease: Flagella and adherent-invasive E. coli
journal, April 2003
- Barnich, Nicolas; Boudeau, Jérôme; Claret, Laurent
- Molecular Microbiology, Vol. 48, Issue 3
Patterns of Gene Flow Define Species of Thermophilic Archaea
journal, February 2012
- Cadillo-Quiroz, Hinsby; Didelot, Xavier; Held, Nicole L.
- PLoS Biology, Vol. 10, Issue 2
The Statistical Analysis of Compositional Data
journal, January 1982
- Aitchison, J.
- Journal of the Royal Statistical Society: Series B (Methodological), Vol. 44, Issue 2
Phylogenetic Logistic Regression for Binary Dependent Variables
journal, November 2009
- Ives, Anthony R.; Garland, Theodore
- Systematic Biology, Vol. 59, Issue 1
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data
journal, September 2016
- Yu, Guangchuang; Smith, David K.; Zhu, Huachen
- Methods in Ecology and Evolution, Vol. 8, Issue 1
Persistent infection with Crohn’s disease-associated adherent-invasive Escherichia coli leads to chronic inflammation and intestinal fibrosis
journal, June 2013
- Small, Cherrie-Lee N.; Reid-Yu, Sarah A.; McPhee, Joseph B.
- Nature Communications, Vol. 4, Issue 1
A Linear-Time Algorithm for Gaussian and Non-Gaussian Trait Evolution Models
journal, February 2014
- Tung Ho, Lam si; Ané, Cécile
- Systematic Biology, Vol. 63, Issue 3
APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004
- Paradis, E.; Claude, J.; Strimmer, K.
- Bioinformatics, Vol. 20, Issue 2
The Phylogenetic Regression
journal, December 1989
- Grafen, A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 326, Issue 1233
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Genomic insights that advance the species definition for prokaryotes
journal, February 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
Gut metagenome in European women with normal, impaired and diabetic glucose control
journal, May 2013
- Karlsson, Fredrik H.; Tremaroli, Valentina; Nookaew, Intawat
- Nature, Vol. 498, Issue 7452
Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour
journal, June 2006
- Ord, Terry J.; Martins, Emília P.
- Animal Behaviour, Vol. 71, Issue 6
An integrated catalog of reference genes in the human gut microbiome
journal, July 2014
- Li, Junhua; Jia, Huijue; Cai, Xianghang
- Nature Biotechnology, Vol. 32, Issue 8
Clostridium difficile-associated enteric disease
journal, December 2002
- Bartlett, John G.
- Current Infectious Disease Reports, Vol. 4, Issue 6
Statistical significance for genomewide studies
journal, July 2003
- Storey, J. D.; Tibshirani, R.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445
Testing in Microbiome-Profiling Studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test
journal, May 2015
- Zhao, Ni; Chen, Jun; Carroll, Ian M.
- The American Journal of Human Genetics, Vol. 96, Issue 5
The nature of confounding in genome-wide association studies
journal, November 2012
- Vilhjálmsson, Bjarni J.; Nordborg, Magnus
- Nature Reviews Genetics, Vol. 14, Issue 1
No Vacancy: How Beneficial Microbes Cooperate with Immunity To Provide Colonization Resistance to Pathogens
journal, April 2015
- Sassone-Corsi, Martina; Raffatellu, Manuela
- The Journal of Immunology, Vol. 194, Issue 9
Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae
journal, January 2012
- Stecher, B.; Denzler, R.; Maier, L.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 4
Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis
journal, September 2015
- Yano, Jessica M.; Yu, Kristie; Donaldson, Gregory P.
