Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects
Fecal microbiota transplantation (FMT) is currently used for treating Clostridium difficile infection and explored for other clinical applications in experimental trials. However, the effectiveness of this therapy could vary, and partly depend on the donor's bacterial species engraftment, whose evaluation is challenging because there are no cost-effective strategies for accurately tracking the microbe transference. In this regard, the precise identification of bacterial species inhabiting the human gut is essential to define their role in human health unambiguously. We used Nanopore-based device to sequence bacterial rrn operons (16S-ITS-23S) and to reveal species-level abundance changes in the human gut microbiota of a FMT trial. By assessing the donor and recipient microbiota before and after FMT, we further evaluated whether this molecular approach reveals strain-level genetic variation to demonstrate microbe transfer and engraftment. Strict control over sequencing data quality and major microbiota covariates was critical for accurately estimating the changes in gut microbial species abundance in the recipients after FMT. We detected strain-level variation via single-nucleotide variants (SNVs) at rrn regions in a species-specific manner. We showed that it was possible to explore successfully the donor-bacterial strain (e.g., Parabacteroides merdae) engraftment in recipients of the FMT by assessing the nucleotide frequencies at rrn-associated SNVs. Our findings indicate that the engraftment of donors' microbiota is to some extent correlated with the improvement of metabolic health in recipients and that parameters such as the baseline gut microbiota configuration, sex, and age of donors should be considered to ensure the success of FMT in humans. The study was prospectively registered at the Dutch Trial registry - NTR4488 (https://www.trialregister.nl/trial/4488).
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Taylor & Francis
2022-05-23
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Subjects: | MinION, Nanopore sequencing, Gut microbiota, rrn operon, Single-nucleotide variation, Species engraftment, Species-level resolution, http://metadata.un.org/sdg/3, Ensure healthy lives and promote well-being for all at all ages, |
Online Access: | http://hdl.handle.net/10261/305686 http://dx.doi.org/10.13039/501100004587 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000780 https://api.elsevier.com/content/abstract/scopus_id/85130461879 |
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dig-iata-es-10261-3056862024-05-16T20:38:17Z Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects Benítez-Páez, Alfonso Hartstra, Annick V Nieuwdorp, Max Sanz Herranz, Yolanda European Commission Ministerio de Ciencia e Innovación (España) Instituto de Salud Carlos III 0000-0001-5707-4340 0000-0002-1615-1976 MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages Fecal microbiota transplantation (FMT) is currently used for treating Clostridium difficile infection and explored for other clinical applications in experimental trials. However, the effectiveness of this therapy could vary, and partly depend on the donor's bacterial species engraftment, whose evaluation is challenging because there are no cost-effective strategies for accurately tracking the microbe transference. In this regard, the precise identification of bacterial species inhabiting the human gut is essential to define their role in human health unambiguously. We used Nanopore-based device to sequence bacterial rrn operons (16S-ITS-23S) and to reveal species-level abundance changes in the human gut microbiota of a FMT trial. By assessing the donor and recipient microbiota before and after FMT, we further evaluated whether this molecular approach reveals strain-level genetic variation to demonstrate microbe transfer and engraftment. Strict control over sequencing data quality and major microbiota covariates was critical for accurately estimating the changes in gut microbial species abundance in the recipients after FMT. We detected strain-level variation via single-nucleotide variants (SNVs) at rrn regions in a species-specific manner. We showed that it was possible to explore successfully the donor-bacterial strain (e.g., Parabacteroides merdae) engraftment in recipients of the FMT by assessing the nucleotide frequencies at rrn-associated SNVs. Our findings indicate that the engraftment of donors' microbiota is to some extent correlated with the improvement of metabolic health in recipients and that parameters such as the baseline gut microbiota configuration, sex, and age of donors should be considered to ensure the success of FMT in humans. The study was prospectively registered at the Dutch Trial