Cargando…

Discrete patterns of microbiome variability across timescales in a wild rodent population

Mammalian gastrointestinal microbiomes are highly variable, both within individuals and across populations, with changes linked to time and ageing being widely reported. Discerning patterns of change in wild mammal populations can therefore prove challenging. We used high-throughput community sequen...

Descripción completa

Detalles Bibliográficos
Autores principales: Fenn, Jonathan, Taylor, Christopher, Goertz, Sarah, Wanelik, Klara M., Paterson, Steve, Begon, Mike, Jackson, Joe, Bradley, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10061908/
https://www.ncbi.nlm.nih.gov/pubmed/36997846
http://dx.doi.org/10.1186/s12866-023-02824-x
_version_ 1785017388704464896
author Fenn, Jonathan
Taylor, Christopher
Goertz, Sarah
Wanelik, Klara M.
Paterson, Steve
Begon, Mike
Jackson, Joe
Bradley, Jan
author_facet Fenn, Jonathan
Taylor, Christopher
Goertz, Sarah
Wanelik, Klara M.
Paterson, Steve
Begon, Mike
Jackson, Joe
Bradley, Jan
author_sort Fenn, Jonathan
collection PubMed
description Mammalian gastrointestinal microbiomes are highly variable, both within individuals and across populations, with changes linked to time and ageing being widely reported. Discerning patterns of change in wild mammal populations can therefore prove challenging. We used high-throughput community sequencing methods to characterise the microbiome of wild field voles (Microtus agrestis) from faecal samples collected across 12 live-trapping field sessions, and then at cull. Changes in α- and β-diversity were modelled over three timescales. Short-term differences (following 1–2 days captivity) were analysed between capture and cull, to ascertain the degree to which the microbiome can change following a rapid change in environment. Medium-term changes were measured between successive trapping sessions (12–16 days apart), and long-term changes between the first and final capture of an individual (from 24 to 129 days). The short period between capture and cull was characterised by a marked loss of species richness, while over medium and long-term in the field, richness slightly increased. Changes across both short and long timescales indicated shifts from a Firmicutes-dominant to a Bacteroidetes-dominant microbiome. Dramatic changes following captivity indicate that changes in microbiome diversity can be rapid, following a change of environment (food sources, temperature, lighting etc.). Medium- and long-term patterns of change indicate an accrual of gut bacteria associated with ageing, with these new bacteria being predominately represented by Bacteroidetes. While the patterns of change observed are unlikely to be universal to wild mammal populations, the potential for analogous shifts across timescales should be considered whenever studying wild animal microbiomes. This is especially true if studies involve animal captivity, as there are potential ramifications both for animal health, and the validity of the data itself as a reflection of a ‘natural’ state of an animal. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02824-x.
format Online
Article
Text
id pubmed-10061908
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-100619082023-03-31 Discrete patterns of microbiome variability across timescales in a wild rodent population Fenn, Jonathan Taylor, Christopher Goertz, Sarah Wanelik, Klara M. Paterson, Steve Begon, Mike Jackson, Joe Bradley, Jan BMC Microbiol Research Mammalian gastrointestinal microbiomes are highly variable, both within individuals and across populations, with changes linked to time and ageing being widely reported. Discerning patterns of change in wild mammal populations can therefore prove challenging. We used high-throughput community sequencing methods to characterise the microbiome of wild field voles (Microtus agrestis) from faecal samples collected across 12 live-trapping field sessions, and then at cull. Changes in α- and β-diversity were modelled over three timescales. Short-term differences (following 1–2 days captivity) were analysed between capture and cull, to ascertain the degree to which the microbiome can change following a rapid change in environment. Medium-term changes were measured between successive trapping sessions (12–16 days apart), and long-term changes between the first and final capture of an individual (from 24 to 129 days). The short period between capture and cull was characterised by a marked loss of species richness, while over medium and long-term in the field, richness slightly increased. Changes across both short and long timescales indicated shifts from a Firmicutes-dominant to a Bacteroidetes-dominant microbiome. Dramatic changes following captivity indicate that changes in microbiome diversity can be rapid, following a change of environment (food sources, temperature, lighting etc.). Medium- and long-term patterns of change indicate an accrual of gut bacteria associated with ageing, with these new bacteria being predominately represented by Bacteroidetes. While the patterns of change observed are unlikely to be universal to wild mammal populations, the potential for analogous shifts across timescales should be considered whenever studying wild animal microbiomes. This is especially true if studies involve animal captivity, as there are potential ramifications both for animal health, and the validity of the data itself as a reflection of a ‘natural’ state of an animal. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02824-x. BioMed Central 2023-03-30 /pmc/articles/PMC10061908/ /pubmed/36997846 http://dx.doi.org/10.1186/s12866-023-02824-x Text en © The Author(s) 2023 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
Fenn, Jonathan
Taylor, Christopher
Goertz, Sarah
Wanelik, Klara M.
Paterson, Steve
Begon, Mike
Jackson, Joe
Bradley, Jan
Discrete patterns of microbiome variability across timescales in a wild rodent population
title Discrete patterns of microbiome variability across timescales in a wild rodent population
title_full Discrete patterns of microbiome variability across timescales in a wild rodent population
title_fullStr Discrete patterns of microbiome variability across timescales in a wild rodent population
title_full_unstemmed Discrete patterns of microbiome variability across timescales in a wild rodent population
title_short Discrete patterns of microbiome variability across timescales in a wild rodent population
title_sort discrete patterns of microbiome variability across timescales in a wild rodent population
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10061908/
https://www.ncbi.nlm.nih.gov/pubmed/36997846
http://dx.doi.org/10.1186/s12866-023-02824-x
work_keys_str_mv AT fennjonathan discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT taylorchristopher discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT goertzsarah discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT wanelikklaram discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT patersonsteve discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT begonmike discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT jacksonjoe discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation
AT bradleyjan discretepatternsofmicrobiomevariabilityacrosstimescalesinawildrodentpopulation