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      Captivity and Infection by the Fungal Pathogen Batrachochytrium salamandrivorans Perturb the Amphibian Skin Microbiome

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          Abstract

          The emerging fungal pathogen, Batrachochytrium salamandrivorans ( Bsal) is responsible for the catastrophic decline of European salamanders and poses a threat to amphibians globally. The amphibian skin microbiome can influence disease outcome for several host-pathogen systems, yet little is known of its role in Bsal infection. In addition, many experimental in-vivo amphibian disease studies to date have relied on specimens that have been kept in captivity for long periods without considering the influence of environment on the microbiome and how this may impact the host response to pathogen exposure. We characterized the impact of captivity and exposure to Bsal on the skin bacterial and fungal communities of two co-occurring European newt species, the smooth newt, Lissotriton vulgaris and the great-crested newt, Triturus cristatus. We show that captivity led to significant losses in bacterial and fungal diversity of amphibian skin, which may be indicative of a decline in microbe-mediated protection. We further demonstrate that in both L. vulgaris and T. cristatus, Bsal infection was associated with changes in the composition of skin bacterial communities with possible negative consequences to host health. Our findings advance current understanding of the role of host-associated microbiota in Bsal infection and highlight important considerations for ex-situ amphibian conservation programmes.

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          Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

          Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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            Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host.

            Batrachochytrium dendrobatidis (Bd) is a chytrid fungus that causes chytridiomycosis in amphibians. Only named in 1999, Bd is a proximate driver of declines in global amphibian biodiversity. The pathogen infects over 350 species of amphibians and is found on all continents except Antarctica. However, the processes that have led to the global distribution of Bd and the occurrence of chytridiomycosis remain unclear. This review explores the molecular, epidemiological, and ecological evidence that Bd evolved from an endemic ancestral lineage to achieve global prominence via anthropogenically mediated spread. We then consider the major host and pathogen factors that have led to the occurrence of chytridiomycosis in amphibian species, populations, and communities.
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              Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians.

              The current biodiversity crisis encompasses a sixth mass extinction event affecting the entire class of amphibians. The infectious disease chytridiomycosis is considered one of the major drivers of global amphibian population decline and extinction and is thought to be caused by a single species of aquatic fungus, Batrachochytrium dendrobatidis. However, several amphibian population declines remain unexplained, among them a steep decrease in fire salamander populations (Salamandra salamandra) that has brought this species to the edge of local extinction. Here we isolated and characterized a unique chytrid fungus, Batrachochytrium salamandrivorans sp. nov., from this salamander population. This chytrid causes erosive skin disease and rapid mortality in experimentally infected fire salamanders and was present in skin lesions of salamanders found dead during the decline event. Together with the closely related B. dendrobatidis, this taxon forms a well-supported chytridiomycete clade, adapted to vertebrate hosts and highly pathogenic to amphibians. However, the lower thermal growth preference of B. salamandrivorans, compared with B. dendrobatidis, and resistance of midwife toads (Alytes obstetricans) to experimental infection with B. salamandrivorans suggest differential niche occupation of the two chytrid fungi.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                23 August 2019
                2019
                : 10
                : 1834
                Affiliations
                [1] 1Department of Zoology, University of Oxford , Oxford, United Kingdom
                [2] 2Department of Infectious Disease Epidemiology, MRC Centre for Global Infectious Disease Analysis, School of Public Health, Imperial College London , London, United Kingdom
                [3] 3Institute of Zoology, Zoological Society of London , London, United Kingdom
                [4] 4College of Life and Environmental Sciences, University of Exeter , Exeter, United Kingdom
                [5] 5Department of Zoology, University of Cambridge , Cambridge, United Kingdom
                [6] 6Froglife , Peterborough, United Kingdom
                Author notes

                Edited by: Amparo Latorre, University of Valencia, Spain

                Reviewed by: Suleyman Yildirim, Istanbul Medipol University, Turkey; Raul Cabrera-Rubio, Teagasc, The Irish Agriculture and Food Development Authority, Ireland

                *Correspondence: Kieran A. Bates kieran.bates@ 123456zoo.ox.ac.uk

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                †These authors have contributed equally to this work

                Article
                10.3389/fmicb.2019.01834
                6716147
                31507541
                dae990b2-0bcc-44c7-875d-05306ffdb443
                Copyright © 2019 Bates, Shelton, Mercier, Hopkins, Harrison, Petrovan and Fisher.

                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.

                History
                : 24 May 2019
                : 25 July 2019
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 69, Pages: 13, Words: 9751
                Funding
                Funded by: Leverhulme Trust 10.13039/501100000275
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                batrachochytrium salamandrivorans,chytridiomycosis,microbiome,microbial ecology,amphibian

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