Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination

Lavrinienko, Anton; Hämäläinen, Anni; Hindström, Rasmus; Tukalenko, Eugene; Boratyński, Zbyszek; Kivisaari, Kati; Mousseau, Timothy A.; Watts, Phillip C.; Mappes, Tapio

doi:10.1111/mec.15945

Cited by 19 publications

(24 citation statements)

References 94 publications

(190 reference statements)

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“…The analysis by Antwis et al (2021) potentially examines the response of Apodemus mice to medium and high absorbed dose rates but does not examine how exposure to radionuclides per se impacts the gut microbiota in different species of rodent. By contrast, comparable impacts of exposure to radionuclides in the gut microbiota of three (out of four) species of Apodemus are apparent in samples collected from the CEZ and the Fukushima accident sites (Lavrinienko, Hämäläinen, et al, 2021).…”

Section: Differences Between Microbiota Detected In Samples From Faec...mentioning

confidence: 99%

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

Watts

Mappes

Tukalenko

et al. 2022

Journal of Animal Ecology

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Evidence that exposure to environmental pollutants can alter the gut microbiota composition of wildlife includes studies of rodents exposed to radionuclides. Antwis et al. (2021) used amplicon sequencing to characterise the gut microbiota of four species of rodent (Myodes glareolus, Apodemus agrarius, A. flavicollis and A. sylvaticus) inhabiting the Chernobyl Exclusion Zone (CEZ) to examine possible changes in gut bacteria (microbiota) and gut fungi (mycobiota) associated with exposure to radionuclides and whether the sample type (from caecum or faeces) affected the analysis. The conclusions derived from the analyses of gut mycobiota are based on data that represent a mixture of ingested fungi (e.g. edible macrofungi, polypores, lichens and ectomycorrhizae) and gut mycobiota (e.g. microfungi and yeasts), which mask the patterns of inter‐ and intraspecific variation in the authentic gut mycobiota. Implying that ‘faecal samples are not an accurate indicator of gut composition’ creates an unnecessary controversy about faecal sampling because the comparison of samples from the caecum and faeces confounds many other possible drivers (including different animals from different locations, sampled in different years) of variation in gut microbiota. It is relevant also that Antwis et al.'s (2021) data lack statistical power to detect an effect of exposure to radionuclides on the gut microbiota because (1) all of their samples of Apodemus mice had experienced a medium or high total absorbed dose rate and (2) they did not collect samples of bank voles (M. glareolus) from replicate contaminated and uncontaminated locations. Discussion of Antwis et al.'s (2021) analysis, especially the claims presented in the Abstract, is important to prevent controversy about the outcome of research on the biological impacts of wildlife inhabiting the CEZ.

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Section: Differences Between Microbiota Detected In Samples From Faec...mentioning

confidence: 99%

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

Watts

Mappes

Tukalenko

et al. 2022

Journal of Animal Ecology

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“…On the other hand, gut bacteria can have complicated effects on host inflammatory immune responses, both in the gut and other tissues ( Ichinohe et al, 2011 ; Hooper, Littman & Macpherson, 2012 ; Wilks & Golovkina, 2012 ; Shukla et al, 2017 ; Lazar et al, 2018 ; Kogut, Lee & Santin, 2020 ), making the effects of commensal gut bacteria on host responses to infections difficult to predict. As anthropogenic impacts on wildlife and their bacterial communities increase in extent, via antibiotics and other stressors ( Kelly et al, 2014 ; Teyssier et al, 2018 ; Trevelline et al, 2019 ; Kraemer, Ramachandran & Perron, 2019 ; Lavrinienko et al, 2021 ), a better understanding of the importance of bacterial communities in wildlife hosts is imperative to prepare for, and predict, effects of emerging wildlife diseases.…”

Section: Introductionmentioning

confidence: 99%

Antibiotic perturbation of gut bacteria does not significantly alter host responses to ocular disease in a songbird species

