Six new species of Cladosporium associated with decayed leaves of native bamboo (Bambusoideae) in a fragment of Brazilian Atlantic Forest

PRICILA P. COSTA; ANDRÉ W. C. ROSADO; OLINTO L. PEREIRA

doi:10.11646/phytotaxa.560.1.1

Issue: Vol. 560 No. 1: 29 August 2022

Type: Article

Published: 2022-08-29

DOI: 10.11646/phytotaxa.560.1.1

Page range: 1-29

Abstract views: 231

PDF downloaded: 9

**Six new species of Cladosporium associated with decayed leaves of native bamboo (Bambusoideae) in a fragment of Brazilian Atlantic Forest**

PRICILA P. COSTA⁺⁻
ANDRÉ W. C. ROSADO⁺⁻
OLINTO L. PEREIRA⁺⁻

Departamento de Microbiologia, Universidade Federal de Viçosa, Minas Gerais, Viçosa 36570–900, Brazil

Departamento de Fitopatologia, Universidade Federal de Viçosa, Minas Gerais, Viçosa 36570–900, Brazil

Departamento de Microbiologia, Universidade Federal de Viçosa, Minas Gerais, Viçosa 36570–900, Brazil; Departamento de Fitopatologia, Universidade Federal de Viçosa, Minas Gerais, Viçosa 36570–900, Brazil

Cladosporiaceae decayed leaf Dothideomycetes fungal diversity fungal taxonomy phylogeny Fungi

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Abstract

The Atlantic Forest has the greatest diversity of plants per hectare, and it is considered the main center of bamboo biodiversity in the world. Studies on bambusicolous fungi are scarce and concentrated in temperate regions. Cladosporium is one of the largest genera of dematiaceous hyphomycetes fungus and their adaptation to different environments allows them to have a broad lifestyle. Currently, this genus has been taxonomically and phylogenetically elucidating with the help of extensive polyphasic analyzes. This study aimed to characterize 17 Cladosporium isolates associated with decayed leaves of three bamboo species at a fragment of the Brazilian Atlantic Forest, namely “Parque Estadual da Serra do Brigadeiro”, Minas Gerais state, Brazil. Phylogenetic studies revealed that all isolates belong to the C. cladosporioides species complex. Six new Cladosporium species were found and named herein as C. aulonemiae, C. bambusicola, C. benschii, C. brigadeirensis, C. chusqueae and C. pseudotenuissimum. This study contributes with several taxonomic novelties for knowledge about the diversity of the C. cladosporioides species complex.

