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A framework for testing the impact of co-infections on host gut microbiomes

Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a fram...

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Autores principales: Schmid, Dominik W., Fackelmann, Gloria, Wasimuddin, Rakotondranary, Jacques, Ratovonamana, Yedidya R., Montero, B. Karina, Ganzhorn, Jörg U., Sommer, Simone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9361228/
https://www.ncbi.nlm.nih.gov/pubmed/35945629
http://dx.doi.org/10.1186/s42523-022-00198-5
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author Schmid, Dominik W.
Fackelmann, Gloria
Wasimuddin
Rakotondranary, Jacques
Ratovonamana, Yedidya R.
Montero, B. Karina
Ganzhorn, Jörg U.
Sommer, Simone
author_facet Schmid, Dominik W.
Fackelmann, Gloria
Wasimuddin
Rakotondranary, Jacques
Ratovonamana, Yedidya R.
Montero, B. Karina
Ganzhorn, Jörg U.
Sommer, Simone
author_sort Schmid, Dominik W.
collection PubMed
description Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00198-5.
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spelling pubmed-93612282022-08-09 A framework for testing the impact of co-infections on host gut microbiomes Schmid, Dominik W. Fackelmann, Gloria Wasimuddin Rakotondranary, Jacques Ratovonamana, Yedidya R. Montero, B. Karina Ganzhorn, Jörg U. Sommer, Simone Anim Microbiome Review Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00198-5. BioMed Central 2022-08-09 /pmc/articles/PMC9361228/ /pubmed/35945629 http://dx.doi.org/10.1186/s42523-022-00198-5 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/) .
spellingShingle Review
Schmid, Dominik W.
Fackelmann, Gloria
Wasimuddin
Rakotondranary, Jacques
Ratovonamana, Yedidya R.
Montero, B. Karina
Ganzhorn, Jörg U.
Sommer, Simone
A framework for testing the impact of co-infections on host gut microbiomes
title A framework for testing the impact of co-infections on host gut microbiomes
title_full A framework for testing the impact of co-infections on host gut microbiomes
title_fullStr A framework for testing the impact of co-infections on host gut microbiomes
title_full_unstemmed A framework for testing the impact of co-infections on host gut microbiomes
title_short A framework for testing the impact of co-infections on host gut microbiomes
title_sort framework for testing the impact of co-infections on host gut microbiomes
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9361228/
https://www.ncbi.nlm.nih.gov/pubmed/35945629
http://dx.doi.org/10.1186/s42523-022-00198-5
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