registry - NTR4488 (https://www.trialregister.nl/trial/4488). This study was supported by the EU Project MyNewGut [No. 613979] of the European Commission 7th Framework Programme and grant [PID2020-119536RB-I00] from the Ministry of Science and Innovation (Spain). This research study was also completed thanks to the [CP19/00132] grant from Miguel Servet program to ABP from the Institute of Health Carlos III (ISCIII) and its co-funding from the European Social Fund (ESF/FSE). Peer reviewed 2023-04-06T10:47:01Z 2023-04-06T10:47:01Z 2022-05-23 artículo http://purl.org/coar/resource_type/c_6501 Gut Microbes 14 (1): 2078621 (2022) 1949-0976 http://hdl.handle.net/10261/305686 10.1080/19490976.2022.2078621 http://dx.doi.org/10.13039/501100004587 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000780 35604764 2-s2.0-85130461879 https://api.elsevier.com/content/abstract/scopus_id/85130461879 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/FP7/123456/613979 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-119536RB-I0 Gut microbes Publisher's version https://doi.org/10.1080/19490976.2022.2078621 Sí open Taylor & Francis |
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MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages |
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MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages Benítez-Páez, Alfonso Hartstra, Annick V Nieuwdorp, Max Sanz Herranz, Yolanda Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
description |
Fecal microbiota transplantation (FMT) is currently used for treating Clostridium difficile infection and explored for other clinical applications in experimental trials. However, the effectiveness of this therapy could vary, and partly depend on the donor's bacterial species engraftment, whose evaluation is challenging because there are no cost-effective strategies for accurately tracking the microbe transference. In this regard, the precise identification of bacterial species inhabiting the human gut is essential to define their role in human health unambiguously. We used Nanopore-based device to sequence bacterial rrn operons (16S-ITS-23S) and to reveal species-level abundance changes in the human gut microbiota of a FMT trial. By assessing the donor and recipient microbiota before and after FMT, we further evaluated whether this molecular approach reveals strain-level genetic variation to demonstrate microbe transfer and engraftment. Strict control over sequencing data quality and major microbiota covariates was critical for accurately estimating the changes in gut microbial species abundance in the recipients after FMT. We detected strain-level variation via single-nucleotide variants (SNVs) at rrn regions in a species-specific manner. We showed that it was possible to explore successfully the donor-bacterial strain (e.g., Parabacteroides merdae) engraftment in recipients of the FMT by assessing the nucleotide frequencies at rrn-associated SNVs. Our findings indicate that the engraftment of donors' microbiota is to some extent correlated with the improvement of metabolic health in recipients and that parameters such as the baseline gut microbiota configuration, sex, and age of donors should be considered to ensure the success of FMT in humans. The study was prospectively registered at the Dutch Trial registry - NTR4488 (https://www.trialregister.nl/trial/4488). |
author2 |
European Commission |
author_facet |
European Commission Benítez-Páez, Alfonso Hartstra, Annick V Nieuwdorp, Max Sanz Herranz, Yolanda |
format |
artículo |
topic_facet |
MinION Nanopore sequencing Gut microbiota rrn operon Single-nucleotide variation Species engraftment Species-level resolution http://metadata.un.org/sdg/3 Ensure healthy lives and promote well-being for all at all ages |
author |
Benítez-Páez, Alfonso Hartstra, Annick V Nieuwdorp, Max Sanz Herranz, Yolanda |
author_sort |
Benítez-Páez, Alfonso |
title |
Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
title_short |
Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
title_full |
Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
title_fullStr |
Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
title_full_unstemmed |
Species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
title_sort |
species- and strain-level assessment using rrn long-amplicons suggests donor's influence on gut microbial transference via fecal transplants in metabolic syndrome subjects |
publisher |
Taylor & Francis |
publishDate |
2022-05-23 |
url |
http://hdl.handle.net/10261/305686 http://dx.doi.org/10.13039/501100004587 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000780 https://api.elsevier.com/content/abstract/scopus_id/85130461879 |
work_keys_str_mv |
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