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La planta medicinal amazónica sucuba (Himatanthus sucuuba) es muy utilizada en etnofarmacología y tiene potencial farmacológico. Sus hongos endofíticos también poseen importantes sustancias bioactivas de interés para la industriafarmacéutica. No existen estudios relacionados con sus microorganismos endofíticos, por lo que en este trabajo se planteó el objetivo de describir los hongos endofíticos de H. sucuuba y evaluar el potencial antibacteriano de sus metabolitos secundarios frente a Staphylococcus aureus, Streptococcus pneumoniae, Escherichia coli y Klebsiella pneumoniae. Para ello se aisló meterial de hojas y tallos utilizando los medios de cultivo agar de papa y dextrosa (PDA) y agar de dextrosa Sabouraud (SDA), con o sin 10 % de extracto vegetal, que luego se incubó a 18 °C o 28 °C. Los hongos aislados se analizaron en busca de características macromorfológicas y se clasificaron en morfoespecies para la caracterización micromorfológica y la producción de extractos de hongos. Los hongos se agruparon en 259 morfoespecies, 135 (52,12 %) se identificaron a nivel de género y se describieron 16 diferentes. Los hongos endofíticos se aislaron con mayor frecuencia de la hoja de H. sucuuba (341) en medio de cultivo SDA a 28 °C. H. sucuuba mostró una gran diversidad, con índice de Shannon de 5,26, índice de diversidad de Simpson (D) de 0,99 e índice de uniformidad de 0,83. De los 235 extractos de hongos probados, 28 (12 %) inhibieron el crecimiento de bacterias Gram-positivas y Gram-negativas. S. pneumoniae y E. coli fueron las bacterias más sensibles y las de K. pneumoniae las más resistentes. Este es el primer informe sobre hongos endofíticos de H. sucuuba que evidencia su potencial para la producción de sustancias antibacterianas.
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Abdalla, M. A., Mcgaw, L. J. (2018). Bioprospecting of South African plants as a unique resource for bioactive endophytic microbes. Frontiers in Pharmacology. 9: 456. https://doi.org/10.3389/fphar.2018.00456.
Aboobaker, Z., Viljoen, A., Chen, W., Crous, P. W., Maharaj, V.J., Van Vuuren, S. (2019). Endophytic fungi isolated from Pelargonium sidoides DC: Antimicrobial interaction and isolation of a bioactive compound. South African Journal of Botany. 122: 535-542. https://doi.org/10.1016/j.sajb.2019.01.011
Azevedo, J. L., Maccheroni, Jr. W., Pereira, J. O., De Araújo, W. L. (2000). Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electronic Journal of Biotechnology. 3: 15-16. https://doi.org/10.4067/S0717-34582000000100004
Barnett, H.L., Hunter, B. B. (1999). Illustrated genera of imperfect fungi. St Paul, Brazil: APS. 218 p.
Batista, B.N., Raposo, N.V.D.M., Silva, I.R.D. (2018). Isolamento e avaliação da atividade antimicrobiana de fungos endofíticos de açaizeiro. Revista Fitos. 12: 161-174. https://doi.org/10.5935/2446-4775.20180015.
Bezerra, J.D.P., Santos, M.G.S., Svedese, V.M., Lima, D.M.M., Fernandes, M.J.S., Paiva, L.M., Souza-Motta, C.M. (2012). Richness of endophytic fungi isolated from Opuntia ficusindica Mill. (Cactaceae) and preliminary screening for enzyme production. World Journal of Microbiology and Biotechnology. 28: 1989-1995. https://doi.org/10.1007/s11274-011-1001-2
Bibi, S.N., Gokhan, Z., Rajesh, J., Mahomoodally, M.F. (2020). Fungal endophytes associated with mangroves–Chemistry and biopharmaceutical potential. South African Journal of Botany. 134: 1-26. https://doi.org/10.1016/j.sajb.2019.12.016
Calero-Armijos, L.L., Herrera-Calderon, O., Arroyo-Acevedo, J.L., Rojas-Armas, J.P., HañariQuispe, R.D., Figueroa-Salvador, L. (2020). Histopathological evaluation of latex of Bellaco-Caspi, Himatanthus sucuuba (Spruce) Woodson on wound healing effect in BALB/C mice. Veterinary World. 13: 1045. https://doi.org/10.14202/vetworld.2020.1045-1049
Chen, R., Tang, J.W., Li, X.R., Liu, M., Ding, W.P., Zhou, Y.F., Wang, W.G., Du, X., Sun, H.D., Puno, P.T. (2018). Secondary metabolites from the endophytic fungus Xylaria sp. hg1009. Natural Products and Bioprospecting. 8 (2): 121-129. https://doi.org/10.1007/s13659-018-0158-x
Cintrón, G., Lugo, A.E., Pool, D.J., Morris, G. (1978). Manguezais de ambientes áridos em Porto Rico e ilhas adjacentes. Biotropica. 10 (2): 110-121. http://www.jstor.org/pss/2388013
Corrado, M. & Rodrigues, K.F. (2004). Antimicrobial evaluation of fungal extracts produced by endophytic strains of Phomopsis sp. Journal of Basic Microbiology. 44: 157-160. https://doi.org/10.1002/jobm.200310341.
