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 · 04 May 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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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

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Estimating relative biomasses of organisms in microbiota using “phylopeptidomics” Pible, Olivier; Allain, François; Jouffret, Virginie Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00797-x	journal	March 2020
Identification of the microbial diversity after fecal microbiota transplantation therapy for chronic intractable constipation using 16s rRNA amplicon sequencing Ohara, Tadashi PLOS ONE, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pone.0214085	journal	March 2019
Sunbeam: an extensible pipeline for analyzing metagenomic sequencing experiments Clarke, Erik L.; Taylor, Louis J.; Zhao, Chunyu https://doi.org/10.1101/326363	posted_content	January 2019
Assessing the viability of transplanted gut microbiota by sequential tagging with D-amino acid-based metabolic probes Wang, Wei; Lin, Liyuan; Du, Yahui Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09267-x	journal	March 2019
Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics Ziels, Ryan M.; Nobu, Masaru K.; Sousa, Diana Z. mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00159-19	journal	August 2019
Long-term colonisation with donor bacteriophages following successful faecal microbial transplantation Draper, L. A.; Ryan, F. J.; Smith, M. K. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0598-x	journal	December 2018
Sunbeam: an extensible pipeline for analyzing metagenomic sequencing experiments Clarke, Erik L.; Taylor, Louis J.; Zhao, Chunyu Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0658-x	journal	March 2019

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Related Subjects

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