278
Views
3
CrossRef citations to date
0
Altmetric
Ecology

Remarkable fungal biodiversity on northern Belgium bats and hibernacula

ORCID Icon, , , , , , & show all
Pages 484-498 | Received 19 Nov 2021, Accepted 09 May 2023, Published online: 08 Jun 2023

LITERATURE CITED

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215(3):403–410. doi:10.1016/S0022-2836(05)80360-2.
  • Ange-Stark M, Cheng TL, Hoyt JR, Langwig KE, Parise KL, Frick WF, Kilpatrick AM, MacManes MD, Foster JT. 2019. White-nose syndrome restructures bat skin microbiomes. bioRxiv. preprint. doi:10.1101/614842.
  • Becker P, de Bel A, Martiny D, Ranque S, Piarroux R, Cassagne C, Detandt M, Hendrickx M. 2014. Identification of filamentous fungi isolates by MALDI-TOF mass spectrometry: clinical evaluation of an extended reference spectra library. Med Mycol. 52(8):826–834. doi:10.1093/mmy/myu064.
  • Berbee M, Pirseyedi M, Hubbard S. 1999. Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia. 91(6):964–977. doi:10.1080/00275514.1999.12061106.
  • Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, et al. 2009. Bat white-nose syndrome: an emerging fungal pathogen? Science. 323(5911):227. doi:10.1126/science.1163874.
  • Borda DR, Nastase-Bucur RM, Spinu M, Uricariu R, Mulec J. 2014. Aerosolized microbes from organic rich materials: case study of bat guano from caves in Romania. J Cave Karts Stud. 76(2):114–126. doi:10.4311/2013MB0116.
  • Carbone I, Kohn LM. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia. 91(3):553–56. doi:10.1080/00275514.1999.12061051.
  • Chao A, Jost L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology. 93(12):2533–2547. doi:10.1890/11-1952.1.
  • Crous PW, Cowan DA, Maggs-Kölling G, Yilmaz N, Larsson E, Angelini C, Brandrud TE, Dearnaley JDW, Dima B, Dovana F, et al. 2020. Fungal Planet description sheets: 1112–1181. Persoonia. 45:251–409. doi:10.3767/persoonia.2020.45.10.
  • Crous PW, Wingfield MJ, Lombard L, Roets F, Swart WJ, Alvarado P, Carnegie AJ, Moreno G, Luangsa-ard J, Thangavel R, et al. 2019. Fungal Planet description sheets: 951–1041. Persoonia. 43:223–425. doi:10.3767/persoonia.2019.43.06.
  • Drees KP, Lorch JM, Puechmaille SJ, Parise KL, Wibbelt G, Hoyt JR, Sun K, Jargalsaikhan A, Dalannast M, Palmer JM, et al. 2017. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio. 8(6):e01941–e17. doi:10.1128/mBio.01941-17.
  • Fenster SD, Navo K, Betancur A, Hubbard D, Reese C, Lehmer EM. 2019. Examination of fungal diversity present on Mexican free-tailed bats, Tadarida brasiliensis mexicana, in Colorado. Southwest Nat. 63:256–267.
  • Fischer NM, Altewischer A, Ranpal S, Dool S, Kerth G, Puechmaille SJ. 2022. Population genetics as a tool to elucidate pathogen reservoirs: lessons from Pseudogymnoascus destructans, the causative agent of White-Nose disease in bats. Mol Ecol. 31(2):675–690. doi:10.1111/mec.16249.
  • Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH. 2010. An emerging disease causes regional population collapse of a common North American bat species. Science. 329(5992):679–682. doi:10.1126/science.1188594.
  • Furtado BG, Savi GD, Angioletto E, Carvalho F. 2020. Filamentous fungi occurrence on Molossus molossus (Pallas, 1766) (Chiroptera: Molossidae) present in an Atlantic Forest remnant in Sothern Brazil. Braz J Biol. 81:1073–1080. doi:10.1590/1519-6984.235374.
  • Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS. 2009. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon. 108(1):147–154. doi:10.5248/108.147.
  • Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 61(4):1323–30. doi:10.1128/aem.61.4.1323-1330.1995.
  • Good IJ. 1953. The population frequencies of species and the estimation of population parameters. Biometrika. 40(3–4):237–264. doi:10.1093/biomet/40.3-4.237.
