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Phenotypic Divergence along Geographic Gradients Reveals Potential for Rapid Adaptation of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans, in North America.

ABSTRACT: White-nose syndrome (WNS) is an ongoing epizootic affecting multiple species of North American bats, caused by epidermal infections of the psychrophilic filamentous fungus Pseudogymnoascus destructans Since its introduction from Europe, WNS has spread rapidly across eastern North America and resulted in high mortality rates in bats. At present, the mechanisms behind its spread and the extent of its adaptation to different geographic and ecological niches remain unknown. The objective of this study was to examine the geographic patterns of phenotypic variation and the potential evidence for adaptation among strains representing broad geographic locations in eastern North America. The morphological features of these strains were evaluated on artificial medium, and the viability of asexual arthroconidia of representative strains was investigated after storage at high (23°C), moderate (14°C), and low (4°C) temperatures at different lengths of time. Our analyses identified evidence for a geographic pattern of colony morphology changes among the clonal descendants of the fungus, with trait values correlated with increased distance from the epicenter of WNS. Our genomic comparisons of three representative isolates revealed novel genetic polymorphisms and suggested potential candidate mutations that might be related to some of the phenotypic changes. These results show that even though this pathogen arrived in North America only recently and reproduces asexually, there has been substantial evolution and phenotypic diversification during its rapid clonal expansion.IMPORTANCE The causal agent of white-nose syndrome in bats is Pseudogymnoascus destructans, a filamentous fungus recently introduced from its native range in Europe. Infections caused by P. destructans have progressed across the eastern parts of Canada and the United States over the last 10 years. It is not clear how the disease is spread, as the pathogen is unable to grow above 23°C and ambient temperature can act as a barrier when hosts disperse. Here, we explore the patterns of phenotypic diversity and the germination of the fungal asexual spores, arthroconidia, from strains across a sizeable area of the epizootic range. Our analyses revealed evidence of adaptation along geographic gradients during its expansion. The results have implications for understanding the diversification of P. destructans and the limits of WNS spread in North America. Given the rapidly expanding distribution of WNS, a detailed understanding of the genetic bases for phenotypic variations in growth, reproduction, and dispersal of P. destructans is urgently needed to help control this disease.

SUBMITTER: Forsythe A

PROVIDER: S-EPMC6070747 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Phenotypic Divergence along Geographic Gradients Reveals Potential for Rapid Adaptation of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans, in North America.

Forsythe Adrian A Giglio Victoria V Asa Jonathan J Xu Jianping J

Applied and environmental microbiology 20180801 16

White-nose syndrome (WNS) is an ongoing epizootic affecting multiple species of North American bats, caused by epidermal infections of the psychrophilic filamentous fungus <i>Pseudogymnoascus destructans</i> Since its introduction from Europe, WNS has spread rapidly across eastern North America and resulted in high mortality rates in bats. At present, the mechanisms behind its spread and the extent of its adaptation to different geographic and ecological niches remain unknown. The objective of t ...[more]

PMID: 29915107

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Project description: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.

Project description:White-nose syndrome (WNS) is causing significant declines in populations of North American hibernating bats, and recent western and southern expansions of the disease have placed additional species at risk. Understanding differences in species susceptibility and identifying management actions to reduce mortality of bats from WNS are top research priorities. However, the use of wild-caught susceptible bats, such as Myotis lucifugus, as model species for WNS research is problematic and places additional pressure on remnant populations. We investigated the feasibility of using Tadarida brasiliensis, a highly abundant species of bat that tolerates captivity, as the basis for an experimental animal model for WNS. Using methods previously established to confirm the etiology of WNS in M. lucifugus, we experimentally infected 11 T. brasiliensis bats with Pseudogymnoascus destructans in the laboratory under conditions that induced hibernation. We detected P. destructans on all 11 experimentally infected bats, 7 of which exhibited localized proliferation of hyphae within the epidermis, dermis, and subcutaneous tissue, similar to invasive cutaneous ascomycosis observed in M. lucifugus bats with WNS. However, the distribution of lesions across wing membranes of T. brasiliensis bats was limited, and only one discrete "cupping erosion," diagnostic for WNS, was identified. Thus, the rarity of lesions definitive for WNS suggests that T. brasiliensis does not likely represent an appropriate model for studying the pathophysiology of this disease. Nonetheless, the results of this study prompt questions concerning the potential for free-ranging, migratory T. brasiliensis bats to become infected with P. destructans and move the fungal pathogen between roost sites used by species susceptible to WNS.IMPORTANCE White-nose syndrome (WNS) is a fungal disease that is causing severe declines of bat populations in North America. Identifying ways to reduce the impacts of this disease is a priority but is inhibited by the lack of an experimental animal model that does not require the use of wild-caught bat species already impacted by WNS. We tested whether Tadarida brasiliensis, one of the most abundant species of bats in the Americas, could serve as a suitable animal model for WNS research. While T. brasiliensis bats were susceptible to experimental infection with the fungus under conditions that induced hibernation, the species exhibited limited pathology diagnostic for WNS. These results indicate that T. brasiliensis is not likely a suitable experimental model for WNS research. However, the recovery of viable WNS-causing fungus from experimentally infected bats indicates a potential for this species to contribute to the spread of the pathogen where it coexists with other species of bats affected by WNS.

Dataset Information

Phenotypic Divergence along Geographic Gradients Reveals Potential for Rapid Adaptation of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans, in North America.

Publications

Phenotypic Divergence along Geographic Gradients Reveals Potential for Rapid Adaptation of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans, in North America.

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