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Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation

BACKGROUND: The virome of lung transplant recipients (LTRs) under immunosuppressive therapy is dominated by non-pathogenic Anelloviridae and further includes several pathogenic viruses such as Herpesviruses or respiratory viruses. It is unclear whether the donor-derived virome in the transplanted lu...

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Autores principales: Widder, Stefanie, Görzer, Irene, Friedel, Benjamin, Rahimi, Nina, Schwarz, Stefan, Jaksch, Peter, Knapp, Sylvia, Puchhammer-Stöckl, Elisabeth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9033415/
https://www.ncbi.nlm.nih.gov/pubmed/35459224
http://dx.doi.org/10.1186/s40168-022-01244-9
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author Widder, Stefanie
Görzer, Irene
Friedel, Benjamin
Rahimi, Nina
Schwarz, Stefan
Jaksch, Peter
Knapp, Sylvia
Puchhammer-Stöckl, Elisabeth
author_facet Widder, Stefanie
Görzer, Irene
Friedel, Benjamin
Rahimi, Nina
Schwarz, Stefan
Jaksch, Peter
Knapp, Sylvia
Puchhammer-Stöckl, Elisabeth
author_sort Widder, Stefanie
collection PubMed
description BACKGROUND: The virome of lung transplant recipients (LTRs) under immunosuppressive therapy is dominated by non-pathogenic Anelloviridae and further includes several pathogenic viruses such as Herpesviruses or respiratory viruses. It is unclear whether the donor-derived virome in the transplanted lung influences recipient virome dynamics in other body compartments and if so, to which degree. Likewise, it is unknown whether dependencies exist among virus populations that mutually shape viral loads and kinetics. RESULTS: To address these questions, we characterized viral communities in airways and plasma of 49 LTRs and analyzed their abundance patterns in a data modeling approach. We found distinct viral clusters that were specific for body compartments and displayed independent dynamics. These clusters robustly gathered specific viral species across the patient cohort. In the lung, viral cluster abundance associated with time after transplantation and we detected mutual exclusion of viral species within the same human host. In plasma, viral cluster dynamics were associated with the indication for transplantation lacking significant short-time changes. Interestingly, pathogenic viruses in the plasma co-occurred specifically with Alpha torque virus genogroup 4 and Gamma torque virus strains suggesting shared functional or ecological requirements. CONCLUSIONS: In summary, the detailed analysis of virome dynamics after lung transplantation revealed host, body compartment, and time-specific dependency patterns among viruses. Furthermore, our results suggested genetic adaptation to the host microenvironment at the level of the virome and support the hypothesis of functional complementarity between Anellovirus groups and other persistent viruses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01244-9.
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spelling pubmed-90334152022-04-24 Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation Widder, Stefanie Görzer, Irene Friedel, Benjamin Rahimi, Nina Schwarz, Stefan Jaksch, Peter Knapp, Sylvia Puchhammer-Stöckl, Elisabeth Microbiome Research BACKGROUND: The virome of lung transplant recipients (LTRs) under immunosuppressive therapy is dominated by non-pathogenic Anelloviridae and further includes several pathogenic viruses such as Herpesviruses or respiratory viruses. It is unclear whether the donor-derived virome in the transplanted lung influences recipient virome dynamics in other body compartments and if so, to which degree. Likewise, it is unknown whether dependencies exist among virus populations that mutually shape viral loads and kinetics. RESULTS: To address these questions, we characterized viral communities in airways and plasma of 49 LTRs and analyzed their abundance patterns in a data modeling approach. We found distinct viral clusters that were specific for body compartments and displayed independent dynamics. These clusters robustly gathered specific viral species across the patient cohort. In the lung, viral cluster abundance associated with time after transplantation and we detected mutual exclusion of viral species within the same human host. In plasma, viral cluster dynamics were associated with the indication for transplantation lacking significant short-time changes. Interestingly, pathogenic viruses in the plasma co-occurred specifically with Alpha torque virus genogroup 4 and Gamma torque virus strains suggesting shared functional or ecological requirements. CONCLUSIONS: In summary, the detailed analysis of virome dynamics after lung transplantation revealed host, body compartment, and time-specific dependency patterns among viruses. Furthermore, our results suggested genetic adaptation to the host microenvironment at the level of the virome and support the hypothesis of functional complementarity between Anellovirus groups and other persistent viruses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01244-9. BioMed Central 2022-04-23 /pmc/articles/PMC9033415/ /pubmed/35459224 http://dx.doi.org/10.1186/s40168-022-01244-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Widder, Stefanie
Görzer, Irene
Friedel, Benjamin
Rahimi, Nina
Schwarz, Stefan
Jaksch, Peter
Knapp, Sylvia
Puchhammer-Stöckl, Elisabeth
Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title_full Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title_fullStr Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title_full_unstemmed Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title_short Metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
title_sort metagenomic sequencing reveals time, host, and body compartment-specific viral dynamics after lung transplantation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9033415/
https://www.ncbi.nlm.nih.gov/pubmed/35459224
http://dx.doi.org/10.1186/s40168-022-01244-9
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