References

Almeida, J.G. (2017) Bambu como insumo industrial do Brasil: reflexão sobre o papel da pesquisa na produção do bamboo laminado colado (BaLC). In: Bambu no Brasil: da Biologia a tecnologia. 1ª ed. Rio de Janeiro, pp. 439–455. 
Bensch, K., Braun, U., Groenewald, J.Z. & Crous, P.W. (2012) The genus Cladosporium. Studies in Mycology 72: 1–401. https://doi.org/10.3114/sim0003
Bensch, K., Groenewald, J.Z., Braun, U., Dijksterhuis, J., de Jesús Yáñez-Morales, M. & Crous, P.W. (2015) Common but different: The expanding realm of Cladosporium. Studies in Mycology 82: 23–74. https://doi.org/10.1016/j.simyco.2015.10.001
Bensch, K., Groenewald, J.Z., Dijksterhuis, J., Starink-Willemse, M., Andersen, B., Summerell, B.A., Shin, H-D., Dungan, F.M., Schroesrs, H-J, Braun, U. & Crous, P.W. (2010) Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Studies in Mycology 67: 1–94. https://doi.org/10.3114/sim.2010.67.01 
Braun, U. & Schubert, K. (2007) Taxonomic revision of the genus Cladosporium s. lat. 7. Descriptions of new species, a new combination and further new data. Schlechtendalia 16: 61–76.
Braun, U., Crous, P.W. & Schubert, K. (2008) Taxonomic revision of the genus Cladosporium s. lat. 8. Reintroduction of Graphiopsis (= Dichocladosporium) with further reassessments of cladosporioid hyphomycetes. Mycotaxon 103: 207–216.
Braun, U., Crous, P.W., Dugan, F.M., Groenewald, J.Z. & Hoog, G.S. de (2003) Phylogeny and taxonomy of Cladosporium-like hyphomycetes, including Davidiella gen. nov., the teleomorph of Cladosporium s. str. Mycological Progress 2: 3–18. https://doi.org/10.1007/s11557-006-0039-2
Braun, U., Hill, C.F. & Schubert, K. (2006) New species and new records of biotrophic micromycetes from Australia, Fiji, New Zealand and Thailand. Fungal Diversity 22: 13–35.
Brazil (2011) Lei 12.484 de 8 de setembro de 2011 – Política Nacional de Incentivo ao Manejo Sustentado e ao Cultivo do Bambu. Diário Oficial República Federativa do Brasil, Brasília, DF. Available from: http://www.planalto.gov.br/ccivil_03/_ato2011-2014/2011/lei/l12484.htm (Accessed April 2021)
Carbone, I. & Kohn, L.M. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556. https://doi.org/10.2307/3761358 
Castañeda-Ruiz, R.F., Gusmão, L.F.P., Heredia-Abarca, G. & Saikawa, M. (2006) Some Hyphomycetes from Brazil. Two new species of Brachydesmiella, two new combinations for Repetophragma, and new records. Mycotaxon 95: 261–270.
Castellani, A. (1939) Viability of some pathogenic fungi in distilled water. Journal of Tropical Medicine and Hygiene 42: 225–226.
Conti, J.B. & Furlan, S.A. (2003) Geoecologia: o clima, os solos e a biota. In: Ross, J.L.S. Geografia do Brasil. 4ª ed. EDUSP, São Paulo, pp. 67–207.
Crous, P.W., Braun, U., Schubert, K. & Groenewald, J.Z. (2007) Delimiting Cladosporium from morphologically similar genera. Studies in Mycology 58: 33–56. https://doi.org/10.3114/sim.2007.58.02
Crous, P.W., Schroers, H-J., Groenewald, J.Z., Braun, U. & Schubert, K. (2006) Metulocladosporiella gen. nov. for the causal organism of Cladosporium speckle disease of banana. Mycological Research 110: 264–275. https://doi.org/10.1016/j.mycres.2005.10.003
Crous, P.W., Shivas, R.G., Quaedvlieg, W., van der Bank, M., Zhang, Y., et al. (2014) Fungal Planet description sheets 214–280. Persoonia 32: 184–306. https://doi.org/10.3767/003158514X682395
Dai, D.Q., Phookamsaki, R., Wijayawardene, N.N., Li, W.J., Bhat, D.J., Xu, J.C., Taylor, J.E., Hyde, K.D. & Chukeatirote, E. (2017) Bambusicolous fungi. Fungal Diversity 82: 1–105. https://doi.org/10.1007/s13225-016-0367-8 
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109 
Dhingra, O.D. & Sinclair, J.B. (1995) Slide culture techniques and preparation of permanent mounts. In: Basic Plant Pathology Methods. 2nd ed. CRC Press, Boca Raton, Florida, pp. 319–320. 
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. https://doi.org/10.1093/nar/gkh340 
Filgueiras, T.S. & Gonçalves, A.P.S. (2004) A checklist of the basal grasses and bamboos in Brazil (Poaceae). In: Bamboo Science and Culture: The Journal of the American Bamboo Society 18 (1): 7–18. 
