Endophytic fungi of Euterpe edulis (açaí-do-sul) fruits: antimicrobial activity and its relation with the growing medium
DOI:
https://doi.org/10.5327/rcaa.v17i1.2844Palabras clave:
Endophytes, biocontrol, Trichoderma sp., Penicillium sp..Resumen
Euterpe edulis (açaí-do-sul) have wide nutritional, pharmaceutical and industrial applications. Its extensive exploitation threatens this species with extinction. The endophytic fungi can produce similar compounds to their hosts. Thus, the present study is aimed to isolate endophytic fungi from the fruits of E. edulis and to evaluate their antimicrobial activities against Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, MRSA, and Candida albicans and the interference of the culture medium. Fungi were isolated in potato dextrose agar (PDA) medium. The isolates were characterized by morphology. The main genera isolated were Fusarium, Alternaria, Penicillium, Trichoderma, Acremonium and Aspergillus. The isolate Penicillium EFP1 shows antimicrobial activity against all the pathogens tested in PDA plus extract (PDAA). When in Sabouraud plus extract (SDAA), Penicillium EFP1 was able to inhibit all pathogens, except for P. aeroginosa. Trichoderma EFT. On the other hand, it only inhibited E. coli, S. aureus and MRSA, and the addition of the extract decreased the inhibition efficiency. The isolate Penicillium EFP1 presented significant inhibitory activity against pathogens, evidencing the potential for research papers in view of industrial interest and metabolites exploitation.
Descargas
Referencias
ABRAHÃO, M.R.E.; MOLINA, G., PASTORE, G.M. Endophytes: Recent developments in biotechnology and the
potential for flavor production. Food Research International, v.52, n.1, p.367-372, 2013. http://doi.org/10.1016/j.
foodres.2013.03.007
ALY, A.H.; DEBBAB, A.; PROKSCH, P. Fungal endophytes: unique plant inhabitants with great promises. Applied
Microbiology and Biotechnology, v.90, p.1829-1845, 2011. http://doi.org/10.1007/s00253-011-3270-y
ARAÚJO, W.L.; LIMA, A.O.S.; AZEVEDO, J.L.; MARCON, J.; SOBRAL, J.K.; LACAVA, P.T. Manual: isolamento de
microrganismos endofiticos. Piracicaba: CALQ, 2002. 86 p.
ARNOLD, A.E.; MAYNARD, Z.; GILBERT, G.S. Fungal endophytes in dicotyledonous neotropical trees: patterns
of abundance and diversity. Mycological Research, v.105, n.12, p.1502-1507, 2001. http://doi.org/10.1017/
S0953756201004956
BACKMAN, P.A.; SIKORA, R.A. Endophytes: An emerging tool for biological control. Biological Control, v.46, n.1,
p.1-3, 2008. http://doi.org/10.1016/j.biocontrol.2008.03.009
BARBOSA, P.P.M.; SPERANZA, P.; OHARA, A.; SILVA, É.B.; ANGELIS, D.A.; MACEDO, G.A. Biocatalysis and
agricultural biotechnology fungi from Brazilian Savannah and Atlantic rainforest show high antibacterial
and antifungal activity. Biocatalysis Agricultural Biotechnology, v.10, p.1-8, 2017. http://doi.org/10.1016/j.
bcab.2017.01.011
BENCHIMOL, M.; TALORA, D.C.; MARIANO-NETO, E.; OLIVEIRA, T.L.S.; LEAL, A.; MIELKE, M.S.; FARIA, D.
Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest.
