Abstract
Opuntia ficus-indica Mill. (forage cactus) is farmed with relative success in the semi-arid region of the Brazilian northeast for commercial purposes, particularly as forage and food. Endophytic microorganisms are those that can be isolated inside plant tissues and can be a new source to production of enzymes with different potentialities. The objective of this study was to describe the richness of endophytic fungi from O. ficus-indica and to detect the capacity of these species to produce extracellular hydrolytic enzymes. Forty-four endophytic fungi species were isolated. Among them, the most commonly found were Cladosporium cladosporioides (20.43%) and C. sphaerospermum (15.99%). Acremonium terricola, Monodictys castaneae, Penicillium glandicola, Phoma tropica and Tetraploa aristata are being reported for the first time as endophytic fungi for Brazil. The majority of isolated fungi exhibited enzymatic potential. Aspergillus japonicus and P. glandicola presented pectinolytic activity. Xylaria sp. was the most important among the other 14 species with positive cellulase activity. All 24 isolates analysed were xylanase-positive. Protease was best produced by isolate PF103. The results indicate that there is a significant richness of endophytic fungi in O. ficus-indica, and that these isolates indicate promising potential for deployment in biotechnological processes involving production of pectinases, cellulases, xylanases and proteases.
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Araújo WL, Saridakis HO, Barroso PAV, Aguilar-Vildoso CI, Azevedo JL (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236
Araújo WL, Marcon J, Maccheroni W Jr, Elsas JDV, Vuurde JWL, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914
Ates M (1991) Izmir ve civarinda soguk hava depolarinda depolanan elmalarda depolama sirasinda bozukluklardaki kuf florasinin saptanmasi konusunda bir arastirma. MSc thesis, E.Ü. Fen Bilimleri Enstitüsü
Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65
Baayen RP, Bonants PJM, Verkley G, Carroll GC, van der Aa HA, de Weerdt M, van Brouwershaven IR, Schutte GC, Maccheroni W Jr, Glienke de Blanco C, Azevedo JL (2002) Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology 92:464–477
Bills GF (1996) Isolation and analysis of endophytic fungal communities from woody plants. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants: systematics, ecology, and evolution. American Phytopathological Society Press, Saint Paul, pp 31–65
Bischoff KM, Wicklow DT, Jordan DB, de Rezende ST, Liu SQ, Hughes SR, Rich JO (2009) Extracellular hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr Microbiol 58:499–503
Braz SCM, Souza-Motta CM, Lima DMM, Neves RP, Magalhães OMC (2009) Viability, taxonomic confirmation and enzymatic detection of Acremonium species preserved under mineral oil in the URM Culture Collection. Rev Soc Bras Med Trop 42:63–66
Butt MS, Tahir-Nadeem M, Ahmad Z, Sultan MT (2008) Xylanases and their applications in baking industry. Food Technol Biotechnol 46:22–31
Carroll G, Petrini O (1983) Patterns of substrate utilization by some fungal endophytes from coniferous foliage. Mycologia 75:53–63
Cavalcanti MAQ, Oliveira LG, Fernandes MJ, Lima DM (2006) Fungos filamentosos isolados do solo em municípios na região **ngó, Brasil. Acta Bot Bras 20:831–837
Chareprasert S, Piapukiew J, Thienhirun S, Whalley AJS, Sihanonth P (2006) Endophytic fungi of teak leaves Tectona grandis L. and rain tree leaves Samanea saman Merr. World J Microbiol Biotechnol 22:481–486
Chen Juan, Ke-**ng Hu, Hou **ao-Qiang, Guo Shun-**ng (2011) Endophytic fungi assemblages from 10 Dendrobium medicinal plants (Orchidaceae). World J Microbiol Biotechnol 27:1009–1016
Costa CR (2007) Fungos associados às plantas ornamentais tropicais no Distrito Federal. Universidade de Brasília, Dissertação
Costa IPMW, Cavalcanti MAQ, Fernandes MJS, Lima DMM (2006) Hyphomycetes from soil of an area affected by copper mining activities in the state of Bahia, Brazil. Braz J Microbiol 37:290–295