  • Holz PH, Lumsden LF, Marenda MS, Browning GF, Hufschmid J. 2018. Two subspecies of bent-winged bats (Miniopterus orianae and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLoS ONE. 13:e0204282. doi:10.1371/journal.pone.0204282.
  • Hubka V, Cmokova A, Skorepova M, Mikula P, Kolarik M. 2014. Trichophyton onychocola sp. nov. isolated from human nail. Med Mycol. 52(3):285–292. doi:10.1093/mmy/myt010.
  • Hubka V, Nissen CV, Jensen RH, Arendrup MC, Cmokova A, Kubatova A, Skorepov M, Kolarik M. 2015. Discovery of a sexual stage in Trichophyton onychocola, a presumed geophilic dermatophyte isolate from toenails of patients with a history of T. rubrum onychomycosis. Med Mycol. 53:798–809. doi:10.1093/mmy/myv044.
  • Imbert S, Normand AC, Cassaing S, Gabriel F, Kristensen L, Bonnal C, Lachaud L, Costa D, Guitard J, Hasseine L, et al. 2020. Multicentric analysis of the species distribution and antifungal susceptibility of cryptic isolates from Aspergillus section Fumigati. Antimicrob Agents Chemother. 64(12):e01374–e20. doi:10.1128/AAC.01374-20.
  • Janicki AF, Frick WF, Kilpatrick AM, Parise KL, Foster JT, McCracken GF. 2015. Efficacy of visual surveys for white-nose syndrome at bat hibernacula. PLoS ONE. 10:e133390. doi:10.1371/journal.pone.0133390.
  • Johnson LJAN, Miller AN, McCleery RA, McClanahan R, Kath JA, Lueschow S, Porras-Alfaro A. 2013. Psychrophilic and psychrotolerant fungi on bats and the presence of Geomyces spp. on bat wings prior to the arrival of white nose syndrome. Appl Environ Microbiol. 79(18):5465–5471. doi:10.1128/AEM.01429-13.
  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 14(6):587–589. doi:10.1038/nmeth.4285.
  • Kokurewicz T, Ogorek R, Pusz W, Matkowski K. 2016. Bats increase the number of cultivable airborne fungi in the “Nietoperek” bat reserve in Western Poland. Microb Ecol. 72(1):36–48. doi:10.1007/s00248-016-0763-3.
  • Kurtzman C, Fell JW, Boekhout T. 2011. The yeasts, a taxonomic study. 5th ed. London (UK): Elsevier Science.
  • Leopardi S, Blake D, Puechmaille SJ. 2015. White-nose syndrome fungus introduced from Europe to North America. Curr Biol. 25(6):R217–R219. doi:10.1016/j.cub.2015.01.047.
  • Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA, et al. 2016. Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 78:1–237.
  • Li Z, Li A, Dai W, Leng H, Liu S, Jin L, Sun K, Feng J. 2022b. Skin microbiota variation among bat species in China and their potential defence against pathogens. Front Microbiol. 13:808788. doi:10.3389/fmicb.2022.808788.
  • Li A, Li Z, Dai W, Parise KL, Leng H, Jin L, Liu S, Sun K, Hoyt JR, Feng J. 2022a. Bacterial community dynamics on bats and the implications for pathogen resistance. Environ Microbiol. 24(3):1484–1498. doi:10.1111/1462-2920.15754.
  • Liu YJ, Whelen S, Hall BD. 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol. 16(12):1799–1808. doi:10.1093/oxfordjournals.molbev.a026092.
  • Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM, Blehert DS. 2013. A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia. 105(2):237–252. doi:10.3852/12-207.
  • Manitchotpisit P, Leathers TD, Peterson SW, Kurtzman CP, Li X-L, Eveleigh DE, Lotrakul P, Prasongsuk S, Dunlap CA, Vermillion KE, et al. 2009. Multilocus phylogenetic analyses, pullulan production and xylanase activity of tropical isolates of Aureobasidium pullulans. Mycol Res. 113(10):1107–1120. doi:10.1016/j.mycres.2009.07.008.