- Cell, Vol. 163, Issue 1
5-HT containing enteroendocrine cells characterised by morphologies, patterns of hormone co-expression, and relationships with nerve fibres in the mouse gastrointestinal tract
journal, February 2021
- Koo, Ada; Fothergill, Linda J.; Kuramoto, Hirofumi
- Histochemistry and Cell Biology, Vol. 155, Issue 6
An integrative analysis of the age-associated multi-omic landscape across cancers
journal, April 2021
- Chatsirisupachai, Kasit; Lesluyes, Tom; Paraoan, Luminita
- Nature Communications, Vol. 12, Issue 1
Systems Analysis of Gut Microbiome Influence on Metabolic Disease in HIV-Positive and High-Risk Populations
journal, June 2021
- Armstrong, Abigail J. S.; Quinn, Kevin; Fouquier, Jennifer
- mSystems, Vol. 6, Issue 3
Molecular characterization of lumpy skin disease virus (LSDV) emerged in Bangladesh reveals unique genetic features compared to contemporary field strains
journal, January 2021
- Badhy, Shukes Chandra; Chowdhury, Mohammad Golam Azam; Settypalli, Tirumala Bharani Kumar
- BMC Veterinary Research, Vol. 17, Issue 1
Testing in Microbiome-Profiling Studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test
text, January 2015
- J., Zhou, Jin; Tamar, Ringel-Kulka,; P., Epstein, Michael
- The University of North Carolina at Chapel Hill University Libraries
Genomic features of bacterial adaptation to plants
text, January 2018
- Sarah, Lebeis,; Bryan, Rangel Alvarez,; Freddy, Monteiro,
- The University of North Carolina at Chapel Hill University Libraries
The Statistical Analysis of Compositional Data
journal, February 1988
- Piepel, Gregory F.
- Technometrics, Vol. 30, Issue 1
Functional Genomics Approach to the Identification of Virulence Genes Involved in Edwardsiella tarda Pathogenesis
journal, July 2003
- Srinivasa Rao, Putanae S.; Lim, Tit Meng; Leung, Ka Yin
- Infection and Immunity, Vol. 71, Issue 7
rentrez: An R package for the NCBI eUtils API
journal, January 2017
- Winter, David,J.
- The R Journal, Vol. 9, Issue 2
Additional file 4: Figure S3. of Changes in microbial ecology after fecal microbiota transplantation for recurrent C. difficile infection affected by underlying inflammatory bowel disease
image, January 2017
- Khanna, Sahil; Vazquez-Baeza, Yoshiki; González, Antonio
- Figshare
Genetic Co-Occurrence Network across Sequenced Microbes
text, January 2012
- Kim, Pan-Jun; Price, Nathan D.
- arXiv
Interaction of gut microbiota with bile acid metabolism and its influence on disease states
journal, November 2016
- Staley, Christopher; Weingarden, Alexa R.; Khoruts, Alexander
- Applied Microbiology and Biotechnology, Vol. 101, Issue 1
Clostridium difficile-associated enteric disease
journal, December 2002
- Bartlett, John G.
- Current Infectious Disease Reports, Vol. 4, Issue 6
Testing in Microbiome-Profiling Studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test
journal, May 2015
- Zhao, Ni; Chen, Jun; Carroll, Ian M.
- The American Journal of Human Genetics, Vol. 96, Issue 5
Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis
journal, September 2015
- Yano, Jessica M.; Yu, Kristie; Donaldson, Gregory P.
- Cell, Vol. 163, Issue 1
Manipulation of the Quorum Sensing Signal AI-2 Affects the Antibiotic-Treated Gut Microbiota
journal, March 2015
- Thompson, Jessica Ann; Oliveira, Rita Almeida; Djukovic, Ana
- Cell Reports, Vol. 10, Issue 11
The Prevalence and Geographic Distribution of Crohn’s Disease and Ulcerative Colitis in the United States
journal, December 2007
- Kappelman, Michael D.; Rifas–Shiman, Sheryl L.; Kleinman, Ken
- Clinical Gastroenterology and Hepatology, Vol. 5, Issue 12
Enterobacteriaceae Act in Concert with the Gut Microbiota to Induce Spontaneous and Maternally Transmitted Colitis
journal, September 2010
- Garrett, Wendy S.; Gallini, Carey A.; Yatsunenko, Tanya
- Cell Host & Microbe, Vol. 8, Issue 3
Transient Inability to Manage Proteobacteria Promotes Chronic Gut Inflammation in TLR5-Deficient Mice
journal, August 2012
- Carvalho, Frederic A.; Koren, Omry; Goodrich, Julia K.
