Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682 (2010).
Google Scholar
Froschauer, A. & Coleman, J. North American bat death toll exceeds 5.5 million from white-nose syndrome. Biol. Rep. US Fish Wildl. Serv. 2, 1–2 (2012).
Blehert, D. S. et al. Bat white-nose syndrome: An emerging fungal pathogen?. Science 323, 227 (2009).
Google Scholar
Meteyer, C. U. et al. Histopathologic criteria to confirm white-nose syndrome in bats. J. Vet. Diagn. Invest. 21, 411–414 (2009).
Google Scholar
O’Donoghue, A. J. et al. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc. Natl. Acad. Sci. USA. 112, 7478–7483 (2015).
Google Scholar
Cryan, P. M., Meteyer, C. U., Boyles, J. G. & Blehert, D. S. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 8, 135 (2010).
Google Scholar
Warnecke, L. et al. Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality. Biol. Lett. 9, 20130177 (2013).
Google Scholar
Verant, M. L., Boyles, J. G., Waldrep, W., Wibbelt, G. & Blehert, D. S. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7, e46280 (2012).
Google Scholar
Field, K. A. et al. The white-nose syndrome transcriptome: Activation of anti-fungal host responses in wing tissue of hibernating little brown Myotis. PLoS Pathog. 11, e1005168 (2015).
Google Scholar
Boyles, J. G. & Willis, C. K. R. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome?. Front. Ecol. Environ. 8, 92–98 (2010).
Google Scholar
Storm, J. J. & Boyles, J. G. Body temperature and body mass of hibernating little brown bats Myotis lucifugus in hibernacula affected by white-nose syndrome. Acta Theriol. 56, 123–127 (2011).
Google Scholar
Lorch, J. M. et al. First detection of bat white-nose syndrome in western North America. MSphere 1, 4 (2016).
Google Scholar
White-Nose Syndrome Response Team. Where is WNS Now? White-Nose Syndrome https://www.whitenosesyndrome.org/spreadmap (2021).
Turner, G. G., Reeder, D. & Coleman, J. T. H. A five-year assessment of mortality and geographic spread of white-nose syndrome in north American bats, with a look at the future: update of white-nose syndrome in bats. Bat Res. News 52, 13 (2011).
Dzal, Y., McGuire, L. P., Veselka, N. & Fenton, M. B. Going, going, gone: The impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus). Biol. Lett. 7, 392–394 (2011).
Google Scholar
Ingersoll, T. E., Sewall, B. J. & Amelon, S. K. Improved analysis of long-term monitoring data demonstrates marked regional declines of bat populations in the eastern United States. PLoS ONE 8, e65907 (2013).
Google Scholar
Vanderwolf, K. J. & McAlpine, D. F. Hibernacula microclimate and declines in overwintering bats during an outbreak of white-nose syndrome near the northern range limit of infection in North America. Ecol. Evol. 11, 2273–2288 (2021).
Google Scholar
Boyles, J. G., Cryan, P. M., McCracken, G. F. & Kunz, T. H. Economic importance of bats in agriculture. Science 332, 41–42 (2011).
Google Scholar
Kunz, T. H., de Torrez, E. B., Bauer, D., Lobova, T. & Fleming, T. H. Ecosystem services provided by bats. Ann. N. Y. Acad. Sci. 1223, 1–38 (2011).
Google Scholar
Puig‐Montserrat, X. & Flaquer, C. Bats actively prey on mosquitoes and other deleterious insects in rice paddies: Potential impact on human health and agriculture. Pest Manag. Sci. (2020).
Micalizzi, E. W. & Smith, M. L. Volatile organic compounds kill the white-nose syndrome fungus, Pseudogymnoascus destructans, in hibernaculum sediment. Can. J. Microbiol. 66, 593–599 (2020).
Google Scholar
Padhi, S., Dias, I., Korn, V. & Bennett, J. Pseudogymnoascus destructans: Causative agent of white-nose syndrome in bats is inhibited by safe volatile organic compounds. Journal of Fungi 4, 48 (2018).
Google Scholar
Chaturvedi, S. et al. Antifungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of geomycosis (WNS) in bats. PLoS ONE 6, e17032 (2011).