Da Silva, M.B., Da Silva, M.P., Dos Reis Júnior, J.D.D., Lima, C.A.C., de Oliveira Souza, A.(2021). Therapeutics activities of Amazonian plant Himatanthus sucuuba (Spruce ex Müll. Arg.) Woodson (Apocynaceae): A Review. Journal of Advances in Biology & Biotechnology. 24 (2): 1-14 Https://doi.org/10.9734/jabb/2021/v24i230197
Ding, X., Liu K., Deng, B., Chen, W., Li W., Liu, F. (2013). Isolation and characterization of endophytic fungi from Camptotheca acuminata. World Journal of Microbiology and Biotechnology. 29: 1831-1838. https://doi.org/10.1007/s11274-013-1345-x
Dini-Andreote, F. (2020). Endophytes: The Second Layer of Plant Defense. Trends in Plant Science.
: 319-322. https://doi.org/10.1016/j.tplants.2020.01.007
Diniz, F.V., Doi, M.S.R.S., Fittipaldy, M.C.P.M., Lopes, R.F., Margarido, S.S.O.R., Pontes, S.M.A., Ramos, D.P., Araújo, A.V., Carvalho, C.M. (2021a). Isolation and identification of endophytic fungi from the amazonian palm Oenocarpus bataua Mart. South American Journal of Basic Education, Technical and Technological. 8 (1): 139-153.
Diniz, F.V., de Araújo, A.V., da Silva Faria, M. A., Elisabete, M., Morselli, P., Ramos, L.J., Carvalho, C.M. (2021b). Cultivable endophytic fungi associated with the murumuru Amazon palm (Astrocaryum ulei Burret). Scientia Vitae. 12 (34): 23-32.
Diniz, F.V., Lima, Y.D.M.M., Paz, F.S., Silva, A.L.D., Gomes, L.C., Santos, G.S., Carvalho, C.M. (2020). Atividade enzimática de fungos endofíticos de bacaba (Oenocarpus bacabaMart.). Biota Amazônia (Biote Amazonie, Biota Amazonia, Amazonian Biota). 10 (3): 7-11 b. https://doi.org/10.18561/2179-5746/biotaamazonia.v10n3p7-11
Duhan, P., Bansal, P., Rani, S. (2020). Isolation, identification and characterization of endophytic bacteria from medicinal plant Tinospora cordifolia. South African Journal of Botany. 134: 43-49. https://doi.org/10.1016/j.sajb.2020.01.047
Egamberdieva, D., Wirth, S., Behrendt, U., Ahmad, P., Berg G. (2017). Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Frontiers in Microbiology. 8: 199. https://doi.org/10.3389/fmicb.2017.00199
Fakhrudin, N., Waltenberger, B., Cabaravdic, M., Atanasov, A. G., Malainer, C., Schachner, D., Heiss, E.H., Liu, R, Noha, SM, Grzywacz, A.M., Mihaly-Bison, J, Awad, E.M., Schuster, D., Breuss, J.M., Rollinger, J.M., Bochkov, V., Stuppner, H., Dirsch, V.M. (2014). Identification of plumericin as a potent new inhibitor of the NF‐κB pathway with anti‐inflammatory activity in vitro and in vivo. British Journal of Pharmacology. 171: 1676-1686. https://doi.org/10.1111/bph.12558
Farhat, H., Urooj, F., Tariq, A., Sultana, V., Ansari, M., Ahmad, V.U., Ehteshamul-Haque, S. (2019). Evaluation of antimicrobial potential of endophytic fungi associated with healthy plants and characterization of compounds produced by endophytic Cephalosporium and Fusarium solani. Biocatalysis and Agricultural Biotechnology. 18: 101043. https://doi.org/10.1016/j.bcab.2019.101043
Fisch, G., Marengo, J.A., Nobre, C.A. (1998). Uma revisão geral sobre o clima da Amazônia. Acta Amazônica. 28: 101-101. https://doi.org/10.1590/1809-43921998282126
