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

ABSTRACTWhite-nose syndrome (WNS) is an ongoing epizootic affecting multiple species of North American bats, caused by epidermal infections of the psychrophilic filamentous fungusPseudogymnoascus 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.IMPORTANCEThe causal agent of white-nose syndrome in bats isPseudogymnoascus destructans, a filamentous fungus recently introduced from its native range in Europe. Infections caused byP. destructanshave 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 ofP. destructansand 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 ofP. destructansis urgently needed to help control this disease.

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Distribution and Environmental Persistence of the Causative Agent of White-Nose Syndrome, Geomyces destructans, in Bat Hibernacula of the Eastern United States

Applied and Environmental Microbiology ◽

10.1128/aem.02939-12 ◽

2012 ◽

Vol 79 (4) ◽

pp. 1293-1301 ◽

Cited By ~ 91

Author(s):

Jeffrey M. Lorch ◽

Laura K. Muller ◽

Robin E. Russell ◽

Michael O'Connor ◽

Daniel L. Lindner ◽

...

Keyword(s):

United States ◽

North America ◽

Late Summer ◽

The United States ◽

Culture Technique ◽

Eastern United States ◽

Content Type ◽

Geomyces Destructans ◽

Sediment Samples ◽

White Nose Syndrome

ABSTRACTWhite-nose syndrome (WNS) is an emerging disease of hibernating bats caused by the recently described fungusGeomyces destructans. First isolated in 2008, the origins of this fungus in North America and its ability to persist in the environment remain undefined. To investigate the correlation between manifestation of WNS and distribution ofG. destructansin the United States, we analyzed sediment samples collected from 55 bat hibernacula (caves and mines) both within and outside the known range of WNS using a newly developed real-time PCR assay.Geomyces destructanswas detected in 17 of 21 sites within the known range of WNS at the time when the samples were collected; the fungus was not found in 28 sites beyond the known range of the disease at the time when environmental samples were collected. These data indicate that the distribution ofG. destructansis correlated with disease in hibernating bats and support the hypothesis that the fungus is likely an exotic species in North America. Additionally, we examined whetherG. destructanspersists in infested bat hibernacula when bats are absent. Sediment samples were collected from 14 WNS-positive hibernacula, and the samples were screened for viable fungus by using a culture technique. ViableG. destructanswas cultivated from 7 of the 14 sites sampled during late summer, when bats were no longer in hibernation, suggesting that the fungus can persist in the environment in the absence of bat hosts for long periods of time.

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Worldwide recombination in emergent white-nose syndrome pathogen Pseudogymnoascus destructans

10.1101/868331 ◽

2019 ◽

Author(s):

Lav Sharma ◽

Márcia Sousa ◽

Ana S. Faria ◽

Margarida Nunes-Pereira ◽

João A. Cabral ◽

...

Keyword(s):

Linkage Disequilibrium ◽

North America ◽

Genetic Recombination ◽

The United States ◽

Mating Types ◽

Linkage Disequilibrium Analysis ◽

Pseudogymnoascus Destructans ◽

White Nose Syndrome ◽

The North ◽

Single Mating

AbstractPseudogymnoascus destructans (Pd), the emergent fungus causing bat “White-Nose Syndrome”, responsible for ∼6 million mortalities in the United States (US), is thought to expand clonally in North America and Europe. Presence of distinct mating-types in Europe led to numerous research attempts searching for population sexuality worldwide. This study not only presents the first evidence of genetic recombination in Pd but also detects recombination in Pd genotype data generated by previous studies in Europe and North America, through clone-corrected linkage disequilibrium analysis. Portuguese and other European populations are apparently reproducing through sex between two mating-types. Seeming parasexual recombination in the invasive single mating-type US population rings alarms for the North American bat populations and deserves urgent attention. This study emphasizes on clone-correction in linkage disequilibrium analysis.One Sentence SummaryClone-correction yielded signs of elusive recombination in the global “clonal” populations of white-nose syndrome pathogen.