- Cell Host & Microbe, Vol. 12, Issue 2
Fusobacterium nucleatum Potentiates Intestinal Tumorigenesis and Modulates the Tumor-Immune Microenvironment
journal, August 2013
- Kostic, Aleksandar D.; Chun, Eunyoung; Robertson, Lauren
- Cell Host & Microbe, Vol. 14, Issue 2
The Treatment-Naive Microbiome in New-Onset Crohn’s Disease
journal, March 2014
- Gevers, Dirk; Kugathasan, Subra; Denson, Lee A.
- Cell Host & Microbe, Vol. 15, Issue 3
Past and future species definitions for Bacteria and Archaea
journal, June 2015
- Rosselló-Móra, Ramon; Amann, Rudolf
- Systematic and Applied Microbiology, Vol. 38, Issue 4
Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation
journal, October 2011
- Zaneveld, Jesse R. R.; Parfrey, Laura Wegener; Van Treuren, Will
- Trends in Microbiology, Vol. 19, Issue 10
F factor conjugation is a true type IV secretion system
journal, July 2003
- Lawley, T. D.; Klimke, W. A.; Gubbins, M. J.
- FEMS Microbiology Letters, Vol. 224, Issue 1
Correlation detection strategies in microbial data sets vary widely in sensitivity and precision
journal, February 2016
- Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine
- The ISME Journal, Vol. 10, Issue 7
Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium
journal, July 2016
- Porter, Stephanie S.; Chang, Peter L.; Conow, Christopher A.
- The ISME Journal, Vol. 11, Issue 1
A microbial symbiosis factor prevents intestinal inflammatory disease
journal, May 2008
- Mazmanian, Sarkis K.; Round, June L.; Kasper, Dennis L.
- Nature, Vol. 453, Issue 7195
A core gut microbiome in obese and lean twins
journal, November 2008
- Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya
- Nature, Vol. 457, Issue 7228
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
A metagenome-wide association study of gut microbiota in type 2 diabetes
journal, September 2012
- Qin, Junjie; Li, Yingrui; Cai, Zhiming
- Nature, Vol. 490, Issue 7418
Gut metagenome in European women with normal, impaired and diabetic glucose control
journal, May 2013
- Karlsson, Fredrik H.; Tremaroli, Valentina; Nookaew, Intawat
- Nature, Vol. 498, Issue 7452
An integrated catalog of reference genes in the human gut microbiome
journal, July 2014
- Li, Junhua; Jia, Huijue; Cai, Xianghang
- Nature Biotechnology, Vol. 32, Issue 8
Persistent infection with Crohn’s disease-associated adherent-invasive Escherichia coli leads to chronic inflammation and intestinal fibrosis
journal, June 2013
- Small, Cherrie-Lee N.; Reid-Yu, Sarah A.; McPhee, Joseph B.
