Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics

Lee, Sonny T. M.; Kahn, Stacy A.; Delmont, Tom O.; Shaiber, Alon; Esen, Ozcan C.; Hubert, Nathaniel A.; Morrison, Hilary G.; Antonopoulos, Dionysios A.; Rubin, David T.; Eren, A. Murat

doi:10.1186/s40168-017-0270-x

Title: Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics

Journal Article · Thu May 04 00:00:00 EDT 2017 · Microbiome

DOI:https://doi.org/10.1186/s40168-017-0270-x· OSTI ID:1415981

Lee, Sonny T. M. ^[1]; Kahn, Stacy A. ^[2]; Delmont, Tom O. ^[1]; Shaiber, Alon ^[1]; Esen, Ozcan C. ^[1]; Hubert, Nathaniel A. ^[1]; Morrison, Hilary G. ^[3]; Antonopoulos, Dionysios A. ^[1]; Rubin, David T. ^[1]; Eren, A. Murat ^[4]

Univ. of Chicago Medicine, Chicago, IL (United States)
Univ. of Chicago Medicine, Chicago, IL (United States); Boston Children's Hospital, Boston, MA (United States)
Marine Biological Lab., Woods Hole, MA (United States)
Univ. of Chicago Medicine, Chicago, IL (United States); Marine Biological Lab., Woods Hole, MA (United States)

Fecal microbiota transplantation (FMT) is an effective treatment for recurrent Clostridium difficile infection and shows promise for treating other medical conditions associated with intestinal dysbioses. However, we lack a sufficient understanding of which microbial populations successfully colonize the recipient gut, and the widely used approaches to study the microbial ecology of FMT experiments fail to provide enough resolution to identify populations that are likely responsible for FMT-derived benefits. Here, we used shotgun metagenomics together with assembly and binning strategies to reconstruct metagenome-assembled genomes (MAGs) from fecal samples of a single FMT donor. We then used metagenomic mapping to track the occurrence and distribution patterns of donor MAGs in two FMT recipients. Our analyses revealed that 22% of the 92 highly complete bacterial MAGs that we identified from the donor successfully colonized and remained abundant in two recipients for at least 8 weeks. Most MAGs with a high colonization rate belonged to the order Bacteroidales. The vast majority of those that lacked evidence of colonization belonged to the order Clostridiales, and colonization success was negatively correlated with the number of genes related to sporulation. Our analysis of 151 publicly available gut metagenomes showed that the donor MAGs that colonized both recipients were prevalent, and the ones that colonized neither were rare across the participants of the Human Microbiome Project. Although our dataset showed a link between taxonomy and the colonization ability of a given MAG, we also identified MAGs that belong to the same taxon with different colonization properties, highlighting the importance of an appropriate level of resolution to explore the functional basis of colonization and to identify targets for cultivation, hypothesis generation, and testing in model systems. Lastly, the analytical strategy adopted in our study can provide genomic insights into bacterial populations that may be critical to the efficacy of FMT due to their success in gut colonization and metabolic properties, and guide cultivation efforts to investigate mechanistic underpinnings of this procedure beyond associations.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: Gastro-Intestinal Research Foundation (GIRF); University of Chicago; USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1415981

Journal Information:: Microbiome, Vol. 5, Issue 1; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 59 works

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References (68)

Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
Temporal and technical variability of human gut metagenomes Voigt, Anita Y.; Costea, Paul I.; Kultima, Jens Roat Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0639-8	journal	April 2015
Long-Term Follow-Up of Colonoscopic Fecal Microbiota Transplant for Recurrent Clostridium difficile Infection Brandt, Lawrence J.; Aroniadis, Olga C.; Mellow, Mark American Journal of Gastroenterology, Vol. 107, Issue 7 https://doi.org/10.1038/ajg.2012.60	journal	January 2012
Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and Genome Analyzer systems Minoche, André E.; Dohm, Juliane C.; Himmelbauer, Heinz Genome Biology, Vol. 12, Issue 11 https://doi.org/10.1186/gb-2011-12-11-r112	journal	January 2011
Systematic Review of Intestinal Microbiota Transplantation (Fecal Bacteriotherapy) for Recurrent Clostridium difficile Infection Gough, Ethan; Shaikh, Henna; Manges, Amee R. Clinical Infectious Diseases, Vol. 53, Issue 10 https://doi.org/10.1093/cid/cir632	journal	November 2011
Fecal Transplants: What Is Being Transferred? Bojanova, Diana P.; Bordenstein, Seth R. PLOS Biology, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pbio.1002503	journal	July 2016
Review article: faecal transplantation therapy for gastrointestinal disease: Review: faecal transplantation Landy, J.; Al-Hassi, H. O.; McLaughlin, S. D. Alimentary Pharmacology & Therapeutics, Vol. 34, Issue 4 https://doi.org/10.1111/j.1365-2036.2011.04737.x	journal	June 2011
High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria Hamilton, Matthew J.; Weingarden, Alexa R.; Unno, Tatsuya Gut Microbes, Vol. 4, Issue 2 https://doi.org/10.4161/gmic.23571	journal	January 2013
Safety, Tolerability, and Clinical Response After Fecal Transplantation in Children and Young Adults With Ulcerative Colitis Kunde, Sachin; Pham, Angela; Bonczyk, Sarah Journal of Pediatric Gastroenterology and Nutrition, Vol. 56, Issue 6 https://doi.org/10.1097/MPG.0b013e318292fa0d	journal	January 2013
Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host Xi, Zhiyong; Gavotte, Laurent; Xie, Yan BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-1	journal	January 2008
Fecal Microbiota Transplantation Induces Remission in Patients With Active Ulcerative Colitis in a Randomized Controlled Trial Moayyedi, Paul; Surette, Michael G.; Kim, Peter T. Gastroenterology, Vol. 149, Issue 1 https://doi.org/10.1053/j.gastro.2015.04.001	journal	July 2015
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
Centrifuge: rapid and sensitive classification of metagenomic sequences Kim, Daehwan; Song, Li; Breitwieser, Florian P. Genome Research, Vol. 26, Issue 12 https://doi.org/10.1101/gr.210641.116	journal	October 2016
Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile van Nood, Els; Vrieze, Anne; Nieuwdorp, Max New England Journal of Medicine, Vol. 368, Issue 5 https://doi.org/10.1056/NEJMoa1205037	journal	January 2013
Clostridium difficile infection: new developments in epidemiology and pathogenesis Rupnik, Maja; Wilcox, Mark H.; Gerding, Dale N. Nature Reviews Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/nrmicro2164	journal	July 2009
Fecal Microbiota Transplantation Inducing Remission in Crohn’s Colitis and the Associated Changes in Fecal Microbial Profile Kao, Dina; Hotte, Naomi; Gillevet, Patrick Journal of Clinical Gastroenterology, Vol. 48, Issue 7 https://doi.org/10.1097/MCG.0000000000000131	journal	January 2014
Durable coexistence of donor and recipient strains after fecal microbiota transplantation Li, Simone S.; Zhu, Ana; Benes, Vladimir Science, Vol. 352, Issue 6285 https://doi.org/10.1126/science.aad8852	journal	April 2016
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Temporal Bacterial Community Dynamics Vary Among Ulcerative Colitis Patients After Fecal Microbiota Transplantation Angelberger, Sieglinde; Reinisch, Walter; Makristathis, Athanasios American Journal of Gastroenterology, Vol. 108, Issue 10 https://doi.org/10.1038/ajg.2013.257	journal	January 2013
An Overview of Ensembl Birney, E. Genome Research, Vol. 14, Issue 5 https://doi.org/10.1101/gr.1860604	journal	May 2004
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Gastrointestinal Microflora Studies in Late‐Onset Autism Finegold, Sydney M.; Molitoris, Denise; Song, Yuli Clinical Infectious Diseases, Vol. 35, Issue s1 https://doi.org/10.1086/341914	journal	September 2002
An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography Nayfach, Stephen; Rodriguez-Mueller, Beltran; Garud, Nandita Genome Research, Vol. 26, Issue 11 https://doi.org/10.1101/gr.201863.115	journal	October 2016
Relationship Between Thyroid Autoimmunity and Yersinia Enterocolitica Antibodies Çorapçioğlu, Demet; Tonyukuk, Vedia; Kiyan, Mehmet Thyroid, Vol. 12, Issue 7 https://doi.org/10.1089/105072502320288483	journal	July 2002
Transfusion-transmitted infections Bihl, Florian; Castelli, Damiano; Marincola, Francesco Journal of Translational Medicine, Vol. 5, Issue 1 https://doi.org/10.1186/1479-5876-5-25	journal	June 2007
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
A core gut microbiome in obese and lean twins Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya Nature, Vol. 457, Issue 7228 https://doi.org/10.1038/nature07540	journal	November 2008
Colonization potential to reconstitute a microbe community in patients detected early after fecal microbe transplant for recurrent C. difficile Kumar, Ranjit; Maynard, Craig L.; Eipers, Peter BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-015-0622-2	journal	January 2016
Fecal Microbiota Transplantation — An Old Therapy Comes of Age Kelly, Ciarán P. New England Journal of Medicine, Vol. 368, Issue 5 https://doi.org/10.1056/NEJMe1214816	journal	January 2013
Seres's pioneering microbiome drug fails mid-stage trial Ratner, Mark Nature Biotechnology, Vol. 34, Issue 10 https://doi.org/10.1038/nbt1016-1004b	journal	October 2016
A patient with severe Crohn's colitis responds to Faecal Microbiota Transplantation Gordon, Hannah; Harbord, Marcus Journal of Crohn's and Colitis, Vol. 8, Issue 3 https://doi.org/10.1016/j.crohns.2013.10.007	journal	March 2014
