Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae

ABSTRACT Understanding the role of fecal microbiota transplantation (FMT) in the decolonization of multidrug-resistant organisms (MDRO) is critical. Specifically, little is known about virome changes in MDRO-infected subjects treated with FMT. Using shotgun metagenomic sequencing, we characterized l...

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Main Authors: Qin Liu, Tao Zuo, Wenqi Lu, Yun Kit Yeoh, Qi Su, Zhilu Xu, Whitney Tang, Keli Yang, Fen Zhang, Louis H. S. Lau, Rashid N. S. Lui, Miu Ling Chin, Rity Wong, Chun Pan Cheung, Wenyi Zhu, Paul K. S. Chan, Francis K. L. Chan, Grace C. Lui, Siew C. Ng
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.01510-21
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author Qin Liu
Tao Zuo
Wenqi Lu
Yun Kit Yeoh
Qi Su
Zhilu Xu
Whitney Tang
Keli Yang
Fen Zhang
Louis H. S. Lau
Rashid N. S. Lui
Miu Ling Chin
Rity Wong
Chun Pan Cheung
Wenyi Zhu
Paul K. S. Chan
Francis K. L. Chan
Grace C. Lui
Siew C. Ng
author_facet Qin Liu
Tao Zuo
Wenqi Lu
Yun Kit Yeoh
Qi Su
Zhilu Xu
Whitney Tang
Keli Yang
Fen Zhang
Louis H. S. Lau
Rashid N. S. Lui
Miu Ling Chin
Rity Wong
Chun Pan Cheung
Wenyi Zhu
Paul K. S. Chan
Francis K. L. Chan
Grace C. Lui
Siew C. Ng
author_sort Qin Liu
collection DOAJ
description ABSTRACT Understanding the role of fecal microbiota transplantation (FMT) in the decolonization of multidrug-resistant organisms (MDRO) is critical. Specifically, little is known about virome changes in MDRO-infected subjects treated with FMT. Using shotgun metagenomic sequencing, we characterized longitudinal dynamics of the gut virome and bacteriome in three recipients who successfully decolonized carbapenem-resistant Enterobacteriaceae (CRE), including Klebsiella spp. and Escherichia coli, after FMT. We observed large shifts of the fecal bacterial microbiota resembling a donor-like community after transfer of a fecal microbiota dominated by the genus Ruminococcus. We found a substantial expansion of Klebsiella phages after FMT with a concordant decrease of Klebsiella spp. and striking increase of Escherichia phages in CRE E. coli carriers after FMT. We also observed the CRE elimination and similar evolution of Klebsiella phage in mice, which may play a role in the collapse of the Klebsiella population after FMT. In summary, our pilot study documented bacteriome and virome alterations after FMT which mediate many of the effects of FMT on the gut microbiome community. IMPORTANCE Fecal microbiota transplantation (FMT) is an effective treatment for multidrug-resistant organisms; however, introducing a complex mixture of microbes also has unknown consequences for landscape features of gut microbiome. We sought to understand bacteriome and virome alterations in patients undergoing FMT to treat infection with carbapenem-resistant Enterobacteriaceae. This finding indicates that transkingdom interactions between the virome and bacteriome communities may have evolved in part to support efficient FMT for treating CRE.
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spelling doaj.art-ad3803a9cef04d1ea331a5dd4c5fd0b62022-12-22T00:20:03ZengAmerican Society for MicrobiologymSystems2379-50772022-06-017310.1128/msystems.01510-21Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant EnterobacteriaceaeQin Liu0Tao Zuo1Wenqi Lu2Yun Kit Yeoh3Qi Su4Zhilu Xu5Whitney Tang6Keli Yang7Fen Zhang8Louis H. S. Lau9Rashid N. S. Lui10Miu Ling Chin11Rity Wong12Chun Pan Cheung13Wenyi Zhu14Paul K. S. Chan15Francis K. L. Chan16Grace C. Lui17Siew C. Ng18Center for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaDepartment of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, ChinaDepartment of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, ChinaDepartment of Microbiology, The Chinese University of Hong Kong, Hong Kong, ChinaDepartment of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaDepartment of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, ChinaCenter for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong, ChinaABSTRACT Understanding the role of fecal microbiota transplantation (FMT) in the decolonization of multidrug-resistant organisms (MDRO) is critical. Specifically, little is known about virome changes in MDRO-infected subjects treated with FMT. Using shotgun metagenomic sequencing, we characterized longitudinal dynamics of the gut virome and bacteriome in three recipients who successfully decolonized carbapenem-resistant Enterobacteriaceae (CRE), including Klebsiella spp. and Escherichia coli, after FMT. We observed large shifts of the fecal bacterial microbiota resembling a donor-like community after transfer of a fecal microbiota dominated by the genus Ruminococcus. We found a substantial expansion of Klebsiella phages after FMT with a concordant decrease of Klebsiella spp. and striking increase of Escherichia phages in CRE E. coli carriers after FMT. We also observed the CRE elimination and similar evolution of Klebsiella phage in mice, which may play a role in the collapse of the Klebsiella population after FMT. In summary, our pilot study documented bacteriome and virome alterations after FMT which mediate many of the effects of FMT on the gut microbiome community. IMPORTANCE Fecal microbiota transplantation (FMT) is an effective treatment for multidrug-resistant organisms; however, introducing a complex mixture of microbes also has unknown consequences for landscape features of gut microbiome. We sought to understand bacteriome and virome alterations in patients undergoing FMT to treat infection with carbapenem-resistant Enterobacteriaceae. This finding indicates that transkingdom interactions between the virome and bacteriome communities may have evolved in part to support efficient FMT for treating CRE.https://journals.asm.org/doi/10.1128/msystems.01510-21CREFMTbacteriomevirome
spellingShingle Qin Liu
Tao Zuo
Wenqi Lu
Yun Kit Yeoh
Qi Su
Zhilu Xu
Whitney Tang
Keli Yang
Fen Zhang
Louis H. S. Lau
Rashid N. S. Lui
Miu Ling Chin
Rity Wong
Chun Pan Cheung
Wenyi Zhu
Paul K. S. Chan
Francis K. L. Chan
Grace C. Lui
Siew C. Ng
Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
mSystems
CRE
FMT
bacteriome
virome
title Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
title_full Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
title_fullStr Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
title_full_unstemmed Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
title_short Longitudinal Evaluation of Gut Bacteriomes and Viromes after Fecal Microbiota Transplantation for Eradication of Carbapenem-Resistant Enterobacteriaceae
title_sort longitudinal evaluation of gut bacteriomes and viromes after fecal microbiota transplantation for eradication of carbapenem resistant enterobacteriaceae
topic CRE
FMT
bacteriome
virome
url https://journals.asm.org/doi/10.1128/msystems.01510-21
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