Pathogenic lineage of Perkinsea associated with mass mortality of frogs across the United States

Abstract

Emerging infectious diseases such as chytridiomycosis and ranavirus infections are important contributors to the worldwide decline of amphibian populations. We reviewed data on 247 anuran mortality events in 43 States of the United States from 1999–2015. Our findings suggest that a severe infectious disease of tadpoles caused by a protist belonging to the phylum Perkinsea might represent the third most common infectious disease of anurans after ranavirus infections and chytridiomycosis. Severe Perkinsea infections (SPI) were systemic and led to multiorganic failure and death. The SPI mortality events affected numerous anuran species and occurred over a broad geographic area, from boreal to subtropical habitats. Livers from all PCR-tested SPI-tadpoles (n = 19) were positive for the Novel Alveolate Group 01 (NAG01) of Perkinsea, while only 2.5% histologically normal tadpole livers tested positive (2/81), suggesting that subclinical infections are uncommon. Phylogenetic analysis demonstrated that SPI is associated with a phylogenetically distinct clade of NAG01 Perkinsea. These data suggest that this virulent Perkinsea clade is an important pathogen of frogs in the United States. Given its association with mortality events and tendency to be overlooked, the potential role of this emerging pathogen in amphibian declines on a broad geographic scale warrants further investigation.

Diverse alveolate infections of tadpoles, a new threat to frogs?

“…In 2007, Davis and colleagues reported a large-scale mortality event in a population of Southern leopard frog tadpoles (Lithobates sphenocephalus) in a pond in Northeast Georgia, United States of America (USA) [4]. Infected tadpoles demonstrated lethargic swimming with recurrent abnormalities, including abdominal distension, subcutaneous oedema, cutaneous erythema and petechia, or patchy pale discoloration of the skin [4,16]. High densities of an initially unknown protist within the liver tissues ( Fig 2B) were observed.…”

“…The agent of severe Perkinsozoa infection has been primarily identified in tadpoles, although there are some reports of infection in adults [18]. Infection by Perkinsozoa is now considered an emerging disease and has been implied as responsible for die-offs of tadpoles throughout the USA, including populations of endangered species [4,16]. Using a targeted 18S rRNA approach, it has been demonstrated that additional diverse members of the freshwater Perkinsozoa clade, named "pathogenic Perkinsea clade" [16] or "novel alveolate group 01," [17] can be detected from liver tissues from a wide diversity of Neobatrachia tadpoles and a range of disparate geographic locations.…”

“…Infection by Perkinsozoa is now considered an emerging disease and has been implied as responsible for die-offs of tadpoles throughout the USA, including populations of endangered species [4,16]. Using a targeted 18S rRNA approach, it has been demonstrated that additional diverse members of the freshwater Perkinsozoa clade, named "pathogenic Perkinsea clade" [16] or "novel alveolate group 01," [17] can be detected from liver tissues from a wide diversity of Neobatrachia tadpoles and a range of disparate geographic locations. However, the relationship between disease and infection in this group is poorly established, and it is not yet clear if only the subclade that has been associated with mortality events across the USA is a disease-causing emerging parasite or whether the wider clade detected [16,17] is also associated with a cryptic disease.…”

When Micro Drives the Macro: A Fresh Look at Disease and its Massive Contributions in the Hindu Kush-Himalaya

“…Among these underlying factors, the role of ms is critical because they may induce immediate and rapid mass mortality of MS leading susceptibility to endangerment and extinction (Field et al 2009;Fey et al 2015;González-Suárez and Revilla 2014;Smith et al 2006;Pedersen et al 2007;Adams et al 2017). For example, mass elimination of Mongolian saigas by Peste des Petits Virus (PPRV) (Chimeddorj and Buuveibaatar 2017), of amphibian populations by Ranavirus, Batrachochytrium dendrobatidis, and Perkinsea (Fey et al 2015;Cheng et al 2011;Duffus et al 2015;Isidoro-Ayza et al 2017;Kwon et al 2017;Geng et al 2011), and of humans and animals by TB, influenza, acute respiratory, and diarrheal pathogens has been already reported around the world (NRC 1993;Gates 2014;DoAH 2016b;DoHS 2017). In these contexts, although several causes might exist, extreme virulence, toxicity, and the pathogenicity of the pathogens actually govern the disease appearance and outbreaks.…”

Concurrent Infection of Batrachochytrium dendrobatidis and Ranavirus among Native Amphibians from Northeastern Oklahoma, USA

“…Furthermore, a recent study of 247 wild anuran mortality events that were documented in North America between 2009 and 2015 found RV to be the cause of 92 events (37%), whereas 50 mortality events (20%) were linked to Bd (Isidoro‐Ayza et al. ).…”