Forest Ecology and Management, v.384, p.314-322, 2017. http://doi.org/10.1016/j.foreco.2016.11.014
BICUDO, M.O.P.; RIBANI, R.H.; BETA, T. Anthocyanins, phenolic acids and antioxidant properties of Juçara fruits
(Euterpe edulis M.) along the on-tree ripening process. Plant Foods for Human Nutrition, v.69, p.142-147,
http://doi.org/10.1007/s11130-014-0406-0
BONFIM, J.A.; VASCONCELLOS, R.L.F.; BALDESIN, L.F.; SIEBER, T.N.; CARDOSO, E.J.B.N. Dark septate
endophytic fungi of native plants along an altitudinal gradient in the Brazilian Atlantic forest. Fungal Ecology,
v.20, p.202-210, 2016. http://doi.org/10.1016/j.funeco.2016.01.008
BORGES, G.D.S.C.; VIEIRA, F.G.K.; COPETTI, C.; GONZAGA, L.V.; ZAMBIAZI, R.C.; MANCINI FILHO, J.; FETT,
R. Chemical characterization, bioactive compounds, and antioxidant capacity of jussara (Euterpe edulis) fruit
from the Atlantic Forest in southern Brazil. Food Research International, v.44, n.7, p.2128-2133, 2011. http://
doi.org/10.1016/j.foodres.2010.12.006
CALVO, A.M.; WILSON, R.A.; BOK, J.W.; KELLER, N.P. Relationship between secondary metabolism and fungal
development. Microbiology and Molecular Biology Reviews, v.66, n.3, p.447-459, 2002. https://dx.doi.org/10.
%2FMMBR.66.3.447-459.2002
CASTRO, C.C.; GUTIÉRREZ, A.H.; SOTÃO, H.M.P. Fungos conidiais em Euterpe oleracea Mart. (açaizeiro) na Ilha
do Combu, Pará-Brasil. Acta Botanica Brasilica, v.26, n.4, p.761-771, 2012. http://doi.org/10.1590/S0102-
CLINICAL AND LABORATORY STANDARDS INSTITUTE (CLSI). Padronização dos testes de Sensibilidade
a Antimicrobianos por Disco-difusão: Norma Aprovada. 8. ed. CLSI, 2003. v. 23, n. 1. Available from:
<http://anvisa.gov.br/servicosaude/manuais/clsi/clsi_OPASM2-A8.pdf>. Accessed on: Mar. 3, 2020.
CUNHA JUNIOR, L.C.C.; NARDINI, V.; KHATIWADA, B.P.; TEIXEIRA, G.H.A.; WALSH, K.B. Classification of intact
açaí (Euterpe oleracea Mart.) and juçara (Euterpe edulis Mart) fruits based on dry matter content by means of
near infrared spectroscopy. Food Control, v.50, p.630-636, 2015. http://doi.org/10.1016/j.foodcont.2014.09.046
DE HOOG, G.S.; GUARRO, J.; GENÉ, J.; FIGUERAS, M.J. Atlas of Clinical Fungi. 2. ed. Utrecht: Centraalbureau
voor Schimmelcultures / Universitat Rovira i Virgili / Reus, 2000.
DEEPIKA, V.B.; MURALI, T.S.; SATYAMOORTHY, K. Modulation of genetic clusters for synthesis of bioactive
molecules in fungal endophytes: A review. Microbiological Research, v.182, p.125-140, 2016. http://doi.
org/10.1016/j.micres.2015.10.009
DEUSCHLE, R.A.N.; CAMARGO, T.; ALVES, S.H.; MALLMANN, C.A.; HEIZMANN, B.M. Fracionamento do
extrato diclorometânico de Senecio desiderabilis Vellozo e avaliação da atividade antimicrobiana. Brazilian
Journal of Pharmacognozy, v.17, n.2, p.220-223, 2007. http://doi.org/10.1590/S0102-695X2007000200015
FREITAS, M.A.B.; VIEIRA, I.C.G.; ALBERNAZ, A.L.K.M.; MAGALHÃES, J.L.L.; LEES, A.C. Floristic impoverishment
of Amazonian floodplain forests managed for açaí fruit production. Forest Ecology and Management, v.351,
p.20-27, 2015. http://doi.org/10.1016/j.foreco.2015.05.008
GRANDI, R.A.P. Hifomicetos decompositores do folhedo de Euterpe edulis. Mart. Hoehnea, v.26, n.1, p.87-101, 1999.
GUL, H.T.; SAEED, S.; KHAN, F.A.Z. Entomopathogenic fungi as effective insect pest management tactic: A Review.
Applied Science and Business Economics, v.1, n.1, p.10-18, 2014.
HIGGINBOTHAM, S.J.; ARNOLD, A.E.; IBAÑEZ, A.; SPADAFORA, C.; COLEY, P.D.; KURSAR, T.A. Bioactivity of
fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants.