Recovery of the Gut Microbiome following Fecal Microbiota Transplantation Seekatz, Anna M.; Aas, Johannes; Gessert, Charles E. mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mBio.00893-14	journal	June 2014
Fecal Microbiota Transplantation for Clostridium difficile Infection: Systematic Review and Meta-Analysis Kassam, Zain; Lee, Christine H.; Yuan, Yuhong American Journal of Gastroenterology, Vol. 108, Issue 4 https://doi.org/10.1038/ajg.2013.59	journal	January 2013
Reset of a critically disturbed microbial ecosystem: faecal transplant in recurrent Clostridium difficile infection Fuentes, Susana; van Nood, Els; Tims, Sebastian The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.13	journal	February 2014
Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease Anderson, J. L.; Edney, R. J.; Whelan, K. Alimentary Pharmacology & Therapeutics, Vol. 36, Issue 6 https://doi.org/10.1111/j.1365-2036.2012.05220.x	journal	July 2012
Transfusion Reactions Due to Bacterial Contamination of Blood and Blood Products Morduchowicz, Gabriel; Pitlik, Silvio D.; Huminer, David Clinical Infectious Diseases, Vol. 13, Issue 2 https://doi.org/10.1093/clinids/13.2.307	journal	March 1991
Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection Weingarden, Alexa; González, Antonio; Vázquez-Baeza, Yoshiki Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0070-0	journal	March 2015
Systematic Review: Adverse Events of Fecal Microbiota Transplantation Wang, Sinan; Xu, Mengque; Wang, Weiqiang PLOS ONE, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pone.0161174	journal	August 2016
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Environmental Genome Shotgun Sequencing of the Sargasso Sea Venter, J. C. Science, Vol. 304, Issue 5667 https://doi.org/10.1126/science.1093857	journal	April 2004
MetaPhlAn2 for enhanced metagenomic taxonomic profiling Truong, Duy Tin; Franzosa, Eric A.; Tickle, Timothy L. Nature Methods, Vol. 12, Issue 10 https://doi.org/10.1038/nmeth.3589	journal	September 2015
Patient-Specific Bacteroides Genome Variants in Pouchitis Vineis, Joseph H.; Ringus, Daina L.; Morrison, Hilary G. mBio, Vol. 7, Issue 6 https://doi.org/10.1128/mBio.01713-16	journal	November 2016
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Machine Learning Meta-analysis of Large Metagenomic Datasets: Tools and Biological Insights Pasolli, Edoardo; Truong, Duy Tin; Malik, Faizan PLOS Computational Biology, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pcbi.1004977	journal	July 2016
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
A Novel Microbiome Therapeutic Increases Gut Microbial Diversity and Prevents Recurrent Clostridium difficile Infection Khanna, Sahil; Pardi, Darrell S.; Kelly, Colleen R. Journal of Infectious Diseases, Vol. 214, Issue 2 https://doi.org/10.1093/infdis/jiv766	journal	February 2016
Should We Standardize the 1,700-Year-Old Fecal Microbiota Transplantation? Zhang, Faming; Luo, Wensheng; Shi, Yan American Journal of Gastroenterology, Vol. 107, Issue 11 https://doi.org/10.1038/ajg.2012.251	journal	January 2012
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
16S rRNA Gene Sequencing for Bacterial Identification in the Diagnostic Laboratory: Pluses, Perils, and Pitfalls Janda, J. M.; Abbott, S. L. Journal of Clinical Microbiology, Vol. 45, Issue 9 https://doi.org/10.1128/JCM.01228-07	journal	July 2007
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
A Filtering Method to Generate High Quality Short Reads Using Illumina Paired-End Technology Eren, A. Murat; Vineis, Joseph H.; Morrison, Hilary G. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066643	journal	June 2013
Identifying biologically relevant differences between metagenomic communities Parks, Donovan H.; Beiko, Robert G. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq041	journal	February 2010
Bowel‐flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Borody, T. J.; George, L.; Andrews, P. Medical Journal of Australia, Vol. 150, Issue 10 https://doi.org/10.5694/j.1326-5377.1989.tb136704.x	journal	May 1989
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric figshare https://doi.org/10.6084/m9.figshare.706369.v1	dataset	January 2013
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric Figshare https://doi.org/10.6084/m9.figshare.706369	dataset	January 2013
MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang arXiv https://doi.org/10.48550/arxiv.1409.7208	preprint	January 2014
Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment Kim, Minji; Lee, Ki-Eun; Cha, In-Tae Current Microbiology, Vol. 78, Issue 8 https://doi.org/10.1007/s00284-021-02576-9	journal	June 2021
Fecal Microbiota Transplantation for Clostridioides difficile in High-Risk Older Adults: Treat Early, Treat Often Agrawal, Gaurav Digestive Diseases and Sciences, Vol. 65, Issue 12 https://doi.org/10.1007/s10620-020-06291-6	journal	April 2020
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
Is Crohn’s Disease Ready for Fecal Microbiota Transplantation? Borody, Thomas J.; Finlayson, Sarah; Paramsothy, Sudarshan Journal of Clinical Gastroenterology, Vol. 48, Issue 7 https://doi.org/10.1097/mcg.0000000000000155	journal	August 2014
Fecal Flora Reconstitution for Recurrent Clostridium difficile Infection: Results and Methodology Rohlke, Faith; Surawicz, Christina M.; Stollman, Neil Journal of Clinical Gastroenterology, Vol. 44, Issue 8 https://doi.org/10.1097/mcg.0b013e3181dadb10	journal	January 2010
Medical Stool Davidovics, Zev H.; Sylvester, Francisco A. Journal of Pediatric Gastroenterology & Nutrition, Vol. 56, Issue 6 https://doi.org/10.1097/mpg.0b013e318295cc5a	journal	June 2013
Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation Chehoud, Christel; Dryga, Anatoly; Hwang, Young mBio, Vol. 7, Issue 2 https://doi.org/10.1128/mbio.00322-16	journal	March 2016
Fecal microbiota transplantation in relapsing Clostridium difficile infection Rohlke, Faith; Stollman, Neil Therapeutic Advances in Gastroenterology, Vol. 5, Issue 6 https://doi.org/10.1177/1756283x12453637	journal	July 2012
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008

