Phylogeographic analysis of Pseudogymnoascus destructans partitivirus-pa explains the spread dynamics of white-nose syndrome in North America

Abstract

Understanding the dynamics of white-nose syndrome spread in time and space is an important component for the disease epidemiology and control. We reported earlier that a novel partitivirus, Pseudogymnoascus destructans partitivirus-pa, had infected the North American isolates of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats. We showed that the diversity of the viral coat protein sequences is correlated to their geographical origin. Here we hypothesize that the geographical adaptation of the virus could be used as a proxy to characterize the spread of white-nose syndrome. We used over 100 virus isolates from diverse locations in North America and applied the phylogeographic analysis tool BEAST to characterize the spread of the disease. The strict clock phylogeographic analysis under the coalescent model in BEAST showed a patchy spread pattern of white-nose syndrome driven from a few source locations including Connecticut, New York, West Virginia, and Kentucky. The source states had significant support in the maximum clade credibility tree and Bayesian stochastic search variable selection analysis. Although the geographic origin of the virus is not definite, it is likely the virus infected the fungus prior to the spread of white-nose syndrome in North America. We also inferred from the BEAST analysis that the recent long-distance spread of the fungus to Washington had its root in Kentucky, likely from the Mammoth cave area and most probably mediated by a human. The time to the most recent common ancestor of the virus is estimated somewhere between the late 1990s to early 2000s. We found the mean substitution rate of 2 X 10−3 substitutions per site per year for the virus which is higher than expected given the persistent lifestyle of the virus, and the stamping-machine mode of replication. Our approach of using the virus as a proxy to understand the spread of white-nose syndrome could be an important tool for the study and management of other infectious diseases.

Bat white-nose disease fungus diversity in time and space

“…Besides, due to the founder effect, whereby genetic richness in the invasive population of a species is reduced due to the introduction of a single or just a few individuals, genetic diversity of P. destructans in North America is magnitudes lower in comparison to Eurasia ( Drees et al 2017a ), which reduces the power of genetic markers to detect population differentiation at such short timescales. To overcome this issue, Thapa et al (2021) used the fast-evolving mycovirus PdPV-pa as a proxy to infer the P. destructans population structure and found very strong differentiation across the studied region in North America. Although there are different factors that can decouple the mycovirus (PdPV-pa) population structure from its host ( P. destructans ) population structure ( Mazé-Guilmo et al 2016 ), the specificities of the current system point towards a situation where both structures should be correlated.…”

“…Although there are different factors that can decouple the mycovirus (PdPV-pa) population structure from its host ( P. destructans ) population structure ( Mazé-Guilmo et al 2016 ), the specificities of the current system point towards a situation where both structures should be correlated. Indeed, PdPV-pa seems to specifically infect P. destructans ( Ren et al 2020 ), all North-American P. destructans isolates seem to be infected with PdPV-pa ( Thapa et al 2016 , Ren et al 2020 , Thapa et al 2021 ) and mycoviruses lack an extracellular life stage and are transmitted only through cell division, sporulation or cell fusion ( Pearson et al 2009 , Son et al 2015 , Kotta-Loizou 2021 ). Taken together, these studies ( Thapa et al 2021 , Fischer et al 2022 ; the present study) strongly suggest that once P. destructans populations have established, the successful establishment of newly-arrived pathogen MLGs is rare in comparison to in situ recruitment (see also Fischer et al 2022 ).…”

Could White-Nose Syndrome Manifest Differently in Myotis Lucifugus in Western Versus Eastern Regions of North America? A Review of Factors

“…White-nose syndrome was first documented in King County, Washington, US, in 2016, although models based on the symbiotic virus associated with Pd suggest the fungus was probably introduced to Washington in 2014 (Thapa et al 2021). As of July 2021, 7 yr later, 163 additional confirmed cases of Pd or WNS had been documented in 7/39 Washington counties (Fig.…”

Gaussian process forecasts Pseudogymnoascus destructans will cover coterminous United States by 2030

“…Wilder et al ( 2015 ) modeled risk of infection among little brown bat Myotis lucifugus hibernacula using both geographic proximity and genetic similarity, finding genetic distance improved model fit. Also using genetic data, Thapa et al ( 2021 ) conducted an illuminating phylogeographic analysis on the coat proteins of a partitivirus infecting Pd to characterize the spread of WNS across North America. Results trace most infections to a few source locations, including New York, Connecticut, West Virginia, and Kentucky; Thapa et al ( 2021 ) asserted the long‐distance spread to Washington was possibly a human‐mediated transmission from the Mammoth Cave region in Kentucky.…”