Post-epizootic microbiome associations across communities of neotropical amphibians

Phillip Jervis*, Pol Pintanel, Kevin Hopkins, Claudia Wierzbicki, Jennifer M.G. Shelton, Emily Skelly, Gonçalo M. Rosa, Diego Almeida-Reinoso, Maria Eugenia-Ordoñez, Santiago Ron, Xavier Harrison, Andrés Merino-Viteri, Matthew C. Fisher

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Microbiome–pathogen interactions are increasingly recognized as an important element of host immunity. While these host-level interactions will have consequences for community disease dynamics, the factors which influence host microbiomes at larger scales are poorly understood. We here describe landscape-scale pathogen–microbiome associations within the context of post-epizootic amphibian chytridiomycosis, a disease caused by the panzootic chytrid fungus Batrachochytrium dendrobatidis. We undertook a survey of Neotropical amphibians across altitudinal gradients in Ecuador ~30 years following the observed amphibian declines and collected skin swab-samples which were metabarcoded using both fungal (ITS-2) and bacterial (r16S) amplicons. The data revealed marked variation in patterns of both B. dendrobatidis infection and microbiome structure that are associated with host life history. Stream breeding amphibians were most likely to be infected with B. dendrobatidis. This increased probability of infection was further associated with increased abundance and diversity of non-Batrachochytrium chytrid fungi in the skin and environmental microbiome. We also show that increased alpha diversity and the relative abundance of fungi are lower in the skin microbiome of adult stream amphibians compared to adult pond-breeding amphibians, an association not seen for bacteria. Finally, stream tadpoles exhibit lower proportions of predicted protective microbial taxa than pond tadpoles, suggesting reduced biotic resistance. Our analyses show that host breeding ecology strongly shapes pathogen–microbiome associations at a landscape scale, a trait that may influence resilience in the face of emerging infectious diseases.

Original languageEnglish
Pages (from-to)1322-1335
Number of pages14
JournalMolecular Ecology
Volume30
Issue number5
DOIs
StatePublished - 7 Jan 2021

Bibliographical note

Publisher Copyright:
© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Funding

We thank Diego Paucar, Freddy Almeida, Paulina Romero, Ricardo Gavilanes, Sofia Salinas, Xiomara Izuereta and Stephen Hopkins for assisting with fieldwork. We thank Dr Mark Wilkinson (Natural History Museum, London) for confirming the identity of caecilians sampled during fieldwork. Sample collection was carried out under Framework Contract for Access to Genetic Resources No. MAE‐DNB‐CM‐2015‐0039 issued by the Ministry of Environment of Ecuador (MAE) to M.E.O. An Export Permit for Scientific Research (No. 30‐2017‐EXP‐CM‐2016‐DNB/MA) issued by MAE allowed the samples to reach Imperial College of London, in the UK. M.C.F. acknowledges support from NERC (NE/E006701/1, NE/E006841/1, NE/G002193/1, NE/K014455/1, NE/K012 509/1, NE/M000591/1, NE/N009800/1, NE/N009967/1, NE/S000844/1, NE/S000992/1), The Morris Animal Foundation (D12ZO‐002 and D16ZO‐022) and the Leverhulme Trust (RPG‐2014‐273). M.C.F. is a Fellow in the CIFAR “Fungal Kingdom” programme. P.J. acknowledges support from the Natural Environment Research Council (NE/L002515/1) and the Science and Solutions for a Changing Planet DTP, Grantham Institute, Imperial College London. The Imperial BRC Genomics Facility has provided resources and support that have contributed to the research results reported within this paper. The Imperial BRC Genomics Facility is supported by NIHR funding to the Imperial Biomedical Research Centre. We thank Diego Paucar, Freddy Almeida, Paulina Romero, Ricardo Gavilanes, Sofia Salinas, Xiomara Izuereta and Stephen Hopkins for assisting with fieldwork. We thank Dr Mark Wilkinson (Natural History Museum, London) for confirming the identity of caecilians sampled during fieldwork. Sample collection was carried out under Framework Contract for Access to Genetic Resources No. MAE-DNB-CM-2015-0039 issued by the Ministry of Environment of Ecuador (MAE) to M.E.O. An Export Permit for Scientific Research (No. 30-2017-EXP-CM-2016-DNB/MA) issued by MAE allowed the samples to reach Imperial College of London, in the UK. M.C.F. acknowledges support from NERC (NE/E006701/1, NE/E006841/1, NE/G002193/1, NE/K014455/1, NE/K012 509/1, NE/M000591/1, NE/N009800/1, NE/N009967/1, NE/S000844/1, NE/S000992/1), The Morris Animal Foundation (D12ZO-002 and D16ZO-022) and the Leverhulme Trust (RPG-2014-273). M.C.F. is a Fellow in the CIFAR ?Fungal Kingdom? programme. P.J. acknowledges support from the Natural Environment Research Council (NE/L002515/1) and the Science and Solutions for a Changing Planet DTP, Grantham Institute, Imperial College London. The Imperial BRC Genomics Facility has provided resources and support that have contributed to the research results reported within this paper. The Imperial BRC Genomics Facility is supported by NIHR funding to the Imperial Biomedical Research Centre.

FundersFunder number
MAE
Ministry of Environment of Ecuador30-2017-EXP-CM-2016-DNB/MA
Morris Animal FoundationD12ZO‐002, D16ZO‐022
Natural Environment Research CouncilNE/M000591/1, NE/G002193/1, NE/L002515/1, NE/S000992/1, NE/E006841/1, NE/N009967/1, NE/E006701/1, NE/N009800/1, NE/K014455/1, NE/K012 509/1, NE/S000844/1
National Institute for Health Research
Leverhulme TrustRPG‐2014‐273
NIHR Imperial Biomedical Research Centre

    Keywords

    • B. dendrobatidis
    • Batrachochytrium
    • Darwin's naturalisation conundrum
    • chytridiomycosis
    • endemic
    • enzootic
    • invasive pathogen

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