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

Abstract 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 ef...

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Main Authors: Xue Yu, Rachel L. Hoyle, Fengguang Guo, Cameron M. Ratliff, Valentin Cantu, Justin Crow, Lixin Xiang, J. Jill Heatley, Guan Zhu
Format: Article
Language:English
Published: BMC 2019-03-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-019-3369-z
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author Xue Yu
Rachel L. Hoyle
Fengguang Guo
Cameron M. Ratliff
Valentin Cantu
Justin Crow
Lixin Xiang
J. Jill Heatley
Guan Zhu
author_facet Xue Yu
Rachel L. Hoyle
Fengguang Guo
Cameron M. Ratliff
Valentin Cantu
Justin Crow
Lixin Xiang
J. Jill Heatley
Guan Zhu
author_sort Xue Yu
collection DOAJ
description Abstract 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.
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spelling doaj.art-fcb738e9a9644969a714d231bef6bcd62022-12-22T03:18:22ZengBMCParasites & Vectors1756-33052019-03-0112111010.1186/s13071-019-3369-zA Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United StatesXue Yu0Rachel L. Hoyle1Fengguang Guo2Cameron M. Ratliff3Valentin Cantu4Justin Crow5Lixin Xiang6J. Jill Heatley7Guan Zhu8Department of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M UniversityDepartment of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M UniversityDepartment of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M UniversityDepartment of Veterinary Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical SciencesUnited States Fish and Wildlife Service, San Marcos Aquatic Resources CenterUnited States Fish and Wildlife Service, San Marcos Aquatic Resources CenterCollege of Life Sciences, Zhejiang UniversityDepartment of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M UniversityDepartment of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M UniversityAbstract 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.http://link.springer.com/article/10.1186/s13071-019-3369-zLungless salamandersEurycea sosorumEurycea nanaEndangered speciesMicrosporidiosisVavraia-like microsporidian
spellingShingle Xue Yu
Rachel L. Hoyle
Fengguang Guo
Cameron M. Ratliff
Valentin Cantu
Justin Crow
Lixin Xiang
J. Jill Heatley
Guan Zhu
A Vavraia-like microsporidium as the cause of deadly infection in threatened and endangered Eurycea salamanders in the United States
Parasites & Vectors
Lungless salamanders
Eurycea sosorum
Eurycea nana
Endangered species
Microsporidiosis
Vavraia-like microsporidian
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 Lungless salamanders
Eurycea sosorum
Eurycea nana
Endangered species
Microsporidiosis
Vavraia-like microsporidian
url http://link.springer.com/article/10.1186/s13071-019-3369-z
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