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60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
colonization
fecal microbiota transplantation
metagenome-assembled genomes
metagenomics

Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019 The current record is supplemented by this dataset	dataset	May 2017
Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019.v1 The current record is supplemented by this other	other	May 2017
Additional file 1: Table S3. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d1 The current record is supplemented by this dataset	dataset	May 2017
Additional file 1: Table S3. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d1.v1 The current record is supplemented by this dataset	dataset	May 2017
Additional file 2: Table S1. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d2 The current record is supplemented by this dataset	dataset	May 2017
Additional file 2: Table S1. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d2.v1 The current record is supplemented by this dataset	dataset	April 2017
Additional file 3: Figure S1. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d3 The current record is supplemented by this dataset	dataset	May 2017
Additional file 3: Figure S1. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d3.v1 The current record is supplemented by this dataset	dataset	May 2017
Additional file 4: Figure S2. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d4 The current record is supplemented by this dataset	dataset	May 2017
Additional file 4: Figure S2. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d4.v1 The current record is supplemented by this dataset	dataset	May 2017
Additional file 5: Figure S3. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d5 The current record is supplemented by this figure	figure	May 2017
Additional file 5: Figure S3. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d5.v1 The current record is supplemented by this figure	figure	May 2017
Additional file 6: Table S2. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d6 The current record is supplemented by this dataset	dataset	May 2017
Additional file 6: Table S2. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d6.v1 The current record is supplemented by this dataset	dataset	May 2017
Additional file 7: Figure S4. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d7 The current record is supplemented by this figure	figure	May 2017
Additional file 7: Figure S4. of Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny; Kahn, Stacy; Delmont, Tom https://doi.org/10.6084/m9.figshare.c.3772019_d7.v1 The current record is supplemented by this dataset	dataset	May 2017