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Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)

Human activity is a major driver of ecological and evolutionary change in wild populations and can have diverse effects on eukaryotic organisms as well as on environmental and host‐associated microbial communities. Although host–microbiome interactions can be a major determinant of host fitness, few...

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Autores principales: Lafuente, Elvira, Carles, Louis, Walser, Jean‐Claude, Giulio, Marco, Wullschleger, Simon, Stamm, Christian, Räsänen, Katja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10130563/
https://www.ncbi.nlm.nih.gov/pubmed/37124094
http://dx.doi.org/10.1111/eva.13540
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author Lafuente, Elvira
Carles, Louis
Walser, Jean‐Claude
Giulio, Marco
Wullschleger, Simon
Stamm, Christian
Räsänen, Katja
author_facet Lafuente, Elvira
Carles, Louis
Walser, Jean‐Claude
Giulio, Marco
Wullschleger, Simon
Stamm, Christian
Räsänen, Katja
author_sort Lafuente, Elvira
collection PubMed
description Human activity is a major driver of ecological and evolutionary change in wild populations and can have diverse effects on eukaryotic organisms as well as on environmental and host‐associated microbial communities. Although host–microbiome interactions can be a major determinant of host fitness, few studies consider the joint responses of hosts and their microbiomes to anthropogenic changes. In freshwater ecosystems, wastewater is a widespread anthropogenic stressor that represents a multifarious environmental perturbation. Here, we experimentally tested the impact of treated wastewater on a keystone host (the freshwater isopod Asellus aquaticus) and its gut microbiome. We used a semi‐natural flume experiment, in combination with 16S rRNA amplicon sequencing, to assess how different concentrations (0%, 30%, and 80%) of nonfiltered wastewater (i.e. with chemical toxicants, nutrients, organic particles, and microbes) versus ultrafiltered wastewater (i.e. only dissolved pollutants and nutrients) affected host survival, growth, and food consumption as well as mid‐ and hindgut bacterial community composition and diversity. Our results show that while host survival was not affected by the treatments, host growth increased and host feeding rate decreased with nonfiltered wastewater – potentially indicating that A. aquaticus fed on organic matter and microbes available in nonfiltered wastewater. Furthermore, even though the midgut microbiome (diversity and composition) was not affected by any of our treatments, nonfiltered wastewater influenced bacterial composition (but not diversity) in the hindgut. Ultrafiltered wastewater, on the other hand, affected both community composition and bacterial diversity in the hindgut, an effect that in our system differed between sexes. While the functional consequences of microbiome changes and their sex specificity are yet to be tested, our results indicate that different components of multifactorial stressors (i.e. different constituents of wastewater) can affect hosts and their microbiome in distinct (even opposing) manners and have a substantial impact on eco‐evolutionary responses to anthropogenic stressors.
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spelling pubmed-101305632023-04-27 Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus) Lafuente, Elvira Carles, Louis Walser, Jean‐Claude Giulio, Marco Wullschleger, Simon Stamm, Christian Räsänen, Katja Evol Appl Original Articles Human activity is a major driver of ecological and evolutionary change in wild populations and can have diverse effects on eukaryotic organisms as well as on environmental and host‐associated microbial communities. Although host–microbiome interactions can be a major determinant of host fitness, few studies consider the joint responses of hosts and their microbiomes to anthropogenic changes. In freshwater ecosystems, wastewater is a widespread anthropogenic stressor that represents a multifarious environmental perturbation. Here, we experimentally tested the impact of treated wastewater on a keystone host (the freshwater isopod Asellus aquaticus) and its gut microbiome. We used a semi‐natural flume experiment, in combination with 16S rRNA amplicon sequencing, to assess how different concentrations (0%, 30%, and 80%) of nonfiltered wastewater (i.e. with chemical toxicants, nutrients, organic particles, and microbes) versus ultrafiltered wastewater (i.e. only dissolved pollutants and nutrients) affected host survival, growth, and food consumption as well as mid‐ and hindgut bacterial community composition and diversity. Our results show that while host survival was not affected by the treatments, host growth increased and host feeding rate decreased with nonfiltered wastewater – potentially indicating that A. aquaticus fed on organic matter and microbes available in nonfiltered wastewater. Furthermore, even though the midgut microbiome (diversity and composition) was not affected by any of our treatments, nonfiltered wastewater influenced bacterial composition (but not diversity) in the hindgut. Ultrafiltered wastewater, on the other hand, affected both community composition and bacterial diversity in the hindgut, an effect that in our system differed between sexes. While the functional consequences of microbiome changes and their sex specificity are yet to be tested, our results indicate that different components of multifactorial stressors (i.e. different constituents of wastewater) can affect hosts and their microbiome in distinct (even opposing) manners and have a substantial impact on eco‐evolutionary responses to anthropogenic stressors. John Wiley and Sons Inc. 2023-03-30 /pmc/articles/PMC10130563/ /pubmed/37124094 http://dx.doi.org/10.1111/eva.13540 Text en © 2023 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Lafuente, Elvira
Carles, Louis
Walser, Jean‐Claude
Giulio, Marco
Wullschleger, Simon
Stamm, Christian
Räsänen, Katja
Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title_full Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title_fullStr Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title_full_unstemmed Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title_short Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)
title_sort effects of anthropogenic stress on hosts and their microbiomes: treated wastewater alters performance and gut microbiome of a key detritivore (asellus aquaticus)
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10130563/
https://www.ncbi.nlm.nih.gov/pubmed/37124094
http://dx.doi.org/10.1111/eva.13540
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