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Highly Sensitive Quantitative PCR for the Detection and Differentiation of Pseudogymnoascus destructans and Other Pseudogymnoascus Species

Applied and Environmental Microbiology ◽

10.1128/aem.02897-13 ◽

2013 ◽

Vol 80 (5) ◽

pp. 1726-1731 ◽

Cited By ~ 28

Author(s):

Megan M. Shuey ◽

Kevin P. Drees ◽

Daniel L. Lindner ◽

Paul Keim ◽

Jeffrey T. Foster

Keyword(s):

North America ◽

Quantitative Pcr ◽

Environmental Samples ◽

Etiologic Agent ◽

Pseudogymnoascus Destructans ◽

Content Type ◽

Real Time Quantitative Pcr ◽

White Nose Syndrome ◽

Highly Sensitive ◽

Management Plans

ABSTRACTWhite-nose syndrome is a fungal disease that has decimated bat populations across eastern North America. Identification of the etiologic agent,Pseudogymnoascus destructans(formerlyGeomyces destructans), in environmental samples is essential to proposed management plans. A major challenge is the presence of closely related species, which are ubiquitous in many soils and cave sediments and often present in high abundance. We present a dual-probe real-time quantitative PCR assay capable of detecting and differentiatingP. destructansfrom closely related fungi in environmental samples from North America. The assay, based on a single nucleotide polymorphism (SNP) specific toP. destructans, is capable of rapid low-level detection from various sampling media, including sediment, fecal samples, wing biopsy specimens, and skin swabs. This method is a highly sensitive, high-throughput method for identifyingP. destructans, otherPseudogymnoascusspp., andGeomycesspp. in the environment, providing a fundamental component of research and risk assessment for addressing this disease, as well as other ecological and mycological work on related fungi.

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Spatial spread of white-nose syndrome in North America, 2006-2018

10.1101/2021.01.28.428526 ◽

2021 ◽

Author(s):

Andrew M. Kramer ◽

Alex Mercier ◽

Sean Maher ◽

Yaw Kumi-Ansu ◽

Sarah Bowden ◽

...

Keyword(s):

Species Richness ◽

North America ◽

Pathogenic Fungus ◽

The United States ◽

Pseudogymnoascus Destructans ◽

Wildlife Diseases ◽

Spatial Spread ◽

White Nose Syndrome ◽

Total Species Richness ◽

Over Time

AbstractWhite-nose syndrome has caused massive mortality in multiple bat species and spread across much of North America, making it one of the most destructive wildlife diseases on record. This has also resulted in it being one of the most well-documented wildlife disease outbreaks, making it possible to look for changes in the pattern of spatial spread over time. We fit a series of spatial interaction models to the United States county-level observations of the pathogenic fungus, Pseudogymnoascus destructans, that causes white-nose syndrome. Models included the distance between caves, cave abundance, measures of winter length and winter onset, and species richness of all bats and hibernating bats only. We found that the best supported models included all of these factors, but that the particular structure and most informative covariates changed over the course of the outbreak, with winter length displacing winter onset as the most informative measure of winter conditions, and evidence for the effects total species richness and hibernation varying from year to year. We also found that weather had detectable effects on spread. While the effect sizes for cave abundance and species richness were relatively stable over the length of the outbreak, distance became less important as time went on. These findings indicate that although models produced early in the outbreak captured important and consistent aspects of the spatial spread of white-nose syndrome, there were also changes over time in the factors associated with spread, suggesting that forecasts may be improved by iterative model refinement.

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Breaching Pathogeographic Barriers by the Bat White-Nose Fungus

mBio ◽

10.1128/mbio.00897-18 ◽

2018 ◽

Vol 9 (3) ◽

Author(s):

Johanna Rhodes ◽

Matthew C. Fisher

Keyword(s):

Fungal Pathogens ◽

Experimental Infection ofTadarida brasiliensiswithPseudogymnoascus destructans, the Fungus That Causes White-Nose Syndrome

mSphere ◽

10.1128/msphere.00250-18 ◽

2018 ◽

Vol 3 (4) ◽

Author(s):

Michelle L. Verant ◽

Carol U. Meteyer ◽

Benjamin Stading ◽

David S. Blehert

Keyword(s):

