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Amphichorda monjolensis sp. nov., a new fungal species isolated from a Brazilian limestone cave, with an update on acremonium-like species in Bionectriaceae

  • Environmental Microbiology - Research Paper
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Abstract

Caves are unique environments characterized by spatial limitations, partial or total absence of direct light, and scarcity of organic carbon and nutrients. Caves are shelters for a variety of adapted animals and microorganisms such as fungi, many of which are still unknown. Amphichorda is a fungal genus belonging to the family Bionectriaceae, which includes cave-dwelling and entomopathogenic species with biotechnological applications. In this study, a new fungal species was identified using morphological and multi-locus phylogenetic analyses of the ITS, LSU, and TEF loci, in the Gruta Velha Nova limestone cave located in the Southern Espinhaço Range, Monjolos, Minas Gerais, Brazil. During the exposure of potato dextrose agar plates to the cave environment, an insect from the family Rhaphidophoridae passed by and fed on the culture medium, resulting in three fungal isolates. Phylogenetic analyses showed that these isolates formed a clade distinct from all known species, leading us to introduce a new species, Amphichorda monjolensis, which may be associated with this insect. Here, we also proposed two new combinations for species of acremonium-like fungi in the Bionectriaceae: Bulbithecium globosisporum (synonym: Acremonium globosisporum) and Hapsidospora curva (synonym: Acremonium curvum). The discovery of A. monjolensis highlights the potential of caves as shelters for new species with significant biotechnological importance.

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Data availability

Sequences generated in this work are available at GenBank (https://www.ncbi.nlm.nih.gov/genbank/). DNA alignments and phylogenetic trees are provided in the Electronic Supplementary Material.

References

  1. Guerra-Mateo D, Gené J, Baulin V, Cano-Lira JF (2023) Phylogeny and taxonomy of the genus Amphichorda (Bionectriaceae): An update on beauveria-like strains and description of a novel species from marine sediments. Diversity 15:795. https://doi.org/10.3390/d15070795

    Article  CAS  Google Scholar 

  2. Li X, Zhang ZY, Ren YL, Chen WH, Liang JD, Pan JM, Huang JZ, Liang ZQ, Han YF (2022) Morphological characteristics and phylogenetic evidence reveal two new species of Acremonium (Hypocreales, Sordariomycetes). MycoKeys 91:85–96. https://doi.org/10.3897/mycokeys.91.86257

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hou LW, Giraldo A, Groenewald JZ, Rämä T, Summerbell RC, Huang GZ, Cai L, Crous PW (2023) Redisposition of acremonium-like fungi in Hypocreales. Stud Mycol 105:23–203. https://doi.org/10.3114/sim.2023.105.02

    Article  Google Scholar 

  4. Zhang ZF, Zhou SY, Eurwilaichitr L, Ingsriswang S, Raza M (2021) Culturable mycobiota from Karst caves in China II, with descriptions of 33 new species. Fungal Divers. https://doi.org/10.1007/s13225-020-00453-7

    Article  PubMed  PubMed Central  Google Scholar 

  5. Zhang ZF, Liu F, Zhou X, Liu XZ, Liu SJ, Cai L (2017) Culturable mycobiota from Karst caves in China, with descriptions of 20 new species. Persoonia 39:1–31. https://doi.org/10.3767/persoonia.2017.39.01

    Article  PubMed  PubMed Central  Google Scholar 

  6. Langenfeld A, Blond A, Gueye S, Herson P, Nay B, Dupont J, Prado S (2011) Insecticidal Cyclodepsipeptides from Beauveria felina. J Nat Prod 74:825–830. https://doi.org/10.1021/np100890n

    Article  PubMed  CAS  Google Scholar 

  7. Liu XF, Tibpromma S, Hughes AC, Chethana KWT, Wijayawardene NN, Dai DQ, Du TY, Elgorban AM, Stephenson SL, Suwannarach N, Xu JC, Lu L, Xu RF, Maharachchikumbura SSN, Zhao CL, Bhat DJ, Sun YM, Karunarathna SC, Mortimer PE (2023) Culturable mycobiota on bats in central and southern Yunnan Province,. Mycosphere 14(1):497–662. https://doi.org/10.5943/mycosphere/14/1/7

    Article  Google Scholar 

  8. Joshi SR, Chettri U (2019) Fungi in hypogean environment: bioprospection perspective. In: Satyanarayana T, Deshmukh SK, Deshpande MV (eds) Advancing frontiers in mycology & mycotechnology. Springer Singapore, Singapore, pp 539–561

    Chapter  Google Scholar 

  9. Poulson TL, White WB (1969) The cave environment: limestone caves provide unique natural laboratories for studying biological and geological processes. Science 165:971–981

