Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome

References

• Frick WF, Pollock JF, Hicks AC, et al. An emerging disease causes regional population collapse of a common North American bat species. Sci. 2010;329:679–682.
   PubMed Web of Science ®Google Scholar
• Maslo B, Valent M, Gumbs JF, et al. Conservation implications of ameliorating survival of little brown bats with white-nose syndrome. Ecol Appl. 2015;25:1832–1840.
   PubMed Web of Science ®Google Scholar
• Vitale C, Best A. The paradox of tolerance: parasite extinction due to the evolution of host defence. J Theor Biol. 2019;474:78–87.
   PubMed Web of Science ®Google Scholar
• Doddington BJ, Grassly NC, Fisher MC, et al. Context-dependent amphibian host population response to an invading pathogen. Ecology. 2013;94:1795–1804.
   PubMed Web of Science ®Google Scholar
• Mordecai EA, Caldwell JM, Grossman MK, et al. Thermal biology of mosquito‐borne disease. Ecol Lett. 2019;22: 1690–1708.
   PubMed Web of Science ®Google Scholar
• Poorten T, Rosenblum EB. Comparative study of host response to chytridiomycosis in a susceptible and a resistant toad species. Mol Ecol. 2016;25:5663–5679.
   PubMed Web of Science ®Google Scholar
• Langwig KE, Frick WF, Hoyt JR, et al. Drivers of variation in species impacts for a multi-host fungal disease of bats. Philos Trans R Soc B Biol Sci. 2016;371:20150456.
   PubMed Web of Science ®Google Scholar
• Field KA, Sewall BJ, Prokkola JM, et al. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol Ecol. 2018;27:3727–3743.
   Web of Science ®Google Scholar
• Mayberry HW, Mcguire LP, Willis CKR. Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome. J Comp Physiol B. 2018;188:333–343.
   PubMed Web of Science ®Google Scholar
• Reeder DM, Frank CL, Turner GG, et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One. 2012;7:e38920–e38920.
   PubMed Web of Science ®Google Scholar
• Turner JM, Warnecke L, Wilcox A, et al. Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiol Behav. 2015;140:71–78.
   PubMed Web of Science ®Google Scholar
• 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. 2012;109:6999–7003.
   PubMed Web of Science ®Google Scholar
• Mcguire LP, Mayberry HW, Willis CKR. White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats. Am J Physiol Integr Comp Physiol. 2017;313:R680–R686.
   PubMed Web of Science ®Google Scholar
• Wilcox A, Warnecke L, Turner JM, et al. Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. Anim Behav. 2014;88:157–164.
   Web of Science ®Google Scholar
• Meteyer CU, Barber D, Mandl JN. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence. 2012;3:583–588.
   PubMed Web of Science ®Google Scholar
• Kovacova V, Bandouchova H, Piacek V, et al. White-nose syndrome detected in bats over an extensive area of Russia. BMC Vet Res. 2018;14:1–9.
   PubMed Web of Science ®Google Scholar
• Martínková N, Pikula J, Zukal J, et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9:1734–1750.
   PubMed Web of Science ®Google Scholar
• Zukal J, Bandouchova H, Brichta J, et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep. 2016;6:1–13.
   PubMed Web of Science ®Google Scholar
• Drees KP, Lorch JM, Puechmaille SJ, et al. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. MBio. 2017;8:e01941–17.
   PubMed Web of Science ®Google Scholar
• Langwig KE, Frick WF, Bried JT, et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett. 2012;15:1050–1057.
   PubMed Web of Science ®Google Scholar
• Davy CM, Donaldson ME, Willis CKR, et al. The other white-nose syndrome transcriptome: tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans. Ecol Evol. 2017;7:7161–7170.
   PubMed Web of Science ®Google Scholar
• Donaldson ME, Davy CM, Willis CKR, et al. Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white-nose syndrome. Evol Appl. 2017;10:1076–1090.
   PubMed Web of Science ®Google Scholar
• Frank CL, Michalski A, McDonough AA, et al. The resistance of a North American bat species (Eptesicus fuscus) to White-Nose Syndrome (WNS). PLoS One. 2014;9:1–14.
   Web of Science ®Google Scholar
• Harazim M, Horáček I, Jakešová L, et al. Natural selection in bats with historical exposure to white-nose syndrome. BMC Zool. 2018;3:1–13.
   Web of Science ®Google Scholar
• Hayman DTS, Pulliam JRC, Marshall JC, et al. Environment, host, and fungal traits predict continental-scale white-nose syndrome in bats. Sci. Adv. 2016;2:e1500831.
   Google Scholar
• Langwig KE, Frick WF, Reynolds R, et al. Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc London B Biol Sci. 2015;282:2014–2335.
