Transcriptional host-pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32552222
PubMed Central
PMC7549942
DOI
10.1080/21505594.2020.1768018
Knihovny.cz E-zdroje
- Klíčová slova
- Eptesicus fuscus, Myotis lucifugus, Myotis myotis, Pseudogymnoascus destructans, Disease ecology, emerging infectious diseases, host–pathogen interactions, susceptibility, virulence,
- MeSH
- Ascomycota genetika patogenita MeSH
- Chiroptera klasifikace mikrobiologie MeSH
- dermatomykózy mikrobiologie veterinární MeSH
- druhová specificita MeSH
- fylogeneze MeSH
- interakce hostitele a patogenu genetika MeSH
- křídla zvířecí mikrobiologie patologie MeSH
- nos mikrobiologie patologie MeSH
- stanovení celkové genové exprese * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Understanding how context (e.g., host species, environmental conditions) drives disease susceptibility is an essential goal of disease ecology. We hypothesized that in bat white-nose syndrome (WNS), species-specific host-pathogen interactions may partly explain varying disease outcomes among host species. We characterized bat and pathogen transcriptomes in paired samples of lesion-positive and lesion-negative wing tissue from bats infected with Pseudogymnoascus destructans in three parallel experiments. The first two experiments analyzed samples collected from the susceptible Nearctic Myotis lucifugus and the less-susceptible Nearctic Eptesicus fuscus, following experimental infection and hibernation in captivity under controlled conditions. The third experiment applied the same analyses to paired samples from infected, free-ranging Myotis myotis, a less susceptible, Palearctic species, following natural infection and hibernation (n = 8 sample pairs/species). Gene expression by P. destructans was similar among the three host species despite varying environmental conditions among the three experiments and was similar within each host species between saprophytic contexts (superficial growth on wings) and pathogenic contexts (growth in lesions on the same wings). In contrast, we observed qualitative variation in host response: M. lucifugus and M. myotis exhibited systemic responses to infection, while E. fuscus up-regulated a remarkably localized response. Our results suggest potential phylogenetic determinants of response to WNS and can inform further studies of context-dependent host-pathogen interactions.
Environmental and Life Sciences Program Trent University Peterborough Canada
Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic
Natural Resources DNA Profiling and Forensics Centre Trent University Peterborough Canada
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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
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
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
Doddington BJ, Grassly NC, Fisher MC, et al. Context-dependent amphibian host population response to an invading pathogen. Ecology. 2013;94:1795–1804. PubMed
Mordecai EA, Caldwell JM, Grossman MK, et al. Thermal biology of mosquito‐borne disease. Ecol Lett. 2019;22: 1690–1708. PubMed PMC
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
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 PMC
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. PubMed
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
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 PMC
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
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 PMC
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 PMC
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.
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 PMC
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 PMC
Martínková N, Pikula J, Zukal J, et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9:1734–1750. PubMed PMC
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 PMC
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 PMC
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
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 PMC
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 PMC
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. PubMed PMC
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.
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. PubMed PMC
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. PubMed PMC
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
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 PMC
Reeder SM, Palmer JM, Prokkola JM, et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence. 2017;8:1695–1707. PubMed PMC
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 PMC
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. PubMed PMC
Zukal J, Bandouchova H, Bartonicka T, et al. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS One. 2014;9:e97224. PubMed PMC
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 PMC
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 PMC
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
Martínková N, Škrabánek P, Pikula J. Modelling invasive pathogen load from non-destructive sampling data. J Theor Biol. 2019;464:98–103. PubMed
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
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 PMC
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 PMC
Jirtle R, Skinner M. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253–262. PubMed PMC
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 PMC
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.
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. PubMed
Pikula J, Amelon SK, Bandouchova H, et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS One. 2017;12:1–21. PubMed PMC
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
Andrews S 2010. FastQC: a quality control tool for high throughput sequence data. [cited 2016 July28]. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30(15):2114–2120. PubMed PMC
Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357. PubMed PMC
Zerbino DR, Achuthan P, Akanni W, et al. Ensembl 2018. Nucleic Acids Res. 2018;46:D754–D761. PubMed PMC
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinforma. 2014;30:923–930. PubMed
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 PMC
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 PMC
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 PMC
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12. DOI:10.1186/1471-2105-12-323 PubMed DOI PMC
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 PMC
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. PubMed PMC
Bates DM, Maechler M, Bolker B, et al. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014;15:55. PubMed PMC
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma. 2010;26:139–140. PubMed PMC
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. PubMed PMC
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 PMC
Klopfenstein DV, Zhang L, Pedersen BS, et al. GOATOOLS: A python library for gene ontology analyses. Sci Rep. 2018;8:10872. PubMed PMC
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 PMC
Chen C, Huang H, Wu CH. Protein bioinformatics databases and resources. Methods Mol Biol. 2017;1558:3–39. PubMed PMC
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 PubMed PMC
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. PubMed PMC
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 PMC
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
Pikula J, Bandouchova H, Novotný L, et al. Histopathology confirms white-nose syndrome in bats in Europe. J Wildl Dis. 2013;48:207–211. PubMed
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
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 PMC
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.
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:10.1038/s41598-018-33975-x. PubMed DOI PMC
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 PMC
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 PMC
Auteri GG, Knowles LL. Decimated little brown bats show potential for adaptive change. Sci Rep. 2020;10:1–10. PubMed PMC
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. PubMed
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
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 PMC
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.
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 PMC
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