    Article  ADS  PubMed  CAS  Google Scholar 

  10. Jurado V, Sáiz-Jiménez C (2016) Vida microbiana en las cavernas: el fascinante mundo de la biodiversidad subterránea y su papel en los procesos de deterioro. Enseñanza Cienc Tierra 24:51–60

    Google Scholar 

  11. Taylor ELS, Stoianoff MAR, Ferreira RL (2013) Mycological study for a management plan of a neotropical show cave (Brazil). Int J Speleol 42:267–277

    Article  Google Scholar 

  12. Nováková A (2009) Microscopic fungi isolated from the Domica Cave system (Slovak Karst National Park, Slovakia). A review. Int J Sport Nutr 38:71–82

    Google Scholar 

  13. Vanderwolf KJ, Malloch D, Mcalpine DF, Forbes GJ (2013) A world review of fungi, yeasts, and slime molds in caves. Int J Speleol 42:77–96

    Article  Google Scholar 

  14. Dobat K (1967) Ein bisher unveroffentlichtes botanisches manuscript Alexander von Humboldts: plantae subterranae Europ (1794) cum Iconibus. Akad Wiss Lit 6:16–19

    Google Scholar 

  15. Held BW, Salomon CE, Blanchette RA (2021) Diverse subterranean fungi of an underground iron ore mine. PLoS ONE. https://doi.org/10.1371/journal.pone.0234208

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zhang ZF, Zhao P, Cai L (2018) Origin of cave fungi. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01407

    Article  PubMed  PubMed Central  Google Scholar 

  17. Cunha AOB, Bezerra JDP, Oliveira TGL, Barbier E, Bernard E, Machado AR, Souza-Motta CM (2020) Living in the dark: Bat caves as hotspots of fungal diversity. PLoS ONE. https://doi.org/10.1371/journal.pone.0243494

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jiang JR, Cai L, Liu F (2017) Oligotrophic fungi from a carbonate cave, with three new species of Cephalotrichum. Mycology 8:164–177

    Article  CAS  Google Scholar 

  19. Pereira MLS, Carvalho JLVR, Lima JMS, Barbier E, Bernard E, Bezerra JDP, Souza-Motta CM (2022) Richness of cladosporium in a tropical bat cave w ith the description of two new species. Mycol Prog 21:345–357. https://doi.org/10.1007/s11557-021-01760-2

    Article  Google Scholar 

  20. Carvalho JLVR, Lima JMS, Barbier E, Bernard E, Bezerra JDP, Souza-Motta CM (2022) Ticket to ride: fungi from bat ectoparasites in a tropical cave and the description of two new species. Braz J Microbiol. https://doi.org/10.1007/s42770-022-00841-y

    Article  PubMed  PubMed Central  Google Scholar 

  21. Alves VCS, Lira RA, Lima JMS, Barbosa RN, Bento DM, Barbier E, Bernard E, Souza-Motta CM, Bezerra JDP (2022) Unravelling the fungal darkness in a tropical cave: richness and the description of one new genus and six new specie. Fungal Syst Evol 10:139–167. https://doi.org/10.3114/fuse.2022.10.06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Condé TO, Leão AF, Dutra YLG, Rosado AWC, Neves SC, Fraga LMS, Kasuya MCM, Pereira OL (2023) Shedding light on the darkness: a new genus and four new species in the family Chaetomiaceae from Brazilian neotropical caves revealed by multi-gene phylogenetic analyses. Mycol Progress 22:49. https://doi.org/10.1007/s11557-023-01899-0

    Article  Google Scholar 

  23. Neves SC, Fraga LMS, Silva AC, Grazziotti PH, Rodrigues FP, Santiago Neves CM (2017) Estudo preliminar sobre as interações geomicrobiológicas em cavidades quartzíticas na Serra do Espinhaço Meridional. Anais do 34º Congresso Brasileiro de Espeleologia. SBE, Ouro Preto, MG, pp 367–373. https://www.cavernas.org.br/wp-content/uploads/2021/07/34cbe_367-373.pdf

  24. Teixeira-Silva CM, Faleiros-Santos T, Roberto GG, Vieira FF, Morais F, Oliveira GPC, Onofre-Oliveira S, Ferreira AS, Matteo DEG (2005) Espeleologia na área cársctica de Monjolos, MG. Anais do 28º Congresso Brasileiro de Espeleologia. SBE, Campinas, SP, pp 146–152. https://www.cavernas.org.br/wp-content/uploads/2021/07/28cbe_146-152.pdf

  25. Cardoso PH, Menini Neto L, Trovó M, Salimena FRG (2021) Checklist and a new species of Lippia (Verbenaceae) from the Diamantina Plateau, Minas Gerais, Brazil. Eur J Teach Educ 733:42–55. https://doi.org/10.5852/ejt.2021.733.1219

