Cargando…

Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species

Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environm...

Descripción completa

Detalles Bibliográficos
Autores principales: Shankregowda, Aruna M., Siriyappagouder, Prabhugouda, Kuizenga, Marijn, Bal, Thijs M. P., Abdelhafiz, Yousri, Eizaguirre, Christophe, Fernandes, Jorge M. O., Kiron, Viswanath, Raeymaekers, Joost A. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601471/
https://www.ncbi.nlm.nih.gov/pubmed/37901806
http://dx.doi.org/10.3389/fmicb.2023.1232358
_version_ 1785126204309766144
author Shankregowda, Aruna M.
Siriyappagouder, Prabhugouda
Kuizenga, Marijn
Bal, Thijs M. P.
Abdelhafiz, Yousri
Eizaguirre, Christophe
Fernandes, Jorge M. O.
Kiron, Viswanath
Raeymaekers, Joost A. M.
author_facet Shankregowda, Aruna M.
Siriyappagouder, Prabhugouda
Kuizenga, Marijn
Bal, Thijs M. P.
Abdelhafiz, Yousri
Eizaguirre, Christophe
Fernandes, Jorge M. O.
Kiron, Viswanath
Raeymaekers, Joost A. M.
author_sort Shankregowda, Aruna M.
collection PubMed
description Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environmental and host-specific factors drive microbial diversity remains largely unknown, limiting our understanding of host-microbiome interactions in natural populations. Here, we compared the intestinal microbiota between two phylogenetically related fishes, the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) in a common landscape. Using amplicon sequencing of the V3-V4 region of the bacterial 16S rRNA gene, we characterised the α and β diversity of the microbial communities in these two fish species from both brackish water and freshwater habitats. Across eight locations, α diversity was higher in the nine-spined stickleback, suggesting a broader niche use in this host species. Habitat was a strong determinant of β diversity in both host species, while host species only explained a small fraction of the variation in gut microbial composition. Strong habitat-specific effects overruled effects of geographic distance and historical freshwater colonisation, suggesting that the gut microbiome correlates primarily with local environmental conditions. Interestingly, the effect of habitat divergence on gut microbial communities was stronger in three-spined stickleback than in nine-spined stickleback, possibly mirroring the stronger level of adaptive divergence in this host species. Overall, our results show that microbial communities reflect habitat divergence rather than colonisation history or dispersal limitation of host species.
format Online
Article
Text
id pubmed-10601471
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-106014712023-10-27 Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species Shankregowda, Aruna M. Siriyappagouder, Prabhugouda Kuizenga, Marijn Bal, Thijs M. P. Abdelhafiz, Yousri Eizaguirre, Christophe Fernandes, Jorge M. O. Kiron, Viswanath Raeymaekers, Joost A. M. Front Microbiol Microbiology Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environmental and host-specific factors drive microbial diversity remains largely unknown, limiting our understanding of host-microbiome interactions in natural populations. Here, we compared the intestinal microbiota between two phylogenetically related fishes, the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) in a common landscape. Using amplicon sequencing of the V3-V4 region of the bacterial 16S rRNA gene, we characterised the α and β diversity of the microbial communities in these two fish species from both brackish water and freshwater habitats. Across eight locations, α diversity was higher in the nine-spined stickleback, suggesting a broader niche use in this host species. Habitat was a strong determinant of β diversity in both host species, while host species only explained a small fraction of the variation in gut microbial composition. Strong habitat-specific effects overruled effects of geographic distance and historical freshwater colonisation, suggesting that the gut microbiome correlates primarily with local environmental conditions. Interestingly, the effect of habitat divergence on gut microbial communities was stronger in three-spined stickleback than in nine-spined stickleback, possibly mirroring the stronger level of adaptive divergence in this host species. Overall, our results show that microbial communities reflect habitat divergence rather than colonisation history or dispersal limitation of host species. Frontiers Media S.A. 2023-10-12 /pmc/articles/PMC10601471/ /pubmed/37901806 http://dx.doi.org/10.3389/fmicb.2023.1232358 Text en Copyright © 2023 Shankregowda, Siriyappagouder, Kuizenga, Bal, Abdelhafiz, Eizaguirre, Fernandes, Kiron and Raeymaekers. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Shankregowda, Aruna M.
Siriyappagouder, Prabhugouda
Kuizenga, Marijn
Bal, Thijs M. P.
Abdelhafiz, Yousri
Eizaguirre, Christophe
Fernandes, Jorge M. O.
Kiron, Viswanath
Raeymaekers, Joost A. M.
Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_full Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_fullStr Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_full_unstemmed Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_short Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_sort host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601471/
https://www.ncbi.nlm.nih.gov/pubmed/37901806
http://dx.doi.org/10.3389/fmicb.2023.1232358
work_keys_str_mv AT shankregowdaarunam hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT siriyappagouderprabhugouda hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT kuizengamarijn hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT balthijsmp hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT abdelhafizyousri hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT eizaguirrechristophe hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT fernandesjorgemo hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT kironviswanath hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies
AT raeymaekersjoostam hosthabitatratherthanevolutionaryhistoryexplainsgutmicrobiomediversityinsympatricsticklebackspecies