  • Martinkova N, Backor P, Bartonicka T, Blazkova P, Cerveny J, Falteisek L, Gaisler J, Hanzal V, Horacek D, Hubalek Z, et al. 2010. Increasing incidence of Geomyces destructans fungus in bats from Czech Republic and Slovakia. PLoS ONE. 11:e13853. doi:10.1371/journal.pone.0013853.
  • Matheny PB, Liu YJ, Ammirati JF, Hall BD. 2002. Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot. 89(4):688–698. doi:10.3732/ajb.89.4.688.
  • Miller AN, Huhndorf SM. 2005. Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi). Mol Phylogenet Evol. 35(1):60–75. doi:10.1016/j.ympev.2005.01.007.
  • Minnis AM, Lindner DL. 2013. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 117(9):638–49. doi:10.1016/j.funbio.2013.07.001.
  • Njus KA. 2014. Molecular techniques for the identification of commensal fungal populations on cave roosting bats [ Master’s thesis]. University of Akron, p. 101. [accessed 2023 Apr 19]. http://rave.ohiolink.edu/etdc/view?acc_num=akron1403716687.
  • Normand A-C, Cassagne C, Ranque S, L’Ollivier C, Fourquet P, Roesems S, Hendrickx M, Piarroux R. 2013. Assessment of various parameters to improve MALDI-TOF MS reference spectra libraries constructed for the routine identification of filamentous fungi. BMC Microbiol. 13(1):76. doi:10.1186/1471-2180-13-76.
  • O’Donnell K, Cigelnik E. 1997. Two devergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol. 7:103–16. doi:10.1006/mpev.1996.0376.
  • O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC. 1998. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci. 95:2044–2049.
  • O’Donnell K, Nirenberg HI, Aoki T, Cigelnik E. 2000. A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience. 41(1):61–78. doi:10.1007/BF02464387.
  • Ogorek R, Kurczaba K, Cal M, Apoznanski G, Kokurewicz T. 2020. A culture-based ID of micromycetes on the wing membranes of greater mouse-eared bats (Myotis myotis) from the Nietoperek site (Poland). Animals. 10:1337. doi:10.3390/ani10081337.
  • Peterson SW. 2008. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia. 100(2):205–26. doi:10.1080/15572536.2008.11832477.
  • Pikula J, Amelon SK, Bandouchova H, Bartonicka T, Berkova H, Brichta J, Hooper S, Kokurewicz T, Kolarik M, Kollner B, et al. 2017. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE. 12(8):e0180435. doi:10.1371/journal.pone.0180435.
  • Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Muhldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, et al. 2011. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE. 6(4):e19167. doi:10.1371/journal.pone.0019167.
  • Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, Razavi M, Mirzadi Gohari A, Mehrabi R, Crous PW. 2011. Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia. 26:57–69. doi:10.3767/003158511X571841.
  • Rehner SA, Buckley E. 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia. 97:84–98. doi:10.3852/mycologia.97.1.84.
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61(3):539–542. doi:10.1093/sysbio/sys029.
  • Rudolph S, Macia-Vicente JG, Lotz-Winter H, Schleuning M, Piepenbring M. 2018. Temporal variation of fungal diversity in a mosaic landscape in Germany. Stud Mycol. 89(1):95–104. doi:10.1016/j.simyco.2018.01.001.
  • Sandoval-Denis M, Guarro J, Cano-Lira JF, Sutton DA, Wiederhold NP, de Hoog GS, Abbott SP, Decock C, Sigler L, Gené J. 2016. Phylogeny and taxonomic revision of Microascaceae with emphasis on synnematous fungi. Stud Mycol. 83(1):193–233. doi:10.1016/j.simyco.2016.07.002.
  • Shapiro JT, Rocha Dos Santos TM, Marchetti CR, Lorenz-Lemke AP, Delarmelina E, Bordignon MO. 2015. Characterization of fungi associated with the nasal hairs of Molossid bats. Fungal Ecol. 18:126–129. doi:10.1016/j.funeco.2015.06.005.
  • Stiller JW, Hall BD. 1997. The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci. 94:4520–4225.
  • Sung GH, Sung JM, Hywel-Jones NL, Spatafora JW. 2007. A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol. 44:1204–1223. doi:10.1016/j.ympev.2007.03.011.