    Article  Google Scholar 

  26. Rapini A, Ribeiro PL, Lambert S, Pirani JR (2008) A flora dos campos rupestres da Cadeia do Espinhaço. Megadiversidade 4:10

    Google Scholar 

  27. Leal-Zanchet AM, Marques AD (2018) Coming out in a harsh environment: a new genus and species for a land flatworm (Platyhelminthes: Tricladida) occurring in a ferruginous cave from the Brazilian savana. PeerJ. https://doi.org/10.7717/peerj.6007

    Article  PubMed  PubMed Central  Google Scholar 

  28. Vasconcelos AMC, Souza FCR, Rodet J, Oliveira CV, Salgado AAR (2013) Karst developed in siliciclastic rocks at Serra do Espinhaço Meridional, Minas Gerais (Brazil). 16th International Congress of Speleology. ICS Proceedings, p 326. https://digitalcommons.usf.edu/cgi/viewcontent.cgi?article=1013&context=kip_talks#page=329

  29. Kuzmina LY, Galimzianova NF, Abdullin SR, Ryabova AS (2012) Microbiota of the Kinderlinskaya Cave (South Urals, Russia). Microbiology 81:251–258. https://doi.org/10.7717/peerj.600710.1134/S0026261712010109

    Article  CAS  Google Scholar 

  30. Borda D, Borda C, Tămaş T (2004) Bats, climate, and air microorganisms in a Romanian cave. Mammalia 68:337–343

    Article  Google Scholar 

  31. Tuite J (1969) Plant pathological methods. Fungi and bacteria. Burgess Publishing Company. https://www.cabdirect.org/cabdirect/abstract/19701101886

  32. Castellani A (1939) Viability of some pathogenic fungi in distilled. water Am J Trop Med Hyg 42:225

    Google Scholar 

  33. Dhingra OD, Sinclair JB (1995) Basic plant pathology methods. CRC Press, Boca Raton

    Google Scholar 

  34. Pinho DB, Firmino AL, Ferreira-Junior WG, Pereira OL (2013) An efficient protocol for DNA extraction from Meliolales and the description of Meliola centellae sp. nov. Mycotaxon 122:333–345

    Article  Google Scholar 

  35. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 18(1):315–322

    Google Scholar 

  36. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. 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. https://doi.org/10.1016/j.ympev.2007.03.011

    Article  PubMed  CAS  Google Scholar 

  38. Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092

    Article  PubMed  CAS  Google Scholar 

  39. 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 61:1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  40. Stephen AR, 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(1):84–98. https://doi.org/10.1080/15572536.2006.11832842

    Article  Google Scholar 

  41. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Nylander JAA (2004) MrModeltest 2.2. Computer program and documentation distributed by the author. Evolutionary Biology Centre. Uppsala University, Uppsala

  44. Ronquist F, Teslenko M, Mark PVD, 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 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  45. Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  ADS  PubMed  CAS  Google Scholar 

  46. Nguyen LT, Schmidt HA, Haeseler AV, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  PubMed  CAS  Google Scholar 

  47. Hoang DT, Chernomor O, Haeseler AV, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522

    Article  PubMed  CAS  Google Scholar 

  48. Kalyaanamoorthy S, Minh BQ, Wong TKF, Haeseler AV, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Rambaut A (2018) FigTree v1.4.4. Tree figure drawing tool. Computer program and documentation distributed by the author at http://tree.bio.ed.ac.uk/software/. Accessed 20 Sept 2020

  50. Riddell RW (1950) Permanent stained mycological preparations obtained by slide culture. Mycologia 42:265–270

    Article  Google Scholar 

  51. Belyagoubi L, Belyagoubi-Benhammou N, Jurado V, Dupont J, Lacoste S, Djebbah F, Ounadjela FZ, Benaissa S, Habi S, Abdelouahid DE, Saiz-Jimenez C (2018) Antimicrobial activities of culturable microorganisms (Actinomycetes and Fungi) isolated from Chaabe Cave, Algeria. Int J Speleol 47:189–199

    Article  Google Scholar 

  52. Xu L, Li Y, Biggins JB, Bowman BR, Verdine GL, Gloer JB, Alspaugh JA, Bills GF (2018) Identification of cyclosporin C from Amphichorda felina using a Cryptococcus neoformans differential temperature sensitivity assay. Appl Microbiol Biotechnol 102:2337–2350. https://doi.org/10.1007/s00253-018-8792-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Marques ELS, Correia DC, Oliveira RBF, Silva KB, Dias JCT, Pirovani CP, Rezende RP (2015) Potencial biotecnológico de microrganismos isolados de cavernas de Paripiranga, Bahia. In: Rasteiro MA, Sallun Filho W (orgs) Anais do 33º Congresso Brasileiro de Espeleologia. SBE, Campinas, SP, pp 161–168. https://www.cavernas.org.br/wp-content/uploads/2021/07/33cbe_161-168.pdf