Freire, M., Carvalho, S., Coutinho, H., Imbeloni, T., Silva, V., Mussi-Dias, V. (2015). Bioprospecção da flora fúngica endofítica de Restinga para uso no controle biológico de pragas. Ciências Biológicas e da Saúde. 5: 35. https://doi.org/10.25242/88685182015767
Gos, F.M., Savi, D.C., Shaaban, K.A., Thorson, J.S., Aluizio, R., Possiede, Y.M., Rohr, J., Glienke, C. (2017). Antibacterial activity of endophytic actinomycetes isolated from the medicinal plant Vochysia divergens (Pantanal, Brazil). Frontiers in Microbiology. 8: 1642.https://doi.org/10.3389/fmicb.2017.01642
Hanada, R.E., Pomella, A.W.V., Costa, H.S., Bezerra, J.L., Loguercio, L.L., Pereira, J.O. (2010). Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion andbiocontrol of black-pod disease. Fungal Biology. 114: 901-910. https://doi.org/10.1016/j.funbio.2010.08.006
Hong, Lu., Zou, W.X., Meng, J.C., Hu, J., Tan, R.X. (2000). New Bioactive Metabolites Produced by Colletotrichum sp., an Endophytic Fungus in Artemisia annua. Plant Science. 151: 67-73. https://doi.org/10.1016/S0168-9452 (99)00199-5
Inácio, I.A., Diniz, F.V., Peters, L.P., Carvalho, C.M. (2021). Characterization of cultivable endophytic fungi from the medicinal plant Senna reticulata (Willd.) HS Irwin & Barneby.Revista Cereus. 13 (2): 42-58. https:/doi.org/10.18605/2175-7275/cereus.v13n2p42-
Kang, X., Liu, C., Shen, P., Hu, L., Lin, R., Ling, J., Xiong, X., Xie, B., Liu, D. (2019).Genomic characterization provides new insights into the biosynthesis of the secondary metabolite huperzine a in the endophyte Colletotrichum gloeosporioides Cg01. Frontiers in microbiology. 9: 3237.
Khare, E., Mishra, J., Arora, N.K. (2018). Multifaceted interactions between endophytes and plant: developments and prospects. Frontiers in Microbiology. 9: 2732. https://doi.org/10.3389/fmicb.2018.02732
Kusari, S., Singh, S., Jayabaskaran, C. (2014). Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends in Biotechnology. 32: 297-303. https://doi.org/10.1016/j.tibtech.2014.03.009
Larrosa, C.R., Duarte, M.R. (2005). Contribution to the anatomical study of the stem of Himatanthus sucuuba (Spruce ex Müll. Arg.) Woodson, Apocynaceae. Revista Brasileira de Farmacognosia. 15: 110-114. https:// doi.org/10.1590/S0102-695X2005000200007
Linhares, J.F.P. & Pinheiro, C.U.B. (2011). Sustentabilidade socioambiental da extração de janaúba (Himatanthus Willd. Ex schult.) no Município de Alcântara, Estado do Maranhão, Brasil. Revista Pan-Amazônica de Saúde. 2: 57-58. https:// doi.org/10.5123/S2176-62232011000400009
Lorenzi, H. (1998). Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Nova Odessa, Brasil: Editora Plantarum. 352 p.
López-Jácome, E., Franco-Cendejas, R., Quezada, H., Morales-Espinosa, R., Castillo-Juárez, I., González-Pedrajo, B., Fernández-Presas, A.M., Tovar-García, A., Angarita-Zapata, V., Licona-Limón, P., Martínez-Vázquez, M., García-Contreras, R. (2019). The race between drug introduction and appearance of microbial resistance. Current balance and alternative approaches. Current Opinion in Pharmacology. 48: 48-56.