Freitas, M.L.R., Gomes, A.A.M., Rosado, A.W.C. & Pereira, O.L. (2021) Cladosporium species from submerged decayed leaves in Brazil, including a new species and new records. Phytotaxa 482 3: 223–239. https://doi.org/10.11646/phytotaxa.482.3.1 
Gonçalves, R.C., Alfenas, A.C. & Mafia, R.G. (2016) Armazenamento de microrganismos em cultura com ênfase em fungos fitopatogênicos. In: Alfenas, A.C & Mafia, R.G. (Eds.) Métodos em Fitopatologia. 2nd ed. Editora UFV, Viçosa, pp. 93–105.
Grombone-Guaratini, M.T., Nascimento, A.A. & Santos-Gonçalves, A.P. (2011) Flowering and fruiting of Aulonemia aristulata: a gynomonoecious woody bamboo species from Atlantic Forest in Brazil. Brazilian Journal of Botany 34 (1): 135–140. https://doi.org/10.1590/S0100-84042011000100012 
Hall, T. (2015) Biological sequence alignment editor for Win95/98/NT/2K/XP/7 (BioEdit), version 7.0.9. Available from: http://www.mbio.ncsu.edu/bioedit/bioedit (accessed 13 February 2017).
Harley, J.L. & Waid, J.S. (1955) A method of studying active mycelia on living roots and other surfaces in the soil. Transactions of the British Mycological Society 38: 104–118. https://doi.org/10.1016/S0007-1536(55)80022-8 
Hyde, K.D., Zhou, D. & Dalisay, T. (2002) Bambusicolous fungi: A review. Fungal Diversity 9: 1–14.
Judziewicz, E.J., Clark, L.G., Londoño, X. & Stern, M.J. (1999) American bamboos. Smithsonian Institution Press, Washington, DC. 392 pp.
Kelchner, S.A. Clark, L., Cortés, G., Oliveira, R.P., Dransfield, S., Filgueiras, T., Fisher, A.E., Guala, G.F., Hodkinson, T., Judziewicz, E., Kumar, M., Li, D.Z., Londoño, X., Mejia, M.T., Santos-Gonçalves, A.P., Stapleton, C., Sungkaew, S., Triplett, J., Widjaja, E. Wong, K.M. & Xia, N.H. (2013) Higher level phylogenetic relationships within the bamboos (Poaceae: Bambusoideae) based on five plastid markers. Molecular Phylogenetics and Evolution 67: 404–413. https://doi.org/10.1016/j.ympev.2013.02.005 
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33 (7): 1870–1874. https://doi.org/10.1093/molbev/msw054 
Link, H.F. (1809) Observationes in ordines plantarum naturales. Dissertatio I, complectens Anandrarum ordines Epiphytas, Mucedines, Gastromycos et Fungos. Der Gesellschaft naturforschender Freunde zu Berlin Magazin für die neuesten Entdeckungen in der gesammten Naturkunde 3: 3–42.
Link, H.F. (1816) Observationes in ordines plantarum naturales. Dissertatio II, sistens nuperas de Mucedinum et Gastromycorum ordinibus observationes. Der Gesellschaft naturforschender Freunde zu Berlin Magazin für die neuesten Entdeckungen in der gesammten Naturkunde 7: 25–45.
Ma, R., Chen, Q., Fan, Y., Wang, Q., Chen, S., Liu, X., Cai, L. & Yao, B. (2017) Six new soil-inhabiting Cladosporium species from plateaus in China. Mycologia 109: 244–260. https://doi.org/10.1080/00275514.2017.1302254
 Marin-Felix, Y., Groenewald, J.Z., Cai, L., Chen, Q., Marincowitz, S., Barnes, I., Bensch, K., Braun, U., Camporesi, E., Damm, U., de Beer, Z.W., Dissanayake, A., Edwards, J., Giraldo, A., Hernández-Restrepo, M., Hyde, K.D., Jayawardena, R.S., Lombard, L., Luangsa-ard, J., McTaggart, A.R., Rossman, A.Y., Sandoval-Denis, M., Shen, M., Shivas, R.G., Tan, Y.P., van der Linde, E.J., Wingfield, M.J., Wood, A.R., Zhang, J.Q., Zhang, Y. & Crous, P.W. (2017) Genera of phytopathogenic fungi: GOPHY 1. Studies in Mycology 86: 99–216. https://doi.org/10.1016/j.simyco.2017.04.002
Miller, M.A., Schwartz, T., Pickett, B.E., He, S., Klem, E.B., Scheuermann, R.H., Passarotti, M., Kaufman, S. & O’Leary, M.A. (2015) A RESTful API for Access to Phylogenetic Tools via the CIPRES Science Gateway. Evolutionary Bioinformatics 11: 43–48. https://doi.org/10.4137/EBO.S21501 
Mota, M.A, Campos, A.K. & Araújo, J.V. (2003) Sporulation, radial growth and biomass production of A. robusta and M. thaumasium submitted to different methods of preservation. Brazilian Journal of Microbiology 34: 157–160. https://dx.doi.org/10.1590/S1517-83822003000200013 
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853–858. https://doi.org/10.1038/35002501 
