2,332
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Plant pathogens provide clues to the potential origin of bat white-nose syndrome Pseudogymnoascus destructans

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 1020-1031 | Received 04 Feb 2022, Accepted 19 May 2022, Published online: 06 Jun 2022

References

  • Hoyt JR, Kilpatrick AM, Langwig KE. Ecology and impacts of white-nose syndrome on bats. Nat Rev Microbiol. 2021;19(3):196–210.
  • Gargas A, Trest M, Christensen M, et al. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon. 2009;108(1):147–154.
  • Minnis AM, Lindner DL. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 2013;117(9):638–649.
  • Turner GG, Meteyer CU, Barton H, et al. Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. J Wildl Dis. 2014;50(3):566–573. DOI:10.7589/2014-03-058
  • Meteyer CU, Buckles EL, Blehert DS, et al. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Investig. 2009;21(4):411–414. DOI:10.1177/104063870902100401
  • Blehert DS, Hicks AC, Behr M, et al. Bat white-nose syndrome: an emerging fungal pathogen? Science (Washington, DC). 2009;323:227.
  • Lorch JM, Minnis AM, Meteyer CU, et al. The fungus Trichophyton redellii sp. nov. causes skin infections that resemble white-nose syndrome of hibernating bats. J Wildl Dis. 2015;51(1):36–47. DOI:10.7589/2014-05-134
  • Berbee ML. The phylogeny of plant and animal pathogens in the Ascomycota. Physiol Mol Plant Pathol. 2001;59(4):165–187.
  • Verant ML, Boyles JG, Waldrep JW, et al. Temperature-Dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS One. 2012;7:e46280.
  • Chinnapun D. Virulence factors involved in pathogenicity of dermatophytes. Walailak J Sci Technol. 2015;12:573–580.
  • Raudabaugh DB, Miller AN. Nutritional capability of and substrate suitability for Pseudogymnoascus destructans, the causal agent of bat white-nose syndrome. PLoS One. 2013;8(10):e78300.
  • Chaturvedi V, Springer DJ, Behr MJ, et al. Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS One. 2010;5(5):e10783. DOI:10.1371/journal.pone.0010783
  • Reynolds HT, Barton HA. Comparison of the white-nose syndrome agent Pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprotrophic enzyme activity. PLoS One. 2014;9(1):e86437.
  • Ye F, Li M, Zhu S, et al. Diagnosis of dermatophytosis using single fungus endogenous fluorescence spectrometry. Biomed Opt Express. 2018;9(6):2733–2742.
  • Cruz-Mireles N, Eseola AB, Osés-Ruiz M, et al. From appressorium to transpressorium—defining the morphogenetic basis of host cell invasion by the rice blast fungus. PLoS Path. 2021;17(7):e1009779.
  • Donaldson ME, Davy CM, Vanderwolf KJ, et al. Growth medium and incubation temperature alter the Pseudogymnoascus destructans transcriptome: implications in identifying virulence factors. Mycologia. 2018;110(2):300–315.
  • Reynolds HT, Ingersoll T, Barton HA. Modeling the environmental growth of Pseudogymnoascus destructans and its impact on the white-nose syndrome epidemic. J Wildl Dis. 2015;51(2):318–331.
  • Wilson MB, Held BW, Freiborg AH, et al. Resource capture and competitive ability of non-pathogenic Pseudogymnoascus spp. And P. destructans, the cause of white-nose syndrome in bats. PLoS One. 2017;12:e0178968.
  • Reynolds HT, Barton HA, Slot JC. Phylogenomic analysis supports a recent change in nitrate assimilation in the white-nose syndrome pathogen, Pseudogymnoascus destructans. Fungal Ecol. 2016;23:20–29.
  • McGuire LP, Turner JM, Warnecke L, et al. White-Nose syndrome disease severity and a comparison of diagnostic methods. Ecohealth. 2016;13(1):60–71. DOI:10.1007/s10393-016-1107-y
  • Meteyer CU, Valent M, Kashmer J, et al. Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome. J Wildl Dis. 2011;47(3):618–626. DOI:10.7589/0090-3558-47.3.618
  • Koeck M, Hardham AR, Dodds PN. The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiol. 2011;13(12):1849–1857.