Animal Model ◽

Experimental Animal ◽

Experimental Infection ◽

Abundant Species ◽

Experimental Animal Model ◽

Pseudogymnoascus Destructans ◽

Tadarida Brasiliensis ◽

Content Type ◽

White Nose Syndrome ◽

Management Actions

ABSTRACTWhite-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 asMyotis lucifugus, as model species for WNS research is problematic and places additional pressure on remnant populations. We investigated the feasibility of usingTadarida 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 inM. lucifugus, we experimentally infected 11T. brasiliensisbats withPseudogymnoascus destructansin the laboratory under conditions that induced hibernation. We detectedP. destructanson 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 inM. lucifugusbats with WNS. However, the distribution of lesions across wing membranes ofT. brasiliensisbats was limited, and only one discrete “cupping erosion,” diagnostic for WNS, was identified. Thus, the rarity of lesions definitive for WNS suggests thatT. brasiliensisdoes 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, migratoryT. brasiliensisbats to become infected withP. destructansand move the fungal pathogen between roost sites used by species susceptible to WNS.IMPORTANCEWhite-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 whetherTadarida brasiliensis, one of the most abundant species of bats in the Americas, could serve as a suitable animal model for WNS research. WhileT. brasiliensisbats were susceptible to experimental infection with the fungus under conditions that induced hibernation, the species exhibited limited pathology diagnostic for WNS. These results indicate thatT. brasiliensisis 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.

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A comparison of earthquake damage areas as a function of magnitude across the United States

Bulletin of the Seismological Society of America ◽

10.1785/bssa0830041064 ◽

1993 ◽

Vol 83 (4) ◽

pp. 1064-1080 ◽

Cited By ~ 4

Author(s):

G. A. Bollinger ◽

M. C. Chapman ◽

M. S. Sibol

Keyword(s):

United States ◽

North America ◽

Ground Motion ◽

Epicentral Distance ◽

The United States ◽

Western United States ◽

Eastern North America ◽

Similar Response ◽

Eastern United States ◽

The West

Abstract This study investigates the relationship between earthquake magnitude and the size of damage areas in the eastern and western United States. To quantify damage area as a function of moment magnitude (M), 149 MMI VI and VII areas for 109 earthquakes (88 in the western United States, 21 in the eastern United States and Canada) were measured. Regression of isoseismal areas versus M indicated that areas in the East were larger than those in the West, at both intensity levels, by an average 5 × in the M 4.5 to 7.5 range. In terms of radii for circles of equivalent area, these results indicate that damaging ground motion from shocks of the same magnitude extend 2 × the epicentral distance in eastern North America compared to the West. To determine source and site parameters consistent with the above results, response spectral levels for eastern North America were stochastically simulated and compared with response spectral ordinates derived from recorded strong ground motion data in the western United States. Stress-drop values of 200 bars, combined with a surficial 2-km-thick low velocity “sedimentary” layer over rock basement, produced results that are compatible with the intensity observations, i.e., similar response spectral levels in the east at approximately twice their epicentral distance in the western U.S. distance. These results suggest that ground motion modeling in eastern North America may need to incorporate source and site parameters different from those presently in general use. The results are also of importance to eastern U.S. hazard assessments as they require allowance for the larger damage areas in preparedness and mitigation programs.

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Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland

Open Life Sciences ◽

10.2478/s11535-013-0280-z ◽

2014 ◽

Vol 9 (4) ◽

pp. 437-443 ◽

Cited By ~ 1

Author(s):

Konrad Sachanowicz ◽

Arkadiusz Stępień ◽

Mateusz Ciechanowski

Keyword(s):