Dai CC, Tian LS, Zhao YT, Chen Y, **e H (2010) Degradation of phenanthrene by the endophytic fungus Ceratobasidum stevensii found in Bischofia polycarpa. Biodegradation 21:244–255
Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi. IHW-Verlag, Eching
Doolotkeldieva TD (2010) Microbiological control of flour-manufacture: dissemination of mycotoxins producing fungi in cereal products. Microbiol Insights 3:1–15
El Bokhary HA (1999) Osmotolerant and osmophilic fungi from house dust, Riyadh, Saudi Arabia. Saudi J Biol Sci 6:147–155
El Kady IA, Zohri AA, Mohamed EM (1997) Phyllosphere and phylloplane fungi of some herbal plants belonging to Labiatae, Solanaceae an Umbelliferae in Egypt. Qatar Univ Sci J 17:247–264
Ellis MB (1971) Dematiaceus Hyphomycetes. Commonwealth Mycological Institute, Kew
Fischer PJ, Sutton BC, Petrini LE, Petrini O (1994) Fungal endophytes from Opuntia stricta: a first report. Nova Hedwigia 59:195–200
Galati EM, Mendello MR, Giuffrida D, Miceli N (2001) Anticulcer activity of Opuntia ficus-indica (L.) Mill. (Cactaceae): ultra structural study. J Ethnopharmacol 76:1–9
Gams W (1971) Cephalosporium—artige Schimmelpilze (Hyphomyceto). G. Fisher, Stuttgart
Glienke-Blanco C, Aguilar-Vildoso CI, Vieira MLCV, Barroso PAV, Azevedo JL (2002) Genetic variability in the endophytic fungus Guignardia citricarpa isolated from citrus plants. Genet Mol Biol 25:251–255
Goulart AJ, Carmona EC, Monti R (2005) Partial purification and properties of cellulase-free alkaline xylanase produced by Rhizopus stolonifer in solid-state fermentation. Braz Arch Biol Technol 48:327–333
Grandi RAP, Silva TV (2006) Fungos anamorfos decompositores do folhedo de Caesalpinia echinata Lam. Rev Bras Bot 29:275–287
Haliki A, Dizbay M (1997) Izmir-Bergama yoresindeki bazi tarimsal alanlardan mezofilik toprak mikrofunguslarinin izolasyonu ve mevsimsel dagilimlari. Turk J Biol 21:329–341
Hata K, Atari R, Sone K (2002) Isolation of endophytic fungi from leaves of Pasania edulis and their within-leaf distributions. Mycoscience 43:369–373
Hurst JL, Pugh GJF, Walton DWH (1983) Fungal succession and substrate utilization on the leaves of three South Georgia phanerogams. Br Antarct Surv Bull 58:89–100
Jordaan A, Taylor JE, Rossenkhan R (2006) Occurrence and possible role of endophytic fungi associated with seed pods of Colophospermum mopane (Fabaceae) in Botswana. S Afr J Bot 72:245–255
Juven BJ, Lindner P, Weisslowicz H (1985) Pectin degradation in plant materials by Leuconostoc mesenteroides. J Appl Bacteriol 58:533–538
Kara O, Bolat I (2007) Influence of soil compaction on microfungal community structure in two soil types in Bartin Province, Turkey. J Basic Microbiol 47:394–399
Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi from Tripterygium wilfordii. Fungal Divers 17:69–90
Lacaz CS, Porto E, Martins JEC, Heins-Vacarri EM, Melo NK (2002) Tratado de Micologia Médica. Sarvier Press, São Paulo
Larran S, Perelló A, Simón MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in weat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686
Latch GCM (1993) Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agric Ecosyst Environ 44:143–156
Leal IR, Silva JMC, Tabarelli M, Lacher TE Jr (2005) Mudando o curso da conservação da biodiversidade na Caatinga do Nordeste do Brasil. Megadiversidade 1:139–146
Lee JC, Kim HR, Kim J, Jam YM (2002) Antioxidant property of an ethanol extract of the stem of Opuntia ficus-indica var. saboten. J Agric Food Chem 50:6490–6496
Lee S, Mel’nik V, Taylor JE, Crous PW (2004) Diversity of saprobic hyphomycetes on Proteaceae and Restionaceae from South Africa. Fungal Divers 17:91–114
Liberto R, Saparrat MCN (2005) Crecimiento y habilidad decolorante potencial de Hyphomycetes (Deuteromycetes) de Río Santiago sobre medio agarizado suplementado con cromóforos sintéticos. Bol Soc Argent Bot 40:145–150
Mariano RLR, Lira RVI, Silveira EB, Menezes M (1997) Levantamento de fungos endofíticos e epifíticos em folhas de coqueiro no Nordeste do Brasil. I. Frequência da população fúngica e efeito da hospedeira. Agrotópica 9:127–134