  • Chowdhury S, Basu A, Kundu S. Biotrophy-Necrotrophy switch in pathogen evoke differential response in resistant and susceptible sesame involving multiple signaling pathways at different phases. Sci Rep. 2017;7(1):17251.
  • Brun S, Silar P Convergent evolution of morphogenetic processes in fungi. In: Evolutionary biology–concepts, molecular and morphological evolution. Berlin, Heidelberg: Springer; 2010. p. 317–328.
  • Cryan PM, Meteyer CU, Boyles JG, et al. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 2010;8(1):1–8.
  • Verant ML, Meteyer CU, Speakman JR, et al. White-Nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol. 2014;14(1):1–11.
  • Van Rooij P, Martel A, Haesebrouck F, et al. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Vet Res. 2015;46(1):1–22.
  • Haffner M. The size of sebaceous glands in relation to the size of hair follicles on the heads of some small mammals (Insectivore, Chiroptera, Rodentia). Ann Anat. 1998;180(2):165–171.
  • Fuller KK, Rhodes JC. Protein kinase a and fungal virulence: a sinister side to a conserved nutrient sensing pathway. Virulence. 2012;3:109–121.
  • Tariq V, Jeffries P. Appressorium formation by Sclerotinia sclerotiorum: scanning electron microscopy. Trans Br Mycol Soc. 1984;82(4):645–651.
  • van Kan JA. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 2006;11(5):247–253.
  • Ikeda K, Park P, Nakayashiki H. Cell biology in phytopathogenic fungi during host infection: Commonalities and differences. J Gen Plant Pathol. 2019;85(3):163–173.
  • Demoor A, Silar P, Brun S. Appressorium: the breakthrough in Dikarya. J Fungi. 2019;5(3):72.
  • Schnee S, Rougeux E, Pezet R, et al. Evidence for constitutive cutinase in urgeminated conidia of Erysiphe necator Schwein. J Cytol Histol. 2013;4:197.
  • Duan Y, Wu H, Ma Z, et al. Scanning electron microscopy and histopathological observations of Beauveria bassiana infection of Colorado potato beetle larvae. Microb Pathog. 2017;111:435–439.
  • Hajek AE. Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera. Microbiol Mol Biol Rev. 1999;63(4):814–835.
  • Brandner J, Zorn-Kruppa M, Yoshida T, et al. Epidermal tight junctions in health and disease. Tissue Barriers. 2015;3(1–2):e974451.
  • Reeder SM, Palmer JM, Prokkola JM, et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence. 2017;8(8):1695–1707.
  • Valent B, Khang CH. Recent advances in rice blast effector research. Curr Opin Plant Biol. 2010;13(4):434–441.
  • Palmer JM, Drees KP, Foster JT, et al. Extreme sensitivity to ultraviolet light in the fungal pathogen causing white-nose syndrome of bats. Nat Commun. 2018;9(1):1–10.
  • Crous PW, Groenewald JZ. They seldom occur alone. Fungal Biol. 2016;120(11):1392–1415.
  • Oguchi T. Studies on the species of Lachnellula in Hokkaido: their morphology, physiology, and pathogenicity. Bull Hokkaido for Exp Stn. 1981;19:187–246.
  • Dean R, Van Kan JA, Pretorius ZA, et al. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13(4):414–430. DOI:10.1111/j.1364-3703.2011.00783.x
  • Pannkuk EL, Risch TS, Savary BJ. Isolation and identification of an extracellular subtilisin-like serine protease secreted by the bat pathogen Pseudogymnoascus destructans. PLoS One. 2015;10(3):e0120508.
  • Chaturvedi V, DeFiglio H, Chaturvedi S. Phenotype profiling of white-nose syndrome pathogen Pseudogymnoascus destructans and closely-related Pseudogymnoascus pannorum reveals metabolic differences underlying fungal lifestyles. F1000res. 2018;7:665.
  • Mosbrugger V, Utescher T, Dilcher DL. Cenozoic continental climatic evolution of Central Europe. Proc Natl Acad Sci USA. 2005;102(42):14964–14969.
  • Zachos JC, Dickens GR, Zeebe RE. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature. 2008;451(7176):279–283.