  54. Rodrigues AA, Carrim AJI, Sadoyma G, Vieira JDG (2009) Potencialidades biotecnológicas de Bacillus cereus isolado em uma caverna. Anais do 15º Congresso Brasileiro de Espeleologia. SBE, Montes Claros, MG, pp 215–220. https://www.cavernas.org.br/wp-content/uploads/2021/07/30cbe_215-220.pdf

  55. Chung Y, El-Shazly M, Chuang D, Hwang T, Asai T, Oshima Y, Ashour ML, Wu Y, Chang F (2013) Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, induces the production of Anti-inflammatory cyclodepsipeptides from Beauveria felina. J Nat Prod 76:1260–1266. https://doi.org/10.1021/np400143j

    Article  PubMed  CAS  Google Scholar 

  56. Du F, Li X, Zhang P, Li C, Wang B (2014) Cyclodepsipeptides and other o-containing heterocyclic metabolites from Beauveria felina EN-135, a marine-derived entomopathogenic fungus. Mar Drugs 12:2816–2826. https://doi.org/10.3390/md12052816

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Du F, Zhang P, Li X, Li C, Cui C, Wang B (2014) Cyclohexadepsipeptides of the isaridin class from the marine- derived fungus Beauveria felina. J Nat Prod 77:1164–1169. https://doi.org/10.1021/np4011037

    Article  PubMed  CAS  Google Scholar 

  58. Liang M, Li W, Qi L, Chen G, Cai L, Yin WB (2021) Establishment of a genetic transformation system in guanophilic fungus Amphichorda guana. J Fungi. https://doi.org/10.3390/jof7020138

    Article  Google Scholar 

  59. Liang M, Lyu HN, Ma ZY, Li EW, Cai L, Yin WB (2021) Genomics-driven discovery of a new cyclodepsipeptide from the guanophilic fungus Amphichorda guana. Org Biomol Chem 19:1960–1964. https://doi.org/10.1039/d1ob00100k

    Article  PubMed  CAS  Google Scholar 

  60. Meng L, Liu Y, Li X, Xu G, Ji N, Wang B (2015) Citrifelins A and B, citrinin adducts with a tetracyclic framework from cocultures of marine-derived isolates of Penicillium citrinum and Beauveria felina. J Nat Prod 78:2301–2305. https://doi.org/10.1021/acs.jnatprod.5b00450

    Article  PubMed  CAS  Google Scholar 

  61. Vita-Marques AM, Lira SP, Berlinck RGS, Seleghim MHR, Sponchiado SRP, Tauk-Tornisielo SM, Barata M, Pessoa C, Moraes MO, Cavalcanti BC, Nascimento GGF, Souza AO, Galetti FCS, Silva CL, Silva M, Pimenta EF, Thiemann O, Passarini MRZ, Sette LD (2008) A multi-screening approach for marine-derived fungal metabolites and the isolation of cyclodepsipeptides from Beauveria felina. Quim Nova 31:1099–1103

    Article  Google Scholar 

  62. Yurchenko AN, Smetanina OF, Kalinovsky AI, Pushilin MA, Glazunov VP, Khudyakova YV, Kirichuk NN, Ermakova SP, Dyshlovoy SA, Yurchenko EA, Afiyatullov SSH (2014) Oxirapentyns f−k from the marine-sediment-derived fungus Isaria felina KMM 4639. J Nat Prod 77:1321–1328. https://doi.org/10.1021/np500014m

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are thankful to colleagues of the Laboratório de Micologia e Etiologia de Doenças Fúngicas/UFV for their valuable help during this work. Authors are also thankful to the Universidade Federal de Viçosa (UFV) and Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM) for providing additional resources to this research.

Funding

This work was supported by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG-VALE RDP-00017-18), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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A.F.L. and T.O.C. performed sampling, laboratory work, data analyses and writing. Y.L.G.D performed laboratory work. A.W.C.R. performed sampling. P.H.G. text review. O.L.P., S.C.N. and L.M.S.F. performed sampling and facilitated funding acquisition. M.C.M.K. and O.L.P. supervised and designed the research project. All authors reviewed the manuscript.

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Correspondence to Olinto Liparini Pereira.

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Leão, A.F., Condé, T.O., Dutra, Y.L.G. et al. Amphichorda monjolensis sp. nov., a new fungal species isolated from a Brazilian limestone cave, with an update on acremonium-like species in Bionectriaceae. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01289-y

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