Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation

ABSTRACT Fecal microbiota transplantation (FMT) is a highly effective treatment for refractory Clostridium difficile infections. However, concerns persist about unwanted cotransfer of pathogenic microbes such as viruses. Here we studed FMT from a single healthy human donor to three pediatric ulcerat...

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Autores principales:	Christel Chehoud, Anatoly Dryga, Young Hwang, Dorottya Nagy-Szakal, Emily B. Hollister, Ruth Ann Luna, James Versalovic, Richard Kellermayer, Frederic D. Bushman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4178c471cbbf42d9a6e127aeef5d832e
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spelling	oai:doaj.org-article:4178c471cbbf42d9a6e127aeef5d832e2021-11-15T15:41:41ZTransfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation10.1128/mBio.00322-162150-7511https://doaj.org/article/4178c471cbbf42d9a6e127aeef5d832e2016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00322-16https://doaj.org/toc/2150-7511ABSTRACT Fecal microbiota transplantation (FMT) is a highly effective treatment for refractory Clostridium difficile infections. However, concerns persist about unwanted cotransfer of pathogenic microbes such as viruses. Here we studed FMT from a single healthy human donor to three pediatric ulcerative colitis patients, each of whom received a course of 22 to 30 FMT treatments. Viral particles were purified from donor and recipient stool samples and sequenced; the reads were then assembled into contigs corresponding to viral genomes or partial genomes. Transfer of selected viruses was confirmed by quantitative PCR. Viral contigs present in the donor could be readily detected in recipients, with up to 32 different donor viral contigs appearing in a recipient sample. Reassuringly, none of these were viruses are known to replicate on human cells. Instead, viral contigs either scored as bacteriophage or could not be attributed taxonomically, suggestive of unstudied phage. The two most frequently transferred gene types were associated with temperate-phage replication. In addition, members of Siphoviridae, the group of typically temperate phages that includes phage lambda, were found to be transferred with significantly greater efficiency than other groups. On the basis of these findings, we propose that the temperate-phage replication style may promote efficient phage transfer between human individuals. In summary, we documented transfer of multiple viral lineages between human individuals through FMT, but in this case series, none were from viral groups known to infect human cells. IMPORTANCE Transfer of whole communities of viruses between humans has rarely been studied but is of likely medical importance. Here we studied fecal microbiota transplantation (FMT), a highly successful treatment for relapsing Clostridium difficile infection and, potentially, other gastrointestinal (GI) diseases. We investigated the transfer of viral communities during FMT and documented transfer of multiple viral lineages between humans. None of these were viruses that replicated on animal cells or that are known to be pathogenic. We found that temperate bacteriophage, which form stable associations with their hosts, were significantly more likely to be transferred during FMT. This supports a model in which the viral temperate replication style may have evolved in part to support efficient viral transmission between environments.Christel ChehoudAnatoly DrygaYoung HwangDorottya Nagy-SzakalEmily B. HollisterRuth Ann LunaJames VersalovicRichard KellermayerFrederic D. BushmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Christel Chehoud Anatoly Dryga Young Hwang Dorottya Nagy-Szakal Emily B. Hollister Ruth Ann Luna James Versalovic Richard Kellermayer Frederic D. Bushman Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
description	ABSTRACT Fecal microbiota transplantation (FMT) is a highly effective treatment for refractory Clostridium difficile infections. However, concerns persist about unwanted cotransfer of pathogenic microbes such as viruses. Here we studed FMT from a single healthy human donor to three pediatric ulcerative colitis patients, each of whom received a course of 22 to 30 FMT treatments. Viral particles were purified from donor and recipient stool samples and sequenced; the reads were then assembled into contigs corresponding to viral genomes or partial genomes. Transfer of selected viruses was confirmed by quantitative PCR. Viral contigs present in the donor could be readily detected in recipients, with up to 32 different donor viral contigs appearing in a recipient sample. Reassuringly, none of these were viruses are known to replicate on human cells. Instead, viral contigs either scored as bacteriophage or could not be attributed taxonomically, suggestive of unstudied phage. The two most frequently transferred gene types were associated with temperate-phage replication. In addition, members of Siphoviridae, the group of typically temperate phages that includes phage lambda, were found to be transferred with significantly greater efficiency than other groups. On the basis of these findings, we propose that the temperate-phage replication style may promote efficient phage transfer between human individuals. In summary, we documented transfer of multiple viral lineages between human individuals through FMT, but in this case series, none were from viral groups known to infect human cells. IMPORTANCE Transfer of whole communities of viruses between humans has rarely been studied but is of likely medical importance. Here we studied fecal microbiota transplantation (FMT), a highly successful treatment for relapsing Clostridium difficile infection and, potentially, other gastrointestinal (GI) diseases. We investigated the transfer of viral communities during FMT and documented transfer of multiple viral lineages between humans. None of these were viruses that replicated on animal cells or that are known to be pathogenic. We found that temperate bacteriophage, which form stable associations with their hosts, were significantly more likely to be transferred during FMT. This supports a model in which the viral temperate replication style may have evolved in part to support efficient viral transmission between environments.
format	article
author	Christel Chehoud Anatoly Dryga Young Hwang Dorottya Nagy-Szakal Emily B. Hollister Ruth Ann Luna James Versalovic Richard Kellermayer Frederic D. Bushman
author_facet	Christel Chehoud Anatoly Dryga Young Hwang Dorottya Nagy-Szakal Emily B. Hollister Ruth Ann Luna James Versalovic Richard Kellermayer Frederic D. Bushman
author_sort	Christel Chehoud
title	Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
title_short	Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
title_full	Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
title_fullStr	Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
title_full_unstemmed	Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation
title_sort	transfer of viral communities between human individuals during fecal microbiota transplantation
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/4178c471cbbf42d9a6e127aeef5d832e
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Transfer of Viral Communities between Human Individuals during Fecal Microbiota Transplantation

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