  • Lovegrove BG. The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum. Biol Rev (Camb). 2012;87(1):128–162.
  • Canale CI, Levesque DL, Lovegrove BG. Tropical heterothermy: does the exception prove the rule or force a re-definition? Living in a Seasonal World. 2012:29–40.
  • Davy CM, Donaldson ME, Bandouchova H, et al. Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome. Virulence. 2020;11(1):781–794. DOI:10.1080/21505594.2020.1768018
  • Lilley TM, Prokkola JM, Blomberg AS, et al. Resistance is futile: RNA-sequencing reveals differing responses to bat fungal pathogen in Nearctic Myotis lucifugus and Palearctic Myotis myotis. Oecologia. 2019;191(2):295–309. DOI:10.1007/s00442-019-04499-6
  • Martínková N, Bačkor P, Bartonička T, et al. Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS One. 2010;5(11):e13853. DOI:10.1371/journal.pone.0013853
  • Drees KP, Lorch JM, Puechmaille SJ, et al. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. Mbio. 2017;8(6): e01941-17. doi:10.1128/mBio.01941-17.
  • Trivedi J, Lachapelle J, Vanderwolf KJ, et al. Fungus causing white-nose syndrome in bats accumulates genetic variability in North America with no sign of recombination. mSphere. 2017;2(4): e00271-17. doi:10.1128/mSphereDirect.00271-17.
  • Puechmaille SJ, Wibbelt G, Korn V, et al. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One. 2011;6(4):e19167. DOI:10.1371/journal.pone.0019167
  • Warnecke L, Turner JM, Bollinger TK, et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci USA. 2012;109(18):6999–7003. DOI:10.1073/pnas.1200374109
  • Kovacova V, Zukal J, Bandouchova H, et al. White-Nose syndrome detected in bats over an extensive area of Russia. BMC Vet Res. 2018;14(1):1–9. DOI:10.1186/s12917-018-1521-1
  • Prophet EB. Laboratory methods in histotechnology. Amer Registry of Pathology; 1992.
  • Drees KP, Palmer JM, Sebra R, et al. Use of multiple sequencing technologies to produce a high-quality genome of the fungus Pseudogymnoascus destructans , the causative agent of bat white-nose syndrome. Genome Announc. 2016;4(3): e00445-16. doi:10.1128/genomeA.00445-16.
  • Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60.
  • Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797.
  • Sievers F, Higgins DG. Clustal omega, accurate alignment of very large numbers of sequences. Multiple sequence alignment methods. Methods Mol Biol. 2014;1079:105–116.
  • Dutheil J, Boussau B. Non-Homogeneous models of sequence evolution in the bio++ suite of libraries and programs. BMC Evol Biol. 2008;8(1):1–12.
  • Tange O. GNU parallel: the command-line power tool. 2011.
  • Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5(3):e9490.
  • Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–1320.
  • Kozlov AM, Darriba D, Flouri T, et al. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35:4453–4455.
  • Guéguen L, Gaillard S, Boussau B, et al. Bio++: efficient extensible libraries and tools for computational molecular evolution. Mol Biol Evol. 2013;30(8):1745–1750. DOI:10.1093/molbev/mst097
  • Kozlov AM, Stamatakis A. Using RAxML-NG in practice. In: Scornavacca C; F Delsuc and N Galtier, editors. Phylogenomics in the Genomic Era: No commercial publisher | Authors open access book. 2020. pp. 1.3:11.3:1.3:25
  • Pattengale ND, Alipour M, Bininda-Emonds OR, et al. How many bootstrap replicates are necessary? J Comput Biol. 2010;17(3):337–354.
  • Yu G, Lam T-Y, Zhu H, et al. Two methods for mapping and visualizing associated data on phylogeny using ggtree. Mol Biol Evol. 2018;35(12):3041–3043.
  • Paradis E, Schliep K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35(3):526–528.
  • Huelsenbeck JP, Nielsen R, Bollback JP. Stochastic mapping of morphological characters. Syst Biol. 2003;52(2):131–158.
  • Nielsen R, Huelsenbeck J. Mapping mutations on phylogenies. Syst Biol. 2002;51(5):729–739.
  • Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3(2):217–223.