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A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States

BACKGROUND: Eurycea sosorum (Barton Springs salamander) and Eurycea nana (San Macros salamander) are listed as endangered and threatened species, respectively, by the U.S. Fish and Wildlife Service (USFWS) with habitats restricted to small regions near Austin, Texas, USA. The conservation efforts wi...

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Autores principales: Yu, Xue, Hoyle, Rachel L., Guo, Fengguang, Ratliff, Cameron M., Cantu, Valentin, Crow, Justin, Xiang, Lixin, Heatley, J. Jill, Zhu, Guan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6419446/
https://www.ncbi.nlm.nih.gov/pubmed/30871588
http://dx.doi.org/10.1186/s13071-019-3369-z
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author Yu, Xue
Hoyle, Rachel L.
Guo, Fengguang
Ratliff, Cameron M.
Cantu, Valentin
Crow, Justin
Xiang, Lixin
Heatley, J. Jill
Zhu, Guan
author_facet Yu, Xue
Hoyle, Rachel L.
Guo, Fengguang
Ratliff, Cameron M.
Cantu, Valentin
Crow, Justin
Xiang, Lixin
Heatley, J. Jill
Zhu, Guan
author_sort Yu, Xue
collection PubMed
description BACKGROUND: Eurycea sosorum (Barton Springs salamander) and Eurycea nana (San Macros salamander) are listed as endangered and threatened species, respectively, by the U.S. Fish and Wildlife Service (USFWS) with habitats restricted to small regions near Austin, Texas, USA. The conservation efforts with the Eurycea salamanders at the captive breeding program in San Marcos Aquatic Resources Center (SMARC), a USFWS facility, have seen an unexpected and increased mortality rate over the past few years. The clinical signs of sick or dead salamanders included erythema, tail loss, asymmetric gills or brachial loss, rhabdomyolysis, kyphosis, and behavior changes, suggesting that an infectious disease might be the culprit. This study aimed to identify the cause of the infection, determine the taxonomic position of the pathogen, and investigate the potential reservoirs of the pathogen in the environment. RESULTS: Histopathological examination indicated microsporidian infection (microsporidiosis) in the sick and dead Eurycea salamanders that was later confirmed by PCR detection. We also determined the near full-length small subunit ribosomal RNA (SSU rRNA) gene from the microsporidian pathogen, which allowed us to determine its phylogenetic position, and to design primers for specific and sensitive detection of the pathogen. Phylogenetic analysis indicated that this pathogen was closely related to the insect parasites Vavraia spp. and the human opportunistic pathogen, Trachipleistophora hominis. This Vavraia-like microsporidium was present in dead salamanders at SMARC archived between 2011 and 2015 (positive rates ranging between 52.0–88.9% by PCR detection), as well as in some aquatic invertebrates at the facility (e.g. snails and small crustaceans). CONCLUSIONS: A Vavraia-like microsporidian was at least one of the major pathogens, if not solely, responsible for the sickness and mortality in the SMARC salamanders, and the pathogen had been present in the center for years. Environmental invertebrates likely served as a source and reservoir of the microsporidian pathogen. These observations provide new knowledge and a foundation for future conservation efforts for Eurycea salamanders including molecular surveys, monitoring of the pathogen, and discovery of effective treatments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3369-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-64194462019-03-27 A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States Yu, Xue Hoyle, Rachel L. Guo, Fengguang Ratliff, Cameron M. Cantu, Valentin Crow, Justin Xiang, Lixin Heatley, J. Jill Zhu, Guan Parasit Vectors Research BACKGROUND: Eurycea sosorum (Barton Springs salamander) and Eurycea nana (San Macros salamander) are listed as endangered and threatened species, respectively, by the U.S. Fish and Wildlife Service (USFWS) with habitats restricted to small regions near Austin, Texas, USA. The conservation efforts with the Eurycea salamanders at the captive breeding program in San Marcos Aquatic Resources Center (SMARC), a USFWS facility, have seen an unexpected and increased mortality rate over the past few years. The clinical signs of sick or dead salamanders included erythema, tail loss, asymmetric gills or brachial loss, rhabdomyolysis, kyphosis, and behavior changes, suggesting that an infectious disease might be the culprit. This study aimed to identify the cause of the infection, determine the taxonomic position of the pathogen, and investigate the potential reservoirs of the pathogen in the environment. RESULTS: Histopathological examination indicated microsporidian infection (microsporidiosis) in the sick and dead Eurycea salamanders that was later confirmed by PCR detection. We also determined the near full-length small subunit ribosomal RNA (SSU rRNA) gene from the microsporidian pathogen, which allowed us to determine its phylogenetic position, and to design primers for specific and sensitive detection of the pathogen. Phylogenetic analysis indicated that this pathogen was closely related to the insect parasites Vavraia spp. and the human opportunistic pathogen, Trachipleistophora hominis. This Vavraia-like microsporidium was present in dead salamanders at SMARC archived between 2011 and 2015 (positive rates ranging between 52.0–88.9% by PCR detection), as well as in some aquatic invertebrates at the facility (e.g. snails and small crustaceans). CONCLUSIONS: A Vavraia-like microsporidian was at least one of the major pathogens, if not solely, responsible for the sickness and mortality in the SMARC salamanders, and the pathogen had been present in the center for years. Environmental invertebrates likely served as a source and reservoir of the microsporidian pathogen. These observations provide new knowledge and a foundation for future conservation efforts for Eurycea salamanders including molecular surveys, monitoring of the pathogen, and discovery of effective treatments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3369-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-14 /pmc/articles/PMC6419446/ /pubmed/30871588 http://dx.doi.org/10.1186/s13071-019-3369-z Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Yu, Xue
Hoyle, Rachel L.
Guo, Fengguang
Ratliff, Cameron M.
Cantu, Valentin
Crow, Justin
Xiang, Lixin
Heatley, J. Jill
Zhu, Guan
A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title_full A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title_fullStr A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title_full_unstemmed A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title_short A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
title_sort vavraia-like microsporidium as the cause of deadly infection in threatened and endangered eurycea salamanders in the united states
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6419446/
https://www.ncbi.nlm.nih.gov/pubmed/30871588
http://dx.doi.org/10.1186/s13071-019-3369-z
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