Neirotti E, Azevedo JL (1988) Técnicas semiquantitativa de avaliação da produção de celulases em Humicola sp. Rev Microbiol 19:78–81
Nováková A (2009) Microscopic fungi isolated from the Domica Cave system (Slovak Karst National Park, Slovakia). A review. Int J Speleol 38:71–82
Okten S (2008) Airborne fungi and bacteria in indoor and outdoor environment of pediatry unit of Edirne Government Hospital. University Graduate School of Natural and Applied Sciences, Thesis
Oses R, Valenzuela S, Freer J, Baeza J, Rodriguez J (2006) Evaluation of fungal endophytes for lignocellulolytic enzyme production and wood biodegradation. Int Biodeterior Biodegrad 57:129–135
Osono T, Takeda H (2001) Effects of organic chemical quality and mineral nitrogen addition on lignin and holocellulose decomposition of beech leaf litter by Xylaria sp. Eur J Soil Biol 37:17–23
Osono T, Takeda H (2002) Comparison of litter decomposing ability among diverse fungi in a cool temperate deciduous forest in Japan. Mycologia 94:421–427
Osterhage C, König GM, Jones PG, Wright AD (2002) 5-Hydroxyramulosin, a new natural product produced by Phoma tropica, a marine-derived fungus from the alga Fucus spiralis. Planta Med 68:1052–1054
Park E, Kahng J, Lee S, Shin K (2000) An anti-inflamatory principle from cactus. Fitoterapia 72:288–290
Paterson R, Russell M (2004) The isoepoxydon dehydrogenase gene of patulin biosynthesis in cultures and secondary metabolites as candidate PCR inhibitors. Mycol Res 108:1431–1437
Patil VA, Mehta BP, Deshmukh AJ (2010) Field evaluation of different fungicides against Phoma leaf spot disease of Indian bean. Int J Pharm Bio Sci 1:1–5
Pereira JO, Carneiro-Vieira ML, Azevedo JL (1999) Endophytic fungi from Musa acuminata and their reintroduction into axenic plants. World J Microbiol Biotechnol 15:37–40
Pérez E, Santos R, Montiel A, Isea F, Marín M, Sandoval L (2003) Método para el muestreo de esporas de hongos en una plantación de guayabo (Psidium guajava L.). Rev Fac Agron (LUZ) 20:52–62
Petrini O, Stone J, Carroll FE (1992) Endophytic fungi in evergreen shrubs in western Oregon: a preliminary study. Can J Bot 60:789–796
Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic fungi of wild banana (Musa acuminata) at Doi Suthep Pui National Park, Thailand. Mycol Res 105:1508–1513
Rakotoniriana EF, Munaut F, Decock C, Randriamampionona D, Iriambololoniaiana M, Rakotomalala T, Rakotonirina EJ, Rabemanantsoa C, Cheuk K, Ratsimamanga SU, Mahillon J, El-Jaziri M, Quetin-Leclercq J, Corbisier AM (2008) Endophytic fungi from leaves of Centella asiatica: occurrence and potential interactions within leaves. Anton Leeuw Int J G 93:26–36
Ruegger MJS, Tauk-Tornisielo SM (2004) Atividade da celulase de fungos isolados do solo da Estação Ecológica de Juréia-Itatins, São Paulo, Brasil. Rev Bras Bot 27:205–211
Saha BC (2002) Production, purification and properties of xylanase from a newly isolated Fusarium proleferatum. Process Biochem 37:1279–1284
Sakellaris G, Nokolaropoulos S, Evangelopoulos AE (1989) Purification and characterisation of an extracellular polygalacturonase from Lactobacillus plantarum train BA 11. J Appl Bacteriol 67:77–85
Samson RA, Frisvad JC (2004) Penicillium subgenus Penicillium: new taxonomics schemes, mycotoxins and other extrolites. Stud Micol 49:1–260
Santamaría J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb Ecol 0:1–8
Santos SFM (2007) Estudo da produção de pectinase por fermentação em estado sólido utilizando pedúnculo de caju como substrato. Tese, Universidade Federal do Rio Grande do Norte
Sarath G, de La Motte RS, Wagner FW (1989) Protease Assay Methods. In: Beynon RJ, Bonde JS (eds) Proteolytics enzymes: an pratical approach. Oxford University Press, Oxford, pp 25–54
Scheinvar L (1995) Taxonomy of utilized Opuntia. In: Barbera G, Inglese P, Pimienta-Barrios E (eds) Agro-ecology, cultivation and uses of cactus pear. Food and Agriculture Organization, Roma, pp 20–27
