Antimicrobial activity improvement after fractionating organic extracts from Lasiodiplodia sp. Fermentation / Melhoria da atividade antimicrobiana após fracionamento de extratos orgânicos de Lasiodiplodia sp. fermentação

Omar Cabezas Gómez, Dajara Moana Barbosa Moreira, Isara Lourdes Cruz Hernández, Raquel Maria Lima Lemes, Jaine Honorata Hortolan Luiz

Abstract


Endophytes constitute a promising source of bioactive substances with therapeutic potentialities. Thereby, an endophytic fungi was isolated from Handroanthus impetiginosus leaves and classified as Lasiodiplodia sp. by DNA sequence analysis and phylogenetic inference in this study. Chlorophorm (Ld-Chlo) and ethyl acetate extracts (Ld-EAm, Ld-AE and Ld-EA+) obtained from fungus fermentation broth have been fractionated, whose extracts and fractions have been tested for assessing their antimicrobial activity against four Gram-positive, two Gram-negative and three yeast strains. It was observed an antimicrobial profile regarding crude extracts against Gram-positive and yeast pathogens. The major inhibition was achieved by Ld-Chlo (MIC of 12.5-25 µg.mL-1) and Ld-EAm (MIC of 12.5-25 µg.mL-1), both against Candida parapsilosis. The extracts were more efficient against Listeria monocytongenes and C. parapsilosis pathogens. Fractionation increased the antimicrobial activity of fractions if compared to crude extracts, probably due to a higher concentration of bioactive compounds. Gass Chromatography (GC-MS) was performed using fractions from Ld-Chlo, through which it was possible to identify four known compounds with recognized antimicrobial activity: (Z)-docos-13-enamide (1), methyl (Z)-octadec-9-enoate (2), (Z)-octadec-9-enamide (3) and dodecanamide (4).. Thence, it is suggested that the fractionation of crude extracts improve antibacterial and antifungal activities and that the identified bioactive compounds are at the helm of the antimicrobial activity presented by some fractions.

 

 


Keywords


antimicrobial activity, Lasiodiplodia sp., endophytic fungi, fermentation, bioactive compounds.

Full Text:

PDF

References


WHO (2017) Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. World Health Organization. https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf?ua=1. Accessed 26 November 2019

Pogue JM, Kaye KS, Cohen DA, Marchaim D (2015) Appropriate antimicrobial therapy in the era of multidrug-resistant human pathogens. Clin Microbiol Infect 21:302–312. https://doi.org/10.1016/j.cmi.2014.12.025

Debroy S, Prosper O, Mishoe A, Mubayi A (2017) Challenges in modeling complexity of neglected tropical diseases: A review of dynamics of visceral leishmaniasis in resource limited settings. Emerg Themes Epidemiol 14:10. https://doi.org/10.1186/s12982-017-0065-3

Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D (2016) A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis 10:1–40. https://doi.org/10.1371/journal.pntd.0004349

Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, Nisar MA, Alvi RF, Aslam MA, Qamar MU, Salamat MKF, Baloch Z (2018) Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist 11:1645–1658. https://doi.org/10.2147/IDR.S173867

Strobel GA, Stierle A, Hess WM (1993) Taxol formation in yew - Taxus. Plant Sci 92(1):1–12. https://doi.org/10.1016/0168-9452(93)90060-D

Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459. https://doi.org/10.1039/b100918o

Kharwar RN, Mishra A, Gond SK, Stierle A, Stierle D (2011) Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep 28:1208–1228. https://doi.org/10.1039/c1np00008j

Deshmukh SK, Verekar SA, Bhave SV (2015) Endophytic fungi: a reservoir of antibacterials. Front Microbiol 5:715. https://doi.org/10.3389/fmicb. 2014.00715

Venieraki A, Dimou M, Katinakis P (2017) Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their hosts. Hell Plant Prot J 10:51–66. https://doi.org/10.1515/hppj-2017-0006

Jha S (2019) Endophyte and Secondary Metabolites. Springer, Switzerland

Dissanayake AJ, Phillips AJL, Li XH, Hyde KD (2016) Botryosphaeriaceae: Current status of genera and species. Mycosphere 7:1001–1073. https://doi.org/10.5943/mycosphere/si/1b/13

Cruywagen EM, Slippers B, Roux J, Wingfield MJ (2016) Phylogenetic species recognition and hybridization in Lasiodiplodia: A case study on species from baobabs. Fungal Biol 121:420-436 http://dx.doi.org/10.1016/j.funbio.2016.07.014

Rodríguez-Gálvez E, Maldonado E, Alves A (2015) Identification and pathogenicity of Lasiodiplodia theobromae causing dieback of table grapes in Peru. Eur J Plant Pathol 141:477-489. https://doi.org/10.1007/s10658-014-0557-8