PLoS One, v.8, n.9, 2013. http://doi.org/10.1371/journal.pone.0073192
HOLLANDER, M.A.; WOLFE, D.; CHICKEN, E. The one-sample location problem. In: HOLLANDER, M.A.;
WOLFE, D.; CHICKEN, E. (orgs.). Nonparametric Statistical Methods. 3. ed. Hoboken: John Wiley & Sons,
http://doi.org/10.1002/9781119196037.ch3
KAWAGUCHI, A.; KOCH, G.G. Sanon: An R Package for Stratified Analysis with Nonparametric Covariable
Adjustment. Journal of Statistical Software, v.67, n.9, p.1-47, 2015. http://doi.org/10.18637/jss.v067.i09
KEMPF, K.; SCHMITT, F.; BILITEWSKI, U.; SCHOBERT, R. Synthesis, stereochemical assignment, and bioactivity
of the Penicillium metabolites penicillenols B1 and B2. Tetrahedron, v.71, n.31, p.5064-5068, 2015. http://doi.
org/10.1016/j.tet.2015.05.116
KERN, M.E.; BLEVINS, K.S. Micologia médica. São Paulo: Premier, 1999.
KOEGEL, S.; BRULÉ, D.; WIEMKEN, A.; BOLLER, T.; COURTY, P.E. The effect of different nitrogen sources on the
symbiotic interaction between Sorghum bicolor and Glomus intraradices: Expression of plant and fungal genes
involved in nitrogen assimilation. Soil Biology Biochemistry, v.86, p.159-163, 2015. http://doi.org/10.1016/j.
soilbio.2015.03.003
LIMA, C.P.; CUNICO, M.M.; MIYASAKI, C.M.S.; MIGUEL, O.G.; CÔCCO, L.C.; YAMAMOTO, C.I.; MIGUEL, M.D.
Conteúdo polifenólico e atividade antioxidante dos frutos da palmeira Juçara (Euterpe edulis Martius). Revista
Brasileira de Plantas Medicinais, v.14, n.2, p.321-326, 2012. http://doi.org/10.1590/S1516-05722012000200011
LUDWIG-MÜLLER, J. Plants and endophytes: equal partners in secondary metabolite production? Biotechnology
Letters, v.37, p.1325-1334, 2015. http://doi.org/10.1007/s10529-015-1814-4
MEDINA, J.M.; MOREIRA, S.L.S.; ALVES, R.C.; MARTINS, M.L.; CAMPOS, A.N.R. Mycorrhizal association in
Euterpe edulis Martius (Palmeira Juçara) in the municipality of Rio Pomba, MG. Vértices, v.14, n.2, p.159-167,
http://doi.org/10.5935/1809-2667.20120050
MUTAWILA, C.; VINALE, F.; HALLEEN, F.; LORITO, M.; MOSTERT, L. Isolation, production and in vitro effects
of the major secondary metabolite produced by Trichoderma species used for the control of grapevine trunk
diseases. Plant Pathology, v.65, n.1, p.104-113, 2016. http://doi.org/10.1111/ppa.12385
NIELSEN, J.C.; NIELSEN, J. Development of fungal cell factories for the production of secondary metabolites:
linking genomics and metabolism. Synthetic and Systems Biotechnology, v.2, n.1, p.5-12, 2017. http://doi.
org/10.1016/j.synbio.2017.02.002
OSTROSKY, E.A.; MIZUMOTO, M.K.; LIMA, M.E.L.; KANEKO, T.M.; NISHIKAWA, S.O.; FREITAS, B.R. Métodos para
avaliação da atividade antimicrobiana e determinação da concentração mínima inibitória (CMI) de plantas medicinais.