Ma, X., Nontachaiyapoom, S., Jayawardena, R.S. (2018). Endophytic Colletotrichum species from Dendrobium spp. in China and Northern Thailand. MycoKeys. 43: 23. https://doi.org/10.3897/mycokeys.43.25081
Mantzoukas, S. & Eliopoulos, P.A. (2020). Endophytic Entomopathogenic Fungi: A Valuable Biological Control Tool against Plant Pests. Applied Sciences. 10: 360. https://doi.org/10.3390/app10010360
Martínez-Álvarez, P., Fernández-González, R.A., Sanz-Ros, A.V., Pando, V., Díez, J.J. (2016). Two fungal endophytes reduce the severity of pitch canker disease in Pinus radiata seedlings. Biological Control. 94: 1-10. https://doi.org/10.1016/j.biocontrol.2015.11.011
McMullin, D.R., Tanney, J.B., Daly, G.J., Miller, J.D. (2020). Antifungal polyketides from the Picea rubens and Vaccinium angustifolium endophyte Lachnellula calyciformis. Mycological Progress. 19 (10): 1101-1112. https://doi.org/10.1007/s11557-020-01620-5
Miranda, A.L.P., Silva, J.R., Rezende, C.M., Neves, J.S., Parrini, S.C., Pinheiro, M.L.B., Cordeiro, M.C., Tamborini, E., Pinto, A.C. (2000). Anti-inflammatory and Analgesic Activities of the Latex Containing Triterpenes from Himatanthus sucuuba. Planta Medica.66: 284-286. https://doi.org/10.1055/s-2000-8572
NCCLS. (2003). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard. Date of access: Janueary 20, 2016. Retrieved from: http://www.sbac.org.br/pt/pdfs/biblioteca/clsi_OPASM7_A6.pdf
Oliveira, J.A. dos S., Polli, A.D., Polonio, J.C., Orlandelli, R.C., Conte, H., Azevedo, J.L., Pamphile, J.A. (2020). Bioprospection and molecular phylogeny of culturable endophytic fungi associated with yellow passion fruit. Acta Scientiarum Biological Sciences. 42 (1): 48321. https://doi.org/10.4025/actascibiolsci.v42i1.48321
Oliveira, K.M., Boas, E.V., Bonett, L.P., Júnior, E.L.C., Bernardi-Wenzel, J. (2015). Isolamento e atividade antibacteriana de fungos endofíticos de Piper glabratum Kunth. Arquivos de Ciências da Saúde UNIPAR. 19: 3-9. https://doi.org/10.25110/arqsaude.v19i1.2015.5258
Osherov, N., May, G.S. (2001). The molecular mechanisms of conidial germination. FEMS Microbiology Letters. 199: 153-160. https://doi.org/10.1111/j.1574-6968.2001.tb10667.x
Passarini, M.R.Z., Santos, C., Lima, N., Berlinck, R.G.S., Sette, L.D. (2013). Filamentous fungi from the Atlantic marine sponge Dragmacidon reticulatum. Archives of Microbiology. 195: 99-111. https://doi.org/10.1007/s00203-012-0854-6
Peters, L.P., Prado, L.S., Silva, FI., Souza, F.S., Carvalho, C.M. (2020). Selection of endophytes as antagonists of Colletotrichum gloeosporioides in açaí palm. Biological Control. 150: 104350. https://doi.org/10.1016/j.biocontrol.2020.104350
Petrini, O., Sieber, T.N., Toti, L., Viret, O. (1993). Ecology, metabolite production, and substrate utilization in endophytic fungi. Natural Toxins. 1: 185-196. https://doi.org/10.1002/nt.2620010306
Photita, W., Lumyong, S., Lumyong, P., Hyde, K.D. (2001). Endophytic fungi of wild banana (Musa acuminata) at doi Suthep Pui National Park, Thailand. Mycological Research. 105: 1508-1513. https://doi.org/10.1017/S0953756201004968
Qu, H.R., Yang, W.W., Zhang, X.Q., Lu, Z.H., Deng, Z.S., Guo, Z.Y., Cao, F., Zou, K., Prokschc, P. (2020). Antibacterial bisabolane sesquiterpenoids and isocoumarin derivatives from the endophytic fungus Phomopsis prunorum. Phytochemistry Letters. 37: 1-4.
