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

Abstract

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 popula-
tions 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 trap-
ping 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 follow-
ing 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 pat-
terns 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.

Citation

Fenn, J., Taylor, C., Goertz, S., Wanelik, K. M., Paterson, S., Begon, M., …Bradley, J. (2023). Discrete patterns of microbiome variability across timescales in a wild rodent population. BMC microbiology, 23(1), https://doi.org/10.1186/s12866-023-02824-x

• Journal Article Type: Article
• Acceptance Date: Mar 15, 2023
• Online Publication Date: Mar 30, 2023
• Publication Date: Mar 30, 2023
• Deposit Date: May 31, 2023
• Publicly Available Date: Jun 1, 2023
• Journal: BMC Microbiology
• Print ISSN: 1471-2180
• Publisher: Springer Verlag
• Peer Reviewed: Peer Reviewed
• Volume: 23
• Issue: 1
• DOI: https://doi.org/10.1186/s12866-023-02824-x
• Keywords: Microbiology (medical); Microbiology
• Additional Information: Received: 22 August 2022; Accepted: 15 March 2023; First Online: 30 March 2023; : ; : All procedures were performed with approval from the University of Liverpool Animal Welfare Committee, under a UK Home Office license (PPL 40/3235 to MB), and according to all related welfare guidelines and regulations. Where relevant, all procedures and reporting are in line with ARRIVE guidelines for the reporting of animal experiments.; : Not applicable.; : The authors declare no competing interests.