- Nature Communications, Vol. 4, Issue 1
The nature of confounding in genome-wide association studies
journal, November 2012
- Vilhjálmsson, Bjarni J.; Nordborg, Magnus
- Nature Reviews Genetics, Vol. 14, Issue 1
The role of phylogenetic relatedness on alien plant success depends on the stage of invasion
journal, August 2022
- Omer, Ali; Fristoe, Trevor; Yang, Qiang
- Nature Plants, Vol. 8, Issue 8
Methods for phylogenetic analysis of microbiome data
journal, May 2018
- Washburne, Alex D.; Morton, James T.; Sanders, Jon
- Nature Microbiology, Vol. 3, Issue 6
Mir34a constrains pancreatic carcinogenesis
journal, June 2020
- Hidalgo-Sastre, Ana; Lubeseder-Martellato, Clara; Engleitner, Thomas
- Scientific Reports, Vol. 10, Issue 1
A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid
journal, April 2001
- Cotter, Paul D.; Gahan, Cormac G. M.; Hill, Colin
- Molecular Microbiology, Vol. 40, Issue 2
Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease: Flagella and adherent-invasive E. coli
journal, April 2003
- Barnich, Nicolas; Boudeau, Jérôme; Claret, Laurent
- Molecular Microbiology, Vol. 48, Issue 3
Genomic insights that advance the species definition for prokaryotes
journal, February 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
The convergence of carbohydrate active gene repertoires in human gut microbes
journal, September 2008
- Lozupone, C. A.; Hamady, M.; Cantarel, B. L.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 39
Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae
journal, January 2012
- Stecher, B.; Denzler, R.; Maier, L.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 4
Statistical significance for genomewide studies
journal, July 2003
- Storey, J. D.; Tibshirani, R.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445
Immunization with a heat-killed preparation of the environmental bacterium Mycobacterium vaccae promotes stress resilience in mice
journal, May 2016
- Reber, Stefan O.; Siebler, Philip H.; Donner, Nina C.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 22
Pairwise comparisons across species are problematic when analyzing functional genomic data
journal, January 2018
- Dunn, Casey W.; Zapata, Felipe; Munro, Catriona
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 3
Phylogenies and the Comparative Method
journal, January 1985
- Felsenstein, Joseph
- The American Naturalist, Vol. 125, Issue 1
APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004
- Paradis, E.; Claude, J.; Strimmer, K.
- Bioinformatics, Vol. 20, Issue 2
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
A general framework for association analysis of microbial communities on a taxonomic tree
journal, December 2016
- Tang, Zheng-Zheng; Chen, Guanhua; Alekseyenko, Alexander V.
- Bioinformatics
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes
journal, September 2005
- Overbeek, R.
- Nucleic Acids Research, Vol. 33, Issue 17
FIGfams: yet another set of protein families
journal, September 2009
- Meyer, Folker; Overbeek, Ross; Rodriguez, Alex
- Nucleic Acids Research, Vol. 37, Issue 20
Phylogenetic Logistic Regression for Binary Dependent Variables
journal, November 2009
- Ives, Anthony R.; Garland, Theodore
- Systematic Biology, Vol. 59, Issue 1
The Phylogenetic Regression
journal, December 1989
- Grafen, A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 326, Issue 1233
Bacteroides reticulotermitis sp. nov., isolated from the gut of a subterranean termite (Reticulitermes speratus)
journal, April 2012
- Sakamoto, M.; Ohkuma, M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2
An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography
journal, October 2016
- Nayfach, Stephen; Rodriguez-Mueller, Beltran; Garud, Nandita
- Genome Research, Vol. 26, Issue 11
Glutamate decarboxylase-dependent acid resistance in orally acquired bacteria: function, distribution and biomedical implications of the gadBC operon: Role of gadBC operon in orally acquired bacteria
journal, September 2012
- De Biase, Daniela; Pennacchietti, Eugenia
- Molecular Microbiology, Vol. 86, Issue 4
Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species
journal, December 2010
- Atarashi, K.; Tanoue, T.; Shima, T.
- Science, Vol. 331, Issue 6015
Helicobacter hepaticus Triggers Colitis in Specific-Pathogen-Free Interleukin-10 (IL-10)-Deficient Mice through an IL-12- and Gamma Interferon-Dependent Mechanism
journal, November 1998
- Kullberg, Marika C.; Ward, Jerrold M.; Gorelick, Peter L.