Rakshith, D., Gurudatt, D.M., Rao, H.Y., Mohana, N.C., Nuthan, B.R., Ramesha, K.P., Satish, S. (2020). Bioactivity-guided isolation of antimicrobial metabolite from Xylaria sp. Process Biochemistry. 92: 378-385.https://doi.org/10.1016/j.procbio.2020.01.028
Rodrigues, E., Almeida, J.M.D., Pires, J.M. (2010). Perfil farmacológico e fitoquímico de plantas indicadas pelos caboclos do Parque Nacional do Jaú (AM) como potenciais analgésicos. Revista Brasileira de Farmacognosia. 20: 981-991.https://doi.org/10.1590/S0102-695X2010005000008
Santos, C., Silva, B.N.S., Ferreira, A.F.T.A.F., Santos, C., Lima, N., Silva Bentes, J.L.S. (2020). Fungal endophytic community associated with guarana (Paullinia cupana var. Sorbilis): diversity driver by genotypes in the centre of origin. Journal of Fungi. 6 (3): 123. https://doi.org/10.3390/jof6030123
Silva, JRA, Rezende, CM, Pinto, AC, Amaral, ACF. (2010). Cytotoxicity and antibacterial studies of iridoids and phenolic compounds isolated from the latex of Himatanthus sucuuba. African Journal of Biotechnology. 9: 7357-7360. https://doi.org/10.5897/AJB10.345
Soares, D.C., Andrade, A.L., Delorenzi, J.C., Silva, J.R., Freire-de-Lima, L., Falcão, C.A., Pinto A.C., Rossi-Bergmann, B., Saraiva, E.M. (2010). Leishmanicidal activity of Himatanthus sucuuba latex against Leishmania amazonensis. Parasitology International. 59: 173-177. https://doi.org/10.1016/j.parint.2010.01.002
Sprenger, L.K., Vanhoni, M.S., Giese, E.G., Dos Santos, J.N., Molento, M.B. (2016). Efeito acaricida in vitro do extrato hidroalcoólico de Himatanthus sucuuba contra Rhipicephalus microplus. Archives of Veterinary Science. 21 (2): 6474. https://doi.org/10.5380/avs.v21i2.44506
Tamura, K., Dudley, J., Nei, M., Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution. 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
Udayanga, D., Liu, X., Mckenzie, E.H., Chukeatirote, E., Bahkali, A.H., Hyde, K.D. (2011). The genus Phomopsis: biology, applications, species concepts and names of common phytopathogens. Fungal Diversity. 50: 189. https://doi.org/10.1007/s13225-011-0126-9
Vaz, A.B.M., Da Costa, A.G.F.C., Raad, L.V.V., Goes-Neto, A. (2014). Fungal endophytes associated with three South American Myrtae (Myrtaceae) exhibit preferences in the colonization at leaf level. Fungal Biology. 118: 277-286. https://doi.org/10.1016/j.funbio.2013.11.010
Vitolo, M. & Pessoa Jr. A. (2015). Biotecnologia Farmacêutica: Aspectos sobre aplicação industrial. São Paulo: Editora Blucher, 50 p.
Weber, R.W., Stenger, E., Meffert, A., Hahn, M. (2004). Brefeldin A production by Phoma medicaginis in dead pre-colonized plant tissue: a strategy for habitat conquest? Mycological Research. 108: 662-671. https://doi.org/10.1017/S0953756204000243
White, T.J., Bruns, T., Lee, S.J.W.T., Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. 18: 315-322.
Yadav, P., Owiti, N., Kim, N. (2015). The role of topoisomerase I in suppressing genome instability associated with a highly transcribed guanine-rich sequence is not restricted to preventing RNA: DNA hybrid accumulation. Nucleic Acids Research. 44: 718-729. https://doi.org/10.1093/nar/gkv1152
Yang, ZD, Li, Z.J., Zhao, J.W., Sun, J.H., Yang, L.J., Shu, Z.M. (2019). Secondary metabolites and PI3K inhibitory activity of Colletotrichum gloeosporioides, a fungal endophyte of Uncaria rhynchophylla. Current Microbiology. 76 (7): 904-908.
Ye, D., Li, T., Yi, Y., Zhang, X., Zou, L. (2019). Characteristics of endophytic fungi from Polygonum hydropiper suggest potential application for P-phytoextraction. Fungal Ecology. 41: 126-136. https://doi.org/10.1016/j.funeco.2019.05.001
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