  • Takashima M, Kurakado S, Cho O, Kikuchi K, Sugiyama J, Sugita T. 2020. Description of four Apiotrichum and two Cutaneotrichosporon species isolated from guano samples from bat-inhabited caves in Japan. Int J Syst Evol Microbiol. 70(8):4458–4469. doi:10.1099/ijsem.0.004277.
  • Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44(W1):W232–W235. doi:10.1093/nar/gkw256.
  • Vanderwolf KJ, Campbell LJ, Goldberg TL, Blehert DS, Lorch JM. 2021a. Skin fungal assemblages of bats vary based on susceptibility to white-nose syndrome. ISME J. 15(3):909–920. doi:10.1038/s41396-020-00821-w.
  • Vanderwolf KJ, Campbell LJ, Taylor DR, Goldberg TL, Blehert DS, Lorch JM. 2021b. Mycobiome traits associated with disease tolerance predict many western North American bat species will be susceptible to white-nose syndrome. Microbiol Spectr. 9:e00254–e21. doi:10.1128/Spectrum.00254-21.
  • Vanderwolf KJ, Malloch D, McAlpine D. 2015. Fungi associated with over-wintering tricolored bats, Perimyotis subflavus, in a white-nose syndrome region of Eastern Canada. J Cave Karts Stud. 77:145–151.
  • Vanderwolf KJ, Malloch D, McAlpine D. 2016b. Fungi on white-nose infected bats (Myotis spp.) in Eastern Canada show no decline in diversity associated with Pseudogymnoascus destructans (Ascomycota: Pseudeurotiaceae). Int J Speleol. 45:43–50. doi:10.5038/1827-806X.45.1.1946.
  • Vanderwolf KJ, Malloch D, McAlpine DF. 2016a. Detecting viable Pseudogymnoascus destructans (Ascomycota: Pseudeurotiaceae) from walls of bat hibernacula: effect of culture media. J Cave Karts Stud. 78(3):158–162. doi:10.4311/2015MB0138.
  • Vanderwolf KJ, Malloch D, McAlpine DF, Forbes GJ. 2013. A world review of fungi, yeasts, and slime molds in caves. Int J Speleol. 42(1):77–96. doi:10.5038/1827-806X.42.1.9.
  • Vilgalys R. Conserved primer sequences for PCR amplification of fungal rDNA. Duke University, USA. 2018. [accessed 2023 Apr 19]. https://sites.duke.edu/vilgalyslab/rdna_primers_for_fungi/.
  • Voigt K, Wöstemeyer J. 2000. Reliable amplification of actin genes facilitates deep-level phylogeny. Microbiol Res. 155(3):179–95. doi:10.1016/S0944-5013(00)80031-2.
  • Voyron S, Lazzari A, Riccucci M, Calvini M, Varese GC. 2011. First mycological investigation on Italian bats. Hystrix. 22:189–197.
  • White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols, a guide to methods and applications. San Diego (CA): Academic Press. p. 315–22.
  • Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, Pruger J, Gorfol T, Grosche L, Bontadina F, et al. 2010. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis. 16:1237–42. doi:10.3201/eid1608.100002.
  • Woudenberg JHC, Meijer M, Houbraken J, Samson RA. 2017. Scopulariopsis and Scopulariopsis-like species from indoor environments. Stud Mycol. 88(1):1–35. doi:10.1016/j.simyco.2017.03.001.
  • Zhang Z, Dong C, Chen W, Mou Q, Lu X, Han Y, Huang J, Liang Z. 2020. The enigmatic Thelebolaceae (Thelebolales, Leotiomycetes): one new genus Solomyces and five new species. Front Microbiol. 11:572596. doi:10.3389/fmicb.2020.572596.
  • Zukal J, Bandouchkova H, Brichta J, Cmokova A, Jaron KS, Kolarik M, Kovacova A, Novakova A, Orlov O, Pikula J, et al. 2016. White-nose syndrome without borders: pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep. 6:19829. doi:10.1038/srep19829.
  • Zukal J, Bandouchova H, Bartonicka T, Berkova H, Brack V, Brichta J, Dolinay M, Jaron KS, Kovacova V, Kovarik M, et al. 2014. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS ONE. 9(5):e97224. doi:10.1371/journal.pone.0097224.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.