Cimmino A, Cinelli T, Masi M, Reveglia P, da Silva MA, Mugnai L, Michereff SJ, Surico G, Evidente A (2017) Phytotoxic lipophilic metabolites produced by grapevine strains of Lasiodiplodia species in Brazil. J Agric Food Chem 65:1102–1107. https://doi.org/10.1021/acs.jafc.6b04906

Félix C, Salvatore MM, DellaGreca M, Meneses R, Duarte AS, Salvatore F, Naviglio D, Gallo M, Jorrín-Novo JV, Alves A, Andolfi A, Esteves AC (2018) Production of toxic metabolites by two strains of Lasiodiplodia theobromae, isolated from a coconut tree and a human patient. Mycol 110:642-653. https://doi.org/10.1080/00275514.2018.1478597

Ali SS, Asman A, Shao J, Balidion JF, Strem MD, Puig AS, Meinhardt LW, Bailey BA (2020) Genome and transcriptome analysis of the latent pathogen Lasiodiplodia theobromae, an emerging threat to the cacao industry. Genome 63:37-52. http://dx.doi.org/10.1139/gen-2019-0112

Wei W, Jiang N, Mei YM, Chu YN, Ge HM, Song YC, Ng SW, Tan RX (2014) An antibacterial metabolite from Lasiodiplodia pseudotheobromae F2. Phytochem 100:103–109. http://dx.doi.org/10.1016/j.phytochem.2014.01.003

Umeokoli BO, Ebrahim W, El-Neketi M, Müller WEG, Kalscheuer R, Lin W, Liu Z, Proksch P (2018) A new depsidone derivative from mangrove sediment derived fungus Lasiodiplodia theobromae. Nat Prod Res. https://doi.org/10.1080/14786419.2018.1496430

Chen S, Chen D, Cai R, Cui H, Long Y, Lu Y, Li C, She Z (2016) Cytotoxic and antibacterial preussomerins from the mangrove endophytic fungus Lasiodiplodia theobromae ZJ-HQ1. J Nat Prod 79:2397-2402. http://dx.doi.org/10.1021/acs.jnatprod.6b00639

Kamal N, Viegelmann CV, Clements CJ, Edrada-Ebel RA (2016) Metabolomics-guided isolation of anti-trypanosomal metabolites from the endophytic fungus Lasiodiplodia theobromae. Planta Med 83:565-573. http://dx.doi.org/10.1055/s-0042-118601

Pandi M, Kumaran RS, Choi YK, Kim HJ, Muthumary J (2011) Isolation and detection of taxol, an anticancer drug produced from Lasiodiplodia theobromae, an endophytic fungus of the medicinal plant Morinda citrifolia. Afr J Biotechnol 10:1428-1435. https://doi.org/10.5897/AJB10.950

Huang J, Xu J, Wang Z, Khan D, Niaz SI, Zhu Y, Lin Y, Li J, Liu L (2017) New lasiodiplodins from mangrove endophytic fungus Lasiodiplodia sp. 318#. Nat Prod Res 31:326–332. https://doi.org/10.1080/14786419.2016.1239096

Martinez-Klimova E, Rodríguez-Peña K, Sánchez S (2017) Endophytes as sources of antibiotics. Biochem Pharmacol 134:1–17. http://dx.doi.org/10.1016/j.bcp.2016.10.010

Huang C, Chen T, Yan Z, Guo H, Hou X, Jiang L, Long Y (2019) Thiocladospolide E and cladospamide A, novel 12-membered macrolide and macrolide lactam from mangrove endophytic fungus Cladosporium sp. SCNU-F0001. Fitoter 137:104246. https://doi.org/10.1016/j.fitote.2019.104246

Devarajan PT, Suryanarayanan TS, Geetha V (2002) Endophytic fungi associated with the tropical seagrass Halophila ovalis (Hydrocharitaceae). Indian J Mar Sci 31:73–74. https://pdfs.semanticscholar.org/1ad8/d3f7a72e072176287e97356875f4a641a478.pdf. Accessed 20 November 2019

Capriles CH, Mata S, Middelveen M (1989) Preservation of fungi in water (Castellani): 20 years. Mycopathol 106:73-79. https://doi.org/10.1007/BF00437084

Raeder J, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17-20. https://doi.org/10.1111/j.1472-765X.1985.tb01479.x

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680. https://doi.org/10.1093/nar/22.22.4673

Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599. https://doi.org/10.1093/molbev/msm092

Kimura MA (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120. https://doi.org/10.1007/BF01731581

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

Clinical and Laboratory Standards Institute (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts-3rd edition. CLSI Approved Standard M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA, USA

Clinical and Laboratory Standards Institute (2015). Methods for Antimicrobial Susceptibility Testing of Aerobic Bacteria-10th edition. CLSI Approved Standard M07-A10. Clinical and Laboratory Standards Institute, Wayne, PA, USA

Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321-324. https://doi.org/10.1016/j.ymeth.2007.01.006.

