Comparative eco-physiology revealed extensive enzymatic curtailment, lipases production and strong conidial resilience of the bat pathogenic fungus Pseudogymnoascus destructans

Veselská, Tereza; Homutová, Karolína; Fraile, Paula García; Kubátová, Alena; Martínková, Natália; Pikula, Jiří; Kolařík, Miroslav

doi:10.1038/s41598-020-73619-7

Cited by 12 publications

(7 citation statements)

References 70 publications

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“…After the iceman’s death, the fungus found suitable survival and growth conditions for its proliferation. This hypothesis is supported by the ecology of the Pseudogymnoascus species, which has a long-term persistence and can survive and grow at a temperature lower than -20 °C and in harsh environments (40, 38, 41). Moreover, there is evidence that some Pseudogymnoascus species, such as P. destructans can survive in the gastrointestinal tract (42).…”

Section: Resultsmentioning

confidence: 94%

Unravelling the ancient fungal DNA from the Iceman’s gut

Oskolkov,

Sandionigi,

Göterström

et al. 2024

Preprint

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Here, we explore the possible ancient fungal species in the gut of Otzi, the Iceman, a naturally mummified human found in the Tyrolean Alps (border between Italy and Austria). While ancient DNA (aDNA) has been extensively used to study human, animal, and plant evolution, this research focuses on ancient microbial diversity, specifically fungi. Fungal DNA is often underestimated in metagenomic samples, however here we hypothesise the possibility of retrieving ancient fungal sequences from Otzi's gut. A robust bioinformatic pipeline has been developed to detect and authenticate fungal aDNA from stomach, small intestine, and large intestine samples. We revealed the presence of Pseudogymnoascus genus, with P. destructans and P. verrucosus as possible species, that were particularly abundant in the stomach and small intestine. We suggest that Otzi may have consumed these fungi accidentally, likely in association with other elements of his diet, and they thrived in his gut after his death due to their adaptability to harsh and cold environments. This research provides insight into the coexistence of ancient humans with specific fungal species and proposes and validates a conservative bioinformatic approach for detecting fungal aDNA in historical metagenomic samples.

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Section: Resultsmentioning

confidence: 94%

Unravelling the ancient fungal DNA from the Iceman’s gut

Oskolkov,

Sandionigi,

Göterström

et al. 2024

Preprint

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“…Cultures of P. destructans alkalinize some growth media in vitro (e.g. 5.6–7.9 pH) ( Veselská et al , 2020 ), but it is unknown if the fungus alkalinizes bat skin. Prior to WNS, skin diseases were not commonly reported in bats, although dermatophytes are known to grow on bat skin ( Simpson et al , 2013 ; Lorch et al.…”

Section: Introductionmentioning

confidence: 99%

Skin pH varies among bat species and seasons and between wild and captive bats

Vanderwolf

Kyle

Faure

et al. 2021

Conservation Physiology

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Skin is a key aspect of the immune system in the defence against pathogens. Skin pH regulates the activity of enzymes produced both by hosts and by microbes on host skin, thus implicating pH in disease susceptibility. Skin pH varies inter- and intra-specifically and is influenced by a variety of intrinsic and extrinsic variables. Increased skin alkalinity is associated with a predisposition to cutaneous infections in humans and dogs, and inter-specific and inter-individual variation in skin pH is implicated in differential susceptibility to some skin diseases. The cutaneous pH of bats has not been characterized but is postulated to play a role in susceptibility to white-nose syndrome (WNS), a fungal infection that has decimated several Nearctic bat species. We used non-invasive probes to measure the pH of bat flight membranes in five species with differing susceptibility to WNS. Skin pH ranged from 4.67 to 8.59 and varied among bat species, geographic locations, body parts, age classes, sexes and seasons. Wild Eptesicus fuscus were consistently more acidic than wild Myotis lucifugus, Myotis leibii and Perimyotis subflavus. Juvenile bats had more acidic skin than adults during maternity season but did not differ during swarming. Male M. lucifugus were more acidic than females during maternity season, yet this trend reversed during swarming. Bat skin was more acidic in summer compared to winter, a pattern also reported in humans. Skin pH was more acidic in captive than wild E. fuscus, suggesting environmental impacts on skin pH. The pH of roosting substrates affects skin pH in captive bats and may partially explain seasonal patterns in wild bats that use different roost types across seasons. Future research on the influence of pH on microbial pathogenic factors and skin barrier function may provide valuable insights on new therapeutic targets for treating bat skin conditions.

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“…Zahn, 1999 for M. myotis ). Fungal spores are known to be more durable than fungal hyphae, but even P. destructans spore viability decreases to a few percent after only 15–20 days at 37°C (Campbell et al, 2020; Veselská et al, 2020), suggesting that the fungus is unlikely to remain viable on bats through the active summer period. Screening results for P. destructans on bats during the summer is consistent with this prediction with only a small fraction of individuals tested carrying DNA of the fungus (e.g.…”

Section: Discussionmentioning

confidence: 99%

Population genetics as a tool to elucidate pathogen reservoirs: Lessons fromPseudogymnoascus destructans, the causative agent of white-nose disease in bats

Fischer

Altewischer

Ranpal

et al. 2021

Preprint

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Emerging infectious diseases pose a major threat to human, animal, and plant health. The risk of species-extinctions increases when pathogens can survive in the absence of the host, for example in environmental reservoirs. However, identifying such reservoirs and modes of infection is often highly challenging. In this study, we investigated the presence and nature of an environmental reservoir for the ascomycete fungus Pseudogymnoascus destructans, the causative agent of white-nose disease. We also characterised the modes and timing of transmission of the pathogen; key elements to better understand the disease dynamics. Using 18 microsatellite markers, we determined the genotypic and genic (based on allele frequencies) differentiation between 1,497 P. destructans isolates collected from nine closely situated hibernacula in North-Eastern Germany. One hibernaculum was the focus of intensive sampling in which both the bats and walls of the site were sampled at regular intervals over five consecutive winter seasons (1,062 isolates). We found significant genic differentiation between sites and few multi-locus genotypes shared across hibernacula (genotypic differentiation). This demonstrates that each hibernaculum has an essentially unique population of the fungus. This would be expected if bats purge viable P. destructans over the summer, preventing the mixing and exchange of the pathogen in maternity colonies, where bats from all of the studied hibernacula meet. Results from the intensively sampled site show higher measures of genotypic richness on walls compared to bats, the absence of genic differentiation between bats and walls, and stable relative abundance of multi-locus genotypes over multiple winter seasons. This clearly implicates hibernacula walls as the main environmental reservoir of the pathogen, from which bats become re-infected annually.

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Comparative eco-physiology revealed extensive enzymatic curtailment, lipases production and strong conidial resilience of the bat pathogenic fungus Pseudogymnoascus destructans

Cited by 12 publications

References 70 publications

Unravelling the ancient fungal DNA from the Iceman’s gut

Unravelling the ancient fungal DNA from the Iceman’s gut

Skin pH varies among bat species and seasons and between wild and captive bats

Population genetics as a tool to elucidate pathogen reservoirs: Lessons fromPseudogymnoascus destructans, the causative agent of white-nose disease in bats

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