Weitzman

Belden

May

et al. 2022

PeerJ

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Bacterial communities in and on wild hosts are increasingly appreciated for their importance in host health. Through both direct and indirect interactions, bacteria lining vertebrate gut mucosa provide hosts protection against infectious pathogens, sometimes even in distal body regions through immune regulation. In house finches (Haemorhous mexicanus), the bacterial pathogen Mycoplasma gallisepticum (MG) causes conjunctivitis, with ocular inflammation mediated by pro- and anti-inflammatory cytokines and infection triggering MG-specific antibodies. Here, we tested the role of gut bacteria in host responses to MG by using oral antibiotics to perturb bacteria in the gut of captive house finches prior to experimental inoculation with MG. We found no clear support for an impact of gut bacterial disruption on conjunctival pathology, MG load, or plasma antibody levels. However, there was a non-significant trend for birds with intact gut communities to have greater conjunctival pathology, suggesting a possible impact of gut bacteria on pro-inflammatory cytokine stimulation. Using 16S bacterial rRNA amplicon sequencing, we found dramatic differences in cloacal bacterial community composition between captive, wild-caught house finches in our experiment and free-living finches from the same population, with lower bacterial richness and core communities composed of fewer genera in captive finches. We hypothesize that captivity may have affected the strength of results in this experiment, necessitating further study with this consideration. The abundance of anthropogenic impacts on wildlife and their bacterial communities, alongside the emergence and spread of infectious diseases, highlights the importance of studies addressing the role of commensal bacteria in health and disease, and the consequences of gut bacterial shifts on wild hosts.

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“…One other group has undertaken a number of studies on the small mammal gut microbiome for animals in Chornobyl and, latterly, Fukushima (e.g. Lavrinienko et al, 2020; Lavrinienko, Hämäläinen, et al, 2021; Lavrinienko, Mappes, et al, 2018; Lavrinienko, Tukalenko, et al, 2018). Their studies have consistently identified associations between radiation and a response within the gut microbiome.…”

Section: Introductionmentioning

confidence: 99%

“…This has led to a number of studies on the impact of radiation on microbiomes within 'natural laboratories', such as the Chornobyl and Fukushima exclusion zones (e.g. Antwis et al, 2021;Lavrinienko, Hämäläinen, et al, 2021;Newbold et al, 2019;Videvall et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Some observations on meaningful and objective inference in radioecological field studies

Jackson

Antwis

Beresford

2022

Journal of Animal Ecology

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1. Anthropogenic releases of radiation are of ongoing importance for environmental protection, but the radiation doses at which natural systems begin to show effects are controversial. More certainty is required in this area to achieve optimal regulation for radioactive substances. We recently carried out a large survey (268 sampled animals and 20 sites) of the association between environmental radiation exposures and small mammal gut-associated microbiomes (fungal and bacterial) in the Chornobyl Exclusion zone (CEZ). Using individual measurements of total absorbed dose rates and a study design and analyses that accounted for spatial non-independence, we found no, or only limited, association.2. Watts et al. have criticised our study: for not filtering candidate non-resident components prior to our fungal microbiome analyses, for our qualified speculations on the relative merits of faecal and gut samples, and for the design of our study which they felt lacked sufficient replication.3. The advantage of filtering non-resident-fungal taxa is not clear and it would not have changed the null (spatially adjusted) association we found between radioactive dose and mycobiome composition because the most discriminatory fungal taxa with regard to dose were non-resident taxa.4. We maintain that it was legitimate for us to make qualified discussion comments on the differences in results between our faecal and gut microbiome analyses and on the relative merits of these sample types. 5. Most importantly, the criticism of our study design by Watts et al. and the designs and analysis of their recent studies in the CEZ show a misunderstanding of the true nature of independent replication in field studies. Recognising the importance of spatial non-independence is essential in the design and analysis of radioecological field surveys.

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Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 19 publications

References 94 publications

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

Antibiotic perturbation of gut bacteria does not significantly alter host responses to ocular disease in a songbird species

Some observations on meaningful and objective inference in radioecological field studies

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