Google Scholar
Cornelison, C. T. et al. A preliminary report on the contact-independent antagonism of Pseudogymnoascus destructans by Rhodococcus rhodochrous strain DAP96253. BMC Microbiol. 14, 246 (2014).
Google Scholar
Boire, N. et al. Potent inhibition of Pseudogymnoascus destructans, the causative agent of white-nose syndrome in bats, by cold-pressed, terpeneless, Valencia orange oil. PLoS ONE 11, 1–10 (2016).
Google Scholar
Padhi, S., Dias, I. & Bennett, J. W. Two volatile-phase alcohols inhibit growth of Pseudogymnoascus destructans, causative agent of white-nose syndrome in bats. Mycology 8, 11–16 (2017).
Google Scholar
Raudabaugh, D. B. & Miller, A. N. Effect of Trans, trans-farnesol on Pseudogymnoascus destructans and several closely related species. Mycopathologia 180, 325–332 (2015).
Google Scholar
Kulhanek. The Application of Chitosan on an Experimental Infection of Pseudogymnoascus Destructans Increases Survival in Little Brown Bats. (Western Michigan University, 2016).
Ghosh, S. et al. Evidence for Anti-Pseudogymnoascus destructans (Pd) activity of propolis. Antibiotics 7, 2 (2017).
Google Scholar
Bernard, R. F. & Grant, E. H. C. Identifying common decision problem elements for the management of emerging fungal diseases of wildlife. Soc. Nat. Resour. (2019).
Haas, D. & Défago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3, 307–319 (2005).
Google Scholar
Becker, M. H. & Harris, R. N. Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS ONE 5, e10957 (2010).
Google Scholar
Gerritsen, J., Smidt, H., Rijkers, G. T. & de Vos, W. M. Intestinal microbiota in human health and disease: The impact of probiotics. Genes Nutr. 6, 209–240 (2011).
Google Scholar
Bletz, M. C. et al. Mitigating amphibian chytridiomycosis with bioaugmentation: Characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16, 807–820 (2013).
Google Scholar
Becker, M. H. et al. Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proc. Biol. Sci. 282, 2881 (2015).
Hamm, P. S. et al. Western bats as a reservoir of novel Streptomyces species with antifungal activity. Appl. Environ. Microbiol. 83, 1–10 (2017).
Google Scholar
Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE https://doi.org/10.1371/journal.pone.0121329 (2015).
Google Scholar
Cheng, T. L. et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J. Appl. Ecol. 54, 701–708 (2017).
Google Scholar
Berg, G. & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1–13 (2009).
Google Scholar
Teplitski, M. & Ritchie, K. How feasible is the biological control of coral diseases?. Trends Ecol. Evol. 24, 378–385 (2009).
Google Scholar
Clay, K. EDITORIAL: Defensive symbiosis: A microbial perspective. Funct. Ecol. 28, 293–298 (2014).
Google Scholar
Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).
Google Scholar
Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl. Acad. Sci. USA. 111, E5049–E5058 (2014).
Google Scholar
Lemieux-Labonté, V., Simard, A., Willis, C. K. R. & Lapointe, F.-J. Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5, 115 (2017).
Google Scholar
Walke, J. B. et al. Most of the dominant members of amphibian skin bacterial communities can be readily cultured. Appl. Environ. Microbiol. 81, 6589–6600 (2015).
Google Scholar
Avena, C. V. et al. Deconstructing the bat skin microbiome: Influences of the host and the environment. Front. Microbiol. 7, 1753 (2016).
Google Scholar
Loudon, A. H. et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J. 8, 830–840 (2014).
Google Scholar
Walke, J. B. et al. Amphibian skin may select for rare environmental microbes. ISME J. 8, 2207–2217 (2014).
Google Scholar
Loudon, A. H. et al. Vertebrate hosts as islands: Dynamics of selection, immigration, loss, persistence, and potential function of bacteria on salamander skin. Front. Microbiol. 7, 333 (2016).
Google Scholar
Winter, A. S. et al. Skin and fur bacterial diversity and community structure on American southwestern bats: Effects of habitat, geography and bat traits. PeerJ 5, e3944 (2017).
Google Scholar
Perofsky, A. C., Lewis, R. J., Abondano, L. A., Di Fiore, A. & Meyers, L. A. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. Proc. Biol. Sci. 284, 2274 (2017).