Revista Brasileira de Farmácia, v.18, n.2, p.301-307, 2008. https://doi.org/10.1590/S0102-695X2008000200026
PAREDES-LOPEZ, O.; CERVANTES-CEJA, M.L.; VIGNA-PÉREZ, M.; HERNÁNDEZ-PÉREZ, T. Berries: improving
human health and healthy aging, and promoting quality life — a review. Plant Foods for Human Nutrition,
v.65, p.299-308, 2010. http://doi.org/10.1007/s11130-010-0177-1
POLTRONIERI, T.P.S.; AZEVEDO, L.A.S.; VERZIGNASSI, J.R.; SILVA, D.E.M. Colletotrichum gloeosporioides em
frutos de juçara (Euterpe edulis) na Mata Atlântica, em Paraty-RJ e Ubatuba-SP. Summa Phytopathologica,
v.40, n.1, p.88-89, 2014. http://doi.org/10.1590/S0100-54052014000100015
POULOSE, S.M.; FISHER, D.R.; LARSON, J.; BIELINSKI, D.F.; RIMANDO, A.M.; CAREY, A.N.; SCHAUSS, A.G.;
SHUKITT-HALE, B. Anthocyanin-rich açai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory
stress signaling in mouse brain BV-2 microglial cells. Journal of Agricultural and Food Chemistry, v.60, n.4,
p.1084-1093, 2012. http://doi.org/10.1021/jf203989k
R CORE TEAM. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical
Computing, 2014. Available at: <http://www.R-project.org/>. Accessed on: Apr. 1, 2018.
RADHAKRISHNAN, R.; LEE, I. Penicillium – sesame interactions: A remedy for mitigating high salinity stress effects
on primary and defense metabolites in plants. Environmental and Experimental Botany, v.116, p.47-60, 2015.
http://doi.org/10.1016/j.envexpbot.2015.03.008
RODRIGUES, K.F. The foliar fungal endophytes of the Amazonian palm Euterpe oleracea. Mycology, v.86, n.3, p.376-
, 1994. http://doi.org/10.2307/3760568
STROBEL, G.; DAISY, B. Bioprospecting for microbial endophytes and their natural products. Microbiology and
Molecular Biology, v.67, n.4, p.491-502, 2003. https://dx.doi.org/10.1128%2FMMBR.67.4.491-502.2003
SURYANARAYANAN, T.S.; THIRUNAVUKKARASU, N.; GOVINDARAJULU, M.B.; SASSE, F.; JANSEN, R.;
MURALI, T.S. Fungal endophytes and bioprospecting. Fungal Biology Reviews, v.23, n.1-2, p.9-19, 2009.
http://doi.org/10.1016/j.fbr.2009.07.001
XU, L.; HAN, T.; WU, J.; ZHANG, Q.; ZHANG, H.; HUANG, B.-K.; RAHMAN, K.; QIN, L.-P. Comparative research of
chemical constituents, antifungal and antitumor properties of ether extracts of Panax ginseng and its endophytic
fungus. Phytomedicine, v.16, n.6-7, p.609-616, 2009. http://doi.org/10.1016/j.phymed.2009.03.014
YANTO, D.H.Y.; HIDAYAT, A.; TACHIBANA, S. Periodical biostimulation with nutrient addition and
bioaugmentation using mixed fungal cultures to maintain enzymatic oxidation during extended bioremediation
of oily soil microcosms. International Biodeterioration and Biodegradation, v.116, p.112-123, 2017. http://
doi.org/10.1016/j.ibiod.2016.10.023
YU, H.; ZHANG, L.; LI, L.; ZHENG, C.; GUO, L.; LI, W.; SUN, P.; QIN, L. Recent developments and future prospects
of antimicrobial metabolites produced by endophytes. Microbiological Research, v.165, n.6, p.437-449, 2010.
Descargas
Publicado
Número
Sección
Licencia
Derechos de autor 2023 Vivien Patrícia Garbin, Cristiane Vieira Helm, Patrícia do Rocio Dalzoto, Andressa Katiski da Costa Stuart, Bruno Accioly Alves Romagnoli, Thiago de Farias Pires, Ida Chapaval Pimentel
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial-SinDerivadas 4.0.
DECLARAÇÃO DE ORIGINALIDADE E DIREITOS AUTORAIS
Declaro que o presente artigo é original, não tendo sido submetido à publicação em qualquer outro periódico nacional ou internacional, quer seja em parte ou em sua totalidade.
Os direitos autorais pertencem exclusivamente aos autores. Os direitos de licenciamento utilizados pelo periódico é a licença Creative Commons Attribution 4.0 (CC BY NC ND 4.0)
Recomenda-se a leitura desse link para maiores informações sobre o tema: fornecimento de créditos e referências de forma correta, entre outros detalhes cruciais para uso adequado do material licenciado.
A obra Revista de Ciências Agroambientais (ISSN 1677-6062) está licenciado com uma Licença Creative Commons - Atribuição-NãoComercial-SemDerivações 4.0 Internacional.