   Web of Science ®Google Scholar
• Moore MS, Field KA, Behr MJ, et al. Energy conserving thermoregulatory patterns and lower disease severity in a bat resistant to the impacts of white-nose syndrome. J Comp Physiol B. 2017;188:163–176.
   PubMed Web of Science ®Google Scholar
• Field KA, Johnson JS, Lilley TM, et al. The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating little brown myotis. PLoS Pathog. 2015;11:e1005168–e1005168.
   PubMed Web of Science ®Google Scholar
• Reeder SM, Palmer JM, Prokkola JM, et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence. 2017;8:1695–1707.
   PubMed Web of Science ®Google Scholar
• 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;191:295–309.
   PubMed Web of Science ®Google Scholar
• Alves DMCC, Terribile LC, Brito D. The potential impact of white-nose syndrome on the conservation status of North American bats. PLoS One. 2014;9:1–7.
   Web of Science ®Google Scholar
• Zukal J, Bandouchova H, Bartonicka T, et al. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS One. 2014;9:e97224.
   PubMed Web of Science ®Google Scholar
• Davy CM, Donaldson ME, Willis CKR, et al. Environmentally persistent pathogens present unique challenges for studies of host–pathogen interactions: reply to Field (2018). Ecol Evol. 2018b;8:5238–5241.
   PubMed Web of Science ®Google Scholar
• Flieger M, Bandouchova H, Cerny J, et al. Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci Rep. 2016;6:1–12.
   PubMed Web of Science ®Google Scholar
• 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;50:566–573.
   PubMed Web of Science ®Google Scholar
• Martínková N, Škrabánek P, Pikula J. Modelling invasive pathogen load from non-destructive sampling data. J Theor Biol. 2019;464:98–103.
   PubMed Web of Science ®Google Scholar
• Donaldson ME, Davy CM, Vanderwolf KJ, et al. Growth media and incubation temperature alter the Pseudogymnoascus destructans transcriptome: implications in identifying virulence factors. Mycologia. 2018;110:300–315.
   PubMed Web of Science ®Google Scholar
• O’Donoghue AJ, Knudsen GM, Beekman C, et al. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc Natl Acad Sci. 2015;112:7478–7483.
   PubMed Web of Science ®Google Scholar
• 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:e0120508–e0120508.
   PubMed Web of Science ®Google Scholar
• Jirtle R, Skinner M. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253–262.
   PubMed Web of Science ®Google Scholar
• Langwig KE, Hoyt J, Parise K, et al. Resistance in persisting bat populations after white-nose syndrome invasion. Philos Trans B. 2017;372:20160044.
   PubMed Web of Science ®Google Scholar
• Vanderwolf KJ, McAlpine DF, Forbes GJ, et al. Bat populations and cave microclimate prior to and at the outbreak of white-nose syndrome in New Brunswick. Can Field-Naturalist. 2012;126:125–134.
   Web of Science ®Google Scholar
• Mcalpine DF, Mcburney S, Sabine M, et al. Molecular detection of pPseudogymnoascus destructans (Ascomycota: pseudeurotiaceae) and unidentified fungal dermatitides on big brown bats (Eptesicus fuscus) overwintering inside buildings in Canada. J Wildl Dis Wildl Dis Assoc. 2016;52:902–906.
   Google Scholar
• Pikula J, Amelon SK, Bandouchova H, et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS One. 2017;12:1–21.
   Web of Science ®Google Scholar
• McGuire LP, Turner JM, Warnecke L, et al. White-nose syndrome disease severity and a comparison of diagnostic methods. Ecohealth. 2016;13:60–71.
   PubMed Web of Science ®Google Scholar
• Andrews S 2010. FastQC: a quality control tool for high throughput sequence data. [cited 2016 Jul 28]. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
   Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30(15):2114–2120.
   PubMed Web of Science ®Google Scholar
• Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357.
   PubMed Web of Science ®Google Scholar
• Zerbino DR, Achuthan P, Akanni W, et al. Ensembl 2018. Nucleic Acids Res. 2018;46:D754–D761.
   PubMed Web of Science ®Google Scholar
• Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinforma. 2014;30:923–930.
   Google Scholar
• Grabherr MG, Haas BJ, Yassour M, et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol. 2011;29:644–652.
   PubMed Web of Science ®Google Scholar
• Waterhouse RM, Seppey M, Simão FA, et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol. 2018;35:543–548.
   PubMed Web of Science ®Google Scholar
• Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
   PubMed Web of Science ®Google Scholar
• Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12. DOI:https://doi.org/10.1186/1471-2105-12-323
   Google Scholar
• Lagesen K, Hallin P, Rødland E, et al. RNAmmer: consistent annotation of rRNA genes in genomic sequences. Nucleic Acids Res. 2007;35:3100–3108.
   PubMed Web of Science ®Google Scholar
• 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:e00445–16.
   PubMedGoogle Scholar
• Bates DM, Maechler M, Bolker B, et al. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.
   Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014;15:55.
   Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma. 2010;26:139–140.
   Google Scholar
• Varet H, Coppée J-Y, Dillies M-A. SARTools: a DESeq2- and edgeR-based R pipeline for comprehensive differential analysis of RNA-Seq data. PLoS One. 2015;11:e0157022.
   Google Scholar
• McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 2004;32:W20–W25.
   PubMed Web of Science ®Google Scholar
• Klopfenstein DV, Zhang L, Pedersen BS, et al. GOATOOLS: A python library for gene ontology analyses. Sci Rep. 2018;8:10872.
   PubMed Web of Science ®Google Scholar
• Kinsella RJ, Kähäri A, Haider S, et al. Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database (Oxford). 2011;2011:bar030–bar030.
   PubMed Web of Science ®Google Scholar
• Chen C, Huang H, Wu CH. Protein bioinformatics databases and resources. Methods Mol Biol. 2017;1558:3–39.
   PubMedGoogle Scholar
• Lopes FC, Silva LADE, Tichota DM, et al. Production of proteolytic enzymes by a keratin-degrading Aspergillus niger. Enzyme Res. 2011;2011: 1-9. https://www.hindawi.com/journals/er/2011/487093
   Google Scholar
• Enguita FJ, Costa MC, Fusco-almeida AM, et al. Transcriptomic crosstalk between fungal invasive pathogens and their host cells: opportunities and challenges for next-generation sequencing methods. J Fungi. 2016;2:1–15.
   Web of Science ®Google Scholar
• 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:e19167–e19167.
   PubMed Web of Science ®Google Scholar
• Bandouchova H, Bartonicka T, Berkova H, et al. Pseudogymnoascus destructans: evidence of virulent skin invasion for bats under natural conditions, Europe. Transbound Emerg Dis. 2015;62:1–5.
   PubMed Web of Science ®Google Scholar
• Pikula J, Bandouchova H, Novotný L, et al. Histopathology confirms white-nose syndrome in bats in Europe. J Wildl Dis. 2013;48:207–211.
   Web of Science ®Google Scholar
• Řezanka T, Viden I, Nováková A, et al. Wax ester analysis of bats suffering from white nose syndrome in Europe. Lipids. 2015;50:633–645.
   PubMed Web of Science ®Google Scholar
• Bandouchova H, Bartonička T, Berkova H, et al. Alterations in the health of hibernating bats under pathogen pressure. Sci Rep. 2018;8:1–11.
   PubMed Web of Science ®Google Scholar
• Zukal J, Berková H, Řehák Z. Activity and shelter selection by Myotis myotis and Rhinolophus hipposideros hibernating in the Kateřinská cave (Czech Republic). Mamm Biol. 2005;70:271–281.
   Web of Science ®Google Scholar
• Davy CM, Donaldson ME, Subudhi S, et al. White-nose syndrome is associated with increased replication of naturally persisting coronaviruses in bats. Sci. Rep. 2018a;8(1):In press. doi:https://doi.org/10.1038/s41598-018-33975-x.
   Google Scholar
• Lilley TM, Prokkola JM, Johnson JS, et al. Immune responses in hibernating little brown myotis (Myotis lucifugus) with white-nose syndrome. Proc R Soc B Biol Sci. 2017;284:20162232.
   PubMed Web of Science ®Google Scholar
• Rapin N, Johns K, Martin L, et al. Activation of Innate immune-response genes in little brown bats (Myotis lucifugus) infected with the fungus Pseudogymnoascus destructans. PLoS One. 2014;9:e112285–e112285.
   PubMed Web of Science ®Google Scholar
• Auteri GG, Knowles LL. Decimated little brown bats show potential for adaptive change. Sci Rep. 2020;10:1–10.
   PubMed Web of Science ®Google Scholar
• Cheng TL, Gerson A, Moore MS, et al. Higher fat stores contribute to persistence of little brown bat populations with white-nose syndrome. J Anim Ecol. 2018;88:591–600.
   Web of Science ®Google Scholar
• Maslo B, Fefferman NH. A case study of bats and white‐nose syndrome demonstrating how to model population viability with evolutionary effects. Conserv Biol. 2015;29:1176–1185.
   PubMed Web of Science ®Google Scholar
• Hoyt JR, Cheng TL, Langwig KE, et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS One. 2015;10:e0121329–e0121329.
   PubMed Web of Science ®Google Scholar
• Cheng TL, Mayberry H, McGuire LP, et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J Appl Ecol. 2016;54:701–708.
   Web of Science ®Google Scholar
• Hoyt JR, Langwig KE, White JP, et al. Field trial of a probiotic bacteria and a chemical, chitosan, to protect bats from white-nose syndrome. Sci Rep. 2019;9:1–9.
   PubMed Web of Science ®Google Scholar