Raulo, A. et al. Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality. J. Anim. Ecol. 87, 388–399 (2018).
Google Scholar
Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. Elife 4, 5224 (2015).
Kolodny, O. et al. Coordinated change at the colony level in fruit bat fur microbiomes through time. Nat. Ecol. Evol. 3, 116–124 (2019).
Google Scholar
Vuong, H. E., Yano, J. M., Fung, T. C. & Hsiao, E. Y. The microbiome and host behavior. Annu. Rev. Neurosci. 40, 21–49 (2017).
Google Scholar
Lausen, C. L., Nagorsen, D. N., Brigham, R. M. & Hobbs, J. Bats of British Columbia 2nd edn. (Royal BC Museum, 2022).
Spring Cleaning: Why Wash a Bridge? https://www.tranbc.ca/2011/06/22/spring-cleaning-why-wash-a-bridge/ (2012).
Maron, P.-A. et al. High microbial diversity promotes soil ecosystem functioning. Appl. Environ. Microbiol. 84, 9 (2018).
Google Scholar
Wagg, C., Bender, S. F., Widmer, F. & van der Heijden, M. G. A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. USA. 111, 5266–5270 (2014).
Google Scholar
Green, S. R. & Gray, P. P. A differential procedure for bacteriological studies useful in the fermentation industry. Arch. Biochem. Biophys. 32, 59–69 (1951).
Google Scholar
Basu, S. et al. Evolution of bacterial and fungal growth media. Bioinformation 11, 182–184 (2015).
Google Scholar
Medina, D. et al. Culture media and individual hosts affect the recovery of culturable bacterial diversity from amphibian skin. Front. Microbiol. 8, 1574 (2017).
Google Scholar
Piovia-Scott, J. et al. Greater species richness of bacterial skin symbionts better suppresses the amphibian fungal pathogen Batrachochytrium dendrobatidis. Microb. Ecol. 74, 217–226 (2017).
Google Scholar
Moeller, A. H. et al. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc. Natl. Acad. Sci. USA. 114, 13768–13773 (2017).
Google Scholar
Ingala, M. R. et al. Comparing microbiome sampling methods in a wild mammal: Fecal and intestinal samples record different signals of host ecology, evolution. Front. Microbiol. 9, 1–10 (2018).
Google Scholar
Lewis, S. E. Night roosting ecology of pallid bats (Antrozous pallidus) in oregon. Am. Midl. Nat. 132, 219–226 (1994).
Google Scholar
Hershey, O. S. & Barton, H. A. The microbial diversity of caves. Cave Ecol. 1, 69–90. https://doi.org/10.1007/978-3-319-98852-8_5 (2018).
Google Scholar
British Columbia Government Mineral Inventory. https://www2.gov.bc.ca/gov/content/industry/mineral-exploration-mining/british-columbia-geological-survey/mineralinventory (2018).
Weller, T. J. et al. A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management. PLoS ONE 13, e0205647 (2018).
Google Scholar
Nagorsen, D. W., Brigham, R. M., Royal British Columbia Museum. Bats of British Columbia (UBC Press, 1993).
Fenton, M. B., Merriam, H. G. & Holroyd, G. L. Bats of Kootenay, Glacier, and Mount Revelstoke national parks in Canada: Identification by echolocation calls, distribution, and biology. Can. J. Zool. 61, 2503–2508 (1983).
Google Scholar
Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L. & McCracken, G. F. Molecular detection of the causative agent of white-nose syndrome on rafinesque’s big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the Southeastern USA. J. Wildl. Dis. 51, 519–522 (2015).
Google Scholar
Lutz, H. L. et al. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. MSystems 4, 1–10 (2019).
Gaona, O., Gómez-Acata, E. S., Cerqueda-García, D., Neri-Barrios, C. X. & Falcón, L. I. Fecal microbiota of different reproductive stages of the central population of the lesser-long nosed bat, Leptonycteris yerbabuenae. PLoS ONE 14, e0219982 (2019).
Google Scholar
Voigt, C. C., Caspers, B. & Speck, S. Bats, bacteria, and bat smell: Sex-specific diversity of microbes in a sexually selected scent organ. J. Mammal. 86, 745–749 (2005).