North America ◽

Mass Mortality ◽

Parasitic Fungus ◽

Pseudogymnoascus Destructans ◽

Southern Poland ◽

White Nose Syndrome ◽

Two Samples ◽

Myotis Myotis ◽

Myotis Daubentonii ◽

Fungal Dna

AbstractPseudogymnoascus destructans (Pd), a parasitic fungus (being responsible for a disease known as white-nose syndrome, WNS) that caused mass mortality of cave-dwelling, hibernating bats in North America, appears to be native of Europe, where it also occurs on wintering bats, but no similar outbreaks of WNS have been recorded. Herein, we provide the first account on prevalence and phenology of P. destructans in Poland. Bats were counted once per month, from October or January to May (2010-2013), in an abandoned ore mine in southern Poland. Presence of P. destructans in two samples was confirmed by sequencing of isolated fungal DNA. Observations of phenotypically identical mycosis on bats hibernating at this site in March 2006 are likely to be the first known records of P. destructans from Poland. All Pd-suspected individuals were Myotis myotis with an exception of one Myotis daubentonii. The first Pd-suspected bats were noted in mid-February, but their number was the highest in March, what overlapped with maximum numbers of hibernating M. myotis. The prevalence in March was 7%–27% of M. myotis individuals. No mass mortality of bats was observed in the mine, with only three dead individuals found in the hibernaculum which hosted up to 130 bats, representing 6–7 species.

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Complete Genome Sequence of Houston Virus, a Newly Discovered Mosquito-Specific Virus Isolated from Culex quinquefasciatus in Mexico

Microbiology Resource Announcements ◽

10.1128/mra.00808-18 ◽

2018 ◽

Vol 7 (10) ◽

Cited By ~ 2

Author(s):

Nohemi Cigarroa-Toledo ◽

Carlos M. Baak-Baak ◽

Rosa C. Cetina-Trejo ◽

Carlos Cordova-Fletes ◽

Mario A. Martinez-Nuñez ◽

...

Keyword(s):

United States ◽

North America ◽

Culex Quinquefasciatus ◽

Complete Genome Sequence ◽

Complete Genome ◽

The United States ◽

Geographic Range ◽

Southern Mexico ◽

Content Type ◽

Specific Virus

We fully sequenced the genome of Houston virus, a recently discovered mosquito-associated virus belonging to the newly established family Mesoniviridae. The isolate was recovered from Culex quinquefasciatus in southern Mexico, which shows that the geographic range of Houston virus is not restricted to the United States in North America.

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Phenotype profiling of white-nose syndrome pathogen Pseudogymnoascus destructans and closely-related Pseudogymnoascus pannorum reveals metabolic differences underlying fungal lifestyles

F1000Research ◽

10.12688/f1000research.15067.2 ◽

2018 ◽

Vol 7 ◽

pp. 665 ◽

Cited By ~ 5

Author(s):

Vishnu Chaturvedi ◽

Holland DeFiglio ◽

Sudha Chaturvedi

Keyword(s):

In Silico ◽

Carbon Sources ◽

The United States ◽

Nitrogen Compounds ◽

Pseudogymnoascus Destructans ◽

White Nose Syndrome ◽

Nutrient Supplements ◽

Carbohydrate Degradation ◽

Metabolic Activities ◽

Phosphorous Compounds

Background: Pseudogymnoascus destructans, a psychrophile, causes bat white-nose syndrome (WNS). Pseudogymnoascus pannorum, a closely related fungus, causes human and canine diseases rarely. Both pathogens were reported from the same mines and caves in the United States, but only P. destructans caused WNS. Earlier genome comparisons revealed that P. pannorum contained more deduced proteins with ascribed enzymatic functions than P. destructans. Methods: We performed metabolic profiling with Biolog PM microarray plates to confirm in silico gene predictions. Results: P. pannorum utilized 78 of 190 carbon sources (41%), and 41 of 91 nitrogen compounds (43%) tested. P. destructans used 23 carbon compounds (12%) and 23 nitrogen compounds (24%). P. destructans exhibited more robust growth on the phosphorous compounds and nutrient supplements (83% and 15%, respectively) compared to P. pannorum (27% and 1%, respectively.). P. pannorum exhibited higher tolerance to osmolytes, pH extremes, and a variety of chemical compounds than P. destructans. Conclusions: An abundance of carbohydrate degradation pathways combined with robust stress tolerance provided clues for the soil distribution of P. pannorum. The limited metabolic profile of P. destructans was compatible with in silico predictions of far fewer proteins and enzymes. P. destructans ability to catabolize diverse phosphorous and nutrient supplements might be critical in the colonization and invasion of bat tissues. The present study of 1,047 different metabolic activities provides a framework for future gene-function investigations of the unique biology of the psychrophilic fungi.

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