O’Donnell, K., Kistler, H.C., Cigelnik, E. & Ploetz, R.C. (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Sciences of the United States of America 95: 2044–2049. https://doi.org/10.1073/pnas.95.5.2044
Pereira, M.L.S., Carvalho, J.L.V.R., Lima, J.M.S., Barbier, E., Bernard, E., Bezerra, J.D.P. & Souza-Motta, C.M. (2022) Richness of Cladosporium in a tropical bat cave with the description of two new species. Mycological Papers. https://doi.org/10.1007/s11557-021-01760-2
Persoon, C.H. (1794) Neuer Versuch einer systematischen Eintheilung der Schwämme. Neues Magazin für die Botanik in ihrem ganzen Umfange 1: 63–128.
Pinho, D.B., Firmino, A.L., Ferreira-Junior, W.G. & Pereira, O.L. (2012) An efficient protocol for DNA extraction from Meliolales and the description of Meliola centellae sp. nov. Mycotaxon 122: 333–345. https://doi.org/10.5248/122.333 
Rambaut, A. (2018) FigTree: Tree figure drawing tool version 1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 28 December 2021)
Rannala, B. & Yang, Z. (1996) Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. Journal of Molecular Evolution 43: 304–311. https://doi.org/10.1007/BF02338839 
Rayner, R.W. (1970) A mycological colour chart. CMI and British Mycological Society. Kew, Surrey, England, 34pp.
Razafinarivo, J., Jany, J.L., Crous, P.W., Looten, R., Gaydou, V., Barbier, G., Mounier, J. & Vasseur, V. (2016) Cladosporium lebrasiae, a new fungal species isolated from milk bread rolls in France. Fungal Biology 120: 1017–1029. https://doi.org/10.1016/j.funbio.2016.04.006
Riddell, R.W. (1950) Permanent stained mycological preparations obtained by slide culture. Mycologia 42: 265–270. https://doi.org/10.1080/00275514.1950.12017830   
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Rosado, A.W.C., Custódio, F.A., Pinho, D.B., Ferreira, A.P.S. & Pereira, O.L. (2019) Cladosporium species associated with disease symptoms on Passiflora edulis and other crops in Brazil, with descriptions of two new species. Phytotaxa 409 (5): 239–260. https://doi.org/10.11646/phytotaxa.409.5.1 
Sandoval-Denis, M., Gené, J., Sutton, D.A., Wiederhold, Cano-Lira, J.F. & Guarro, J. (2016) New species of Cladosporium associated with human and animal infections. Persoonia 36: 281–298. https://doi.org/10.3767/003158516X691951 
Sanquetta, C.R., Mognon, F., Corte, A.P.D., de Novaes, A.B. & Blum, C.T. (2017) Em busca de características promissoras: avaliação experimental de seis espécies de bambu em Pinhais (PR). In: Bambu no Brasil: da Biologia a tecnologia. Instituto de Ciência Hoje. Rio de Janeiro, pp. 270–280.
Schubert, K., Groenewald, J.Z., Braun, U., Dijksterhuis, J., Starink, M., Hill, C.F., Zalar, P., de Hoog, G.S. & Crous, P.W. (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology 58: 105–156. https://doi.org/10.3114/sim.2007.58.05 
Seifert, K.A., Hughes, S.J., Boulay, H. & Louis-Seize, G. (2007) Taxonomy, nomenclature and phylogeny of three cladosporium-like hyphomycetes, Sorocybe resinae, Seifertia azalea and the Hormoconis anamorph of Amorphotheca resinae. Studies in Mycology 58: 235–245. https://doi.org/10.3114/sim.2007.58.09
Seifert, K.A., Nickerson, N.L., Corlett, M., Jackson, E.D., Louis-Seize, G. & Davies, R.J. (2004) Devriesia, a new hyphomycete genus to accommodate heat-resistant, cladosporium-like fungi. Canadian Journal of Botany 82: 914–926. https://doi.org/10.1139/b04-070
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/JB.172.8.4238-4246.1990 
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR Protocols: a guide to methods and applications. Academic Press, New York, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1 
Wirsel, S.G.R., Runge-Froböse, C., Ahrén, D.G., Kemen, E., Oliver, R.P. & Mendgen, K.W. (2002) Four or more species of Cladosporium sympatrically colonize Phragmites australis. Fungal Genetics and Biology 35: 99–113. https://dx.doi.org/10.1006/fgbi.2001.1314
Zalar, P.D., De Hoog, G., Schroers, H.J., Crous, P.W, Groenewald, J.Z. & Gunde-Cimerman, N. (2007) Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Studies in Mycology 58: 157–183. https://doi.org/10.3114/sim.2007.58.06