Google Scholar
Gharout-Sait, A. et al. Occurrence of carbapenemase-producing Klebsiella pneumoniae in bat guano. Microb. Drug Resist. 25, 1057–1062 (2019).
Google Scholar
Sánchez, C. et al. Contribution of citrate metabolism to the growth of Lactococcus lactis CRL264 at low pH. Appl. Environ. Microbiol. 74, 1136–1144 (2008).
Google Scholar
Charyulu, E. M. & Gnanamani, A. Condition stabilization for Pseudomonas aeruginosa MTCC 5210 to yield high titers of extra cellular antimicrobial secondary metabolite using response surface methodology. Curr. Res. Bacteriol. 4, 197–213 (2010).
Google Scholar
Shen, Y. et al. Psychrobacillus lasiicapitis sp. nov., isolated from the head of an ant (Lasius fuliginosus). Int. J. Syst. Evol. Microbiol. 67, 4462–4467 (2017).
Google Scholar
Rodríguez, M., Reina, J. C., Béjar, V. & Llamas, I. Psychrobacillus vulpis sp. nov., a new species isolated from faeces of a red fox in Spain. Int. J. Syst. Evol. Microbiol. 70, 882–888 (2020).
Google Scholar
Pham, V. H. T., Jeong, S.-W. & Kim, J. Psychrobacillus soli sp. nov., capable of degrading oil, isolated from oil-contaminated soil. Int. J. Syst. Evol. Microbiol. 65, 3046–3052 (2015).
Google Scholar
Kontro, M., Lignell, U., Hirvonen, M.-R. & Nevalainen, A. pH effects on 10 Streptomyces spp. growth and sporulation depend on nutrients. Lett. Appl. Microbiol. 41, 32–38 (2005).
Google Scholar
Wodzinski, R. S., Umholtz, T. E., Rundle, J. R. & Beer, S. V. Mechanisms of inhibition of Erwinia amylovora by Erw. herbicola in vitro and in vivo. J. Appl. Bacteriol. 76, 22–29 (1994).
Google Scholar
Kuncharoen, N. et al. Achromobacter aloeverae sp. nov., isolated from the root of Aloe vera (L.) Burm. f. Int. J. Syst. Evol. Microbiol. 67, 37–41 (2017).
Google Scholar
Aizawa, T. et al. Curtobacterium ammoniigenes sp. nov., an ammonia-producing bacterium isolated from plants inhabiting acidic swamps in actual acid sulfate soil areas of Vietnam. Int. J. Syst. Evol. Microbiol. 57, 1447–1452 (2007).
Google Scholar
Kaira, G. S., Dhakar, K. & Pandey, A. A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range. AMB Express 5, 92 (2015).
Google Scholar
Moon, J. & Kim, J. Isolation of Paenibacillus pinesoli sp. Nov. from forest soil in Gyeonggi-Do, Korea. J. Microbiol. 52, 273–277 (2014).
Google Scholar
Heyrman, J. et al. Bacillus novalis sp. nov., Bacillus vireti sp. nov., Bacillus soli sp. nov., Bacillus bataviensis sp. nov. and Bacillus drentensis sp. nov., from the Drentse A grasslands. Int. J. Syst. Evol. Microbiol. 54, 47–57 (2004).
Google Scholar
Hughes, K. L. & Sulaiman, I. The ecology of Rhodococcus equi and physicochemical influences on growth. Vet. Microbiol. 14, 241–250 (1987).
Google Scholar
Schrempf, H. Recognition and degradation of chitin by streptomycetes. Antonie Van Leeuwenhoek 79, 285–289 (2001).
Google Scholar
Seco, E. M., Cuesta, T., Fotso, S., Laatsch, H. & Malpartida, F. Two polyene amides produced by genetically modified Streptomyces diastaticus var. 108. Chem. Biol. 12, 535–543 (2005).
Google Scholar
Kembel, S. W., Wu, M., Eisen, J. A. & Green, J. L. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput. Biol. 8, e1002743 (2012).
Google Scholar
León, M. et al. Antifungal activity of selected indigenous pseudomonas and bacillus from the soybean rhizosphere. Int. J. Microbiol. 2009, 572049 (2009).