- Infection and Immunity, Vol. 66, Issue 11
Adherent Invasive Escherichia coli Strains from Patients with Crohn's Disease Survive and Replicate within Macrophages without Inducing Host Cell Death
journal, September 2001
- Glasser, Anne-Lise; Boudeau, Jerome; Barnich, Nicolas
- Infection and Immunity, Vol. 69, Issue 9
Surviving Between Hosts: Sporulation and Transmission
journal, August 2016
- Swick, Michelle C.; Koehler, Theresa M.; Driks, Adam
- Microbiology Spectrum, Vol. 4, Issue 4
AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition
journal, July 2013
- Chassaing, Benoit; Koren, Omry; Carvalho, Frederic A.
- Gut, Vol. 63, Issue 7
SRAdb: query and use public next-generation sequencing data from within R
journal, January 2013
- Zhu, Yuelin; Stephens, Robert M.; Meltzer, Paul S.
- BMC Bioinformatics, Vol. 14, Issue 1
Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis
journal, January 2014
- Fernandes, Andrew D.; Reid, Jennifer NS; Macklaim, Jean M.
- Microbiome, Vol. 2, Issue 1
Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection
journal, March 2015
- Weingarden, Alexa; González, Antonio; Vázquez-Baeza, Yoshiki
- Microbiome, Vol. 3, Issue 1
Patterns of Gene Flow Define Species of Thermophilic Archaea
journal, February 2012
- Cadillo-Quiroz, Hinsby; Didelot, Xavier; Held, Nicole L.
- PLoS Biology, Vol. 10, Issue 2
Genetic Co-Occurrence Network across Sequenced Microbes
journal, December 2011
- Kim, Pan-Jun; Price, Nathan D.
- PLoS Computational Biology, Vol. 7, Issue 12
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
MCMCpack : Markov Chain Monte Carlo in R
journal, January 2011
- Martin, Andrew D.; Quinn, Kevin M.; Park, Jong Hee
- Journal of Statistical Software, Vol. 42, Issue 9
Generalized linear mixed models for phylogenetic analyses of community structure
journal, August 2011
- Ives, Anthony R.; Helmus, Matthew R.
- Ecological Monographs, Vol. 81, Issue 3
Microbiome Datasets Are Compositional: And This Is Not Optional
journal, November 2017
- Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera
- Frontiers in Microbiology, Vol. 8
Works referencing / citing this record:
New insights from uncultivated genomes of the global human gut microbiome
journal, March 2019
- Nayfach, Stephen; Shi, Zhou Jason; Seshadri, Rekha
- Nature, Vol. 568, Issue 7753
Evolutionary dynamics of bacteria in the gut microbiome within and across hosts
journal, January 2019
- Garud, Nandita R.; Good, Benjamin H.; Hallatschek, Oskar
- PLOS Biology, Vol. 17, Issue 1
Computational Structural Biology: Successes, Future Directions, and Challenges
journal, February 2019
- Nussinov, Ruth; Tsai, Chung-Jung; Shehu, Amarda
- Molecules, Vol. 24, Issue 3
Methods for phylogenetic analysis of microbiome data
journal, May 2018
- Washburne, Alex D.; Morton, James T.; Sanders, Jon
- Nature Microbiology, Vol. 3, Issue 6
phylogenize: correcting for phylogeny reveals genes associated with microbial distributions
journal, October 2019
- Bradley, Patrick H.; Pollard, Katherine S.
- Bioinformatics, Vol. 36, Issue 4
New insights from uncultivated genomes of the global human gut microbiome
journal, March 2019
- Nayfach, Stephen; Shi, Zhou Jason; Seshadri, Rekha
- Nature, Vol. 568, Issue 7753
The Glutaminase-Dependent Acid Resistance System: Qualitative and Quantitative Assays and Analysis of Its Distribution in Enteric Bacteria
journal, November 2018
- Pennacchietti, Eugenia; D'Alonzo, Chiara; Freddi, Luca
- Frontiers in Microbiology, Vol. 9
Computational Structural Biology: Successes, Future Directions, and Challenges
journal, February 2019
- Nussinov, Ruth; Tsai, Chung-Jung; Shehu, Amarda
- Molecules, Vol. 24, Issue 3
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