Schoenlein NC, Corso CR, Schoenlein-Crusius IH, de Souza JI, Oliveira LHS (2008) Fungos anamorfos do solo da região dos lagos no Município de Santa Gertrudes, SP, Brasil. Rev Bras Bot 31:667–678
Schoenlein-Crusius IH, Milanez AI (1998) Fungos microscópicos da Mata Atlântica de Paranapiacaba, São Paulo, Brasil1. Rev Bras Bot 21:73–79
Serda SK, Yucel A (2002) Phospholipase and protease activities in clinical Candida isolates with reference to the sources of strains. Mycoses 45:160–165
Silva JMC, Tabarelli M, Fonseca MT, Lins LV (orgs.) (2004) Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Ministério do Meio Ambiente, Brasília
Silva RLO, Luz JS, Silveira EB, Cavalcante UMT (2006) Fungos endofíticos em Annona spp.: isolamento, caracterização enzimática e promoção do crescimento em mudas de pinha (Annona squamosa L.). Acta Bot Bras 20:649–655
Sinclair RCD (1990) A taxonomic study of some saprophytic hyphomycetes of southern Africa. University of Pretoria, Thesis
Siqueira MV, Braun U, Souza-Motta CM (2008) Corynespora subcylindrica sp. nov., a new hyphomycete species from Brazil and a discussion on the taxonomy of corynespora-like genera. Sydowia 60:113–122
Stone JK, Polishook JD, White F Jr (2004) Endophytic Fungi. In: Muller JM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic Press, San Diego, pp 241–270
Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639
Suto M, Takebayashi M, Sait K, Tanaka M, Yokota A, Tomita F (2002) Endophytes as produces of xylanase. J Biosci Bioeng 93:88–90
Sutton BC (1980) The Coelomycetes: fungi imperfecti with pycnidia, acervuli and stromata. Commonwealth Mycological Institute, Kew
Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459
Tanaka K, Hirayama K, Yonezawa H, Hatakeyama S, Harada Y, Sano T, Shirouzu T, Hosoya T (2009) Molecular taxonomy of bambusicolous fungi: Tetraplosphaeriaceae, a new pleosporalean family with Tetraploa-like anamorphs. Stud Mycol 64:175–209
Teixeira JC, Evangelista AR, Perez JRO, Trindade IACM, Moron IR (1999) Cinética da digestão ruminal da palma forrageira (Nopalea cochenillifera (L.) Lyons (Cactaceae) em bovinos e caprinos. Ciência e Agrotecnologia 23:179–186
Teixeira MFS, Filho JLL, Durán N (2000) Carbon sources effect on pectinase production from Aspergillus japonicus 586. Braz J Microbiol 31:286–290
Topal S (1998) Turkiye’nin dominant mikoflorasiyla kultur kolleksiyon merkezi olusturulmasi. J Kukem 21:69–88
Uenojo M, Pastore GM (2006) Isolamento e seleção de microrganismos pectinolíticos a partir de resíduos provenientes de agroindústrias para produção de aromas frutais. Ciência Tecnologia Alimentar 26:509–515
Vishwanatha KS, Rao A, Singh SA (2009) Characterization of acid protease expressed from Aspergillus oryzae MTCC 5341. Food Chem 114:402–407
Wang Y, Dai C-C (2011) Endophytes: a potencial resource for biosynthesis, biotranformation, and biodegradation. Review article. Ann Microbiol 61:207–215
Wang FW, Jiao RH, Cheng AB, Tan SH, Song YC (2007) Antimicrobial potentials of endophytic fungi residing in Quercus variabilis and brefeldin a obtained from Cladosporium sp. World J Microbiol Biotechnol 23:79–83
Wei DL, Kirimur K, Usami S, Lin TH (1996) Purification and characterization of an extracellular β-glucosidase from the wood-grown fungus Xylaria regalis. Curr Microbiol 33:297–301
**ng X, Guo S, Fu J (2010) Biodiversity and distribution of endophytic fungi associated with Panax quinquefolium L. cultivated in a forest reserve. Symbiosis 51:161–166
Yoon JH, Hong SB, Ko SJ, Kim SH (2007) Detection of extracellular enzyme activity in Penicillium using chromogenic media. Mycobiology 35:166–169
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We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for Brazil, and Federal University of Pernambuco (UFPE) for funding this Project.
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Bezerra, J.D.P., Santos, M.G.S., Svedese, V.M. et al. Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28, 1989–1995 (2012). https://doi.org/10.1007/s11274-011-1001-2
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DOI: https://doi.org/10.1007/s11274-011-1001-2