Google Scholar
Van Hai, N. & Fotedar, R. Comparison of the effects of the prebiotics (Bio-Mos® and β-1, 3-D-glucan) and the customised probiotics (Pseudomonas synxantha and P. aeruginosa) on the culture of juvenile western king prawns (Penaeus latisulcatus Kishinouye, 1896). Aquaculture 289, 310–316 (2009).
Google Scholar
Lauer, A., Simon, M. A., Banning, J. L., Lam, B. A. & Harris, R. N. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J. 2, 145–157 (2008).
Google Scholar
Ligon, J. M. et al. Natural products with antifungal activity fromPseudomonas biocontrol bacteria. Pest Manag. Sci. 56, 688–695 (2000).
Google Scholar
Scholz-Schroeder, B. K., Hutchison, M. L., Grgurina, I. & Gross, D. C. The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol. Plant Microb. Interact. 14, 336–348 (2001).
Google Scholar
Souza, J. T. & Raaijmakers, J. M. Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS Microbiol. Ecol. 43, 21–34 (2003).
Google Scholar
Mavrodi, D. V. et al. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J. Bacteriol. 183, 6454–6465 (2001).
Google Scholar
Diby, P. et al. Mycolytic enzymes produced by Pseudomonas fluorescens and Trichoderma spp. against Phytophthora capsici, the foot rot pathogen of black pepper (Piper nigrum L.). Ann. Microbiol. 55, 129–133 (2005).
Google Scholar
Vengust, M., Knapic, T. & Weese, J. S. The fecal bacterial microbiota of bats; Slovenia. PLoS ONE 13, e0196728 (2018).
Google Scholar
Banskar, S., Mourya, D. T. & Shouche, Y. S. Bacterial diversity indicates dietary overlap among bats of different feeding habits. Microbiol. Res. 182, 99–108 (2016).
Google Scholar
Wolkers-Rooijackers, J. C. M., Rebmann, K., Bosch, T. & Hazeleger, W. C. Fecal Bacterial Communities in Insectivorous Bats from the Netherlands and Their Role as a Possible Vector for Foodborne Diseases. Acta Chiropterol. 20, 475 (2019).
Google Scholar
Weller, T. J., Scott, S. A., Rodhouse, T. J., Ormsbee, P. C. & Zinck, J. M. Field identification of the cryptic vespertilionid bats, Myotis lucifugus and M. yumanensis. Acta Chiropt. 9, 133–147 (2007).
Google Scholar
Khankhet, J. et al. Clonal expansion of the Pseudogymnoascus destructans genotype in North America is accompanied by significant variation in phenotypic expression. PLoS ONE 9, e104625 (2014).
Google Scholar
McArthur, R. L., Ghosh, S. & Cheeptham, N. Improvement of protocols for the screening of biological control agents against white-nose syndrome. JEMI 2, 1–7 (2017).
Rajkumar, S. S. et al. Clonal genotype of Geomyces destructans among bats with white nose syndrome, New York, USA. Emerg. Infect. Dis. 17, 1273–1276 (2011).
Google Scholar
Ren, P. et al. Clonal spread of Geomyces destructans among bats, Midwestern and Southern United States. Emerg. Infect. Dis. 18, 883–885 (2012).
Google Scholar
Wilson, K. Genomc DNA extraction using the modified CTAB method. Curr. Protoc. Mol. Biol. 1, 1–2 (1997).
Edwards, U., Rogall, T., Blöcker, H., Emde, M. & Böttger, E. C. Isolation and direct complete nucleotide determination of entire genes: Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17, 7843–7853 (1989).
Google Scholar
Stackebrandt, E. & Liesack, W. Handbook of New Bacterial Systematics (Springer, 1993).
O’Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).
Google Scholar
Camacho, C. et al. BLAST+: Architecture and applications. BMC Bioinformatics 10, 421 (2009).
Google Scholar
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Google Scholar
Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2015).
Venables, W. N. & Ripley, B. D. Modern applied statistics with S. Stat. Comput. https://doi.org/10.1007/978-0-387-21706-2 (2002).
Google Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Google Scholar
Lenth, R. & Lenth, M. R. Package ‘lsmeans’. Am. Stat. 34, 216–221 (2018).
Kassambara, A. ggpubr:‘ggplot2’ based publication ready plots. R package version 0.1. 7 (2018).
Source: Ecology - nature.com