Phillips AJL, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, Groenewald JZ, Crous PW (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167. https://doi.org/10.3114/sim0021

Slippers B, Roux J, Wingfield MJ, Van der Walt FJJ, Jami F, Mehl JWM, Marais GJ (2014) Confronting the constraints of morphological taxonomy in the Botryosphaeriales. Pers 33:155–168. 10.3767/003158514X684780

Holetz FB, Pessini GL, Sanches NR, Cortez DA, Nakamura CV, Filho BP (2002) Screening of some plants used in the Brazilian folk medicine for the treatment of infectious diseases. Meml Inst Oswaldo Cruz 97:1027-1031. https://doi.org/10.1590/s0074-02762002000700017

Kuete V (2010) Potential of cameroonian plants and derived products against microbial infections: A Review. Planta Med 76: 1479–1491. https://doi.org/10.1055/s-0030-1250027

Etame RE, Mouokeu RS, Pouaha CLC, Kenfack IV, Tchientcheu R, Assam JPA, Poundeu FSM, Tiabou AT, Etoa FX, Kuiate JR, Ngane RAN (2018) Effect of fractioning on antibacterial activity of Enantia chlorantha Oliver (Annonaceae) Methanol Extract and Mode of Action. Evid Based Complement Altern Med. https://doi.org/10.1155/2018/4831593

Etame RE, Mouokeu RS, Poundeu FSM, Voukeng IK, Cidjeu CLP, Tiabou AT, Yaya AJY, Ngane RAN, Kuiate JR, Etoa FX (2019) Effect of fractioning on antibacterial activity of n-butanol fraction from Enantia chlorantha stem bark methanol extract. BMC Complement Altern Med 19:56 https://doi.org/10.1186/s12906-019-2459-y

Voukeng IK, Nganou BK, Sandjo LP, Celik I, Beng VP, Tane P, Kuete V (2017) Antibacterial activities of the methanol extract, fractions and compounds from Elaeophorbia drupifera (Thonn.) Stapf. (Euphorbiaceae). BMC Complement Altern Med 17:28. https://doi.org/10.1186/s12906-016-1509-y

Palem PPC, Kuriakose GC, Jayabaskaran C (2015) Correction: an endophytic fungus, Talaromyces radicus, isolated from Catharanthus roseus, produces vincristine and vinblastine, which induce apoptotic cell death. Appl Microbiol Biotechnol. https://doi.org/10.1371/ journal.pone.0153111

Weiner LM, Webb AK, Limbago B, Dudeck MA, Patel J, Kallen AJ, Edwards JR, Sievert DM (2016) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011–2014. Infect Control Hosp Epidemiol 37:1288-1301. https://doi.org/10.1017/ice.2016.174

Paul S, Kannan I, Mohanram K (2019) Extensive ERG11 mutations associated with fluconazole-resistant Candida albicans isolated from HIV-infected patients. Curr Med Mycol 5:1-6. https://doi.org/10.18502/cmm.5.3.1739

Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, Rodloff A, Fu W, Ling TA (2010) Results from the ARTEMIS DISK global antifungal surveillance study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J Clin Microbiol 48:1366–77. https://doi.org/10.1128/JCM.02117-09

Colombo AL, Nucci M, Park BJ, Nouér SA, Arthington-Skaggs B, da Matta DA, Warnock D, Morgan J (2006) Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J Clin Microbiol 44:2816–23. https://doi.org/10.1128/JCM.00773-06

Pfaller MA, Andes DR, Diekema DJ, Horn DL, Reboli AC, Rotstein C, Franks B, Azie NE (2014) Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2,496 patients: data from the Prospective Antifungal Therapy (PATH) registry 2004–2008. PLoS One. https://doi.org/10.1371/journal.pone.0101510

Hinrichsen SL, Falcão E, Vilella TAS, Colombo AL, Nucci M, Moura L, Rêgo L, Lira C, Almeida L (2008) [Candidemia in a tertiary hospital in northeastern Brazil]. Rev Soc Bras Med Trop 41:394–8. https://doi.org/10.1590/s0037-86822008000400014

Pinhati HM, Casulari LA, Souza AC, Siqueira RA, Damasceno CM, Colombo AL (2016) Outbreak of candidemia caused by fluconazole resistant Candida parapsilosis strains in an intensive care unit. BMC Infect Dis. 10.1186/s12879-016-1767-9

CDC (2019) Antibiotic resistance threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf. Accessed 25 December 2019

Adnan M, Nazim Uddin Chy M, Mostafa Kamal ATM, Obyedul Kalam Azad M, Paul A, Uddin SB, Barlow JW, Faruque MO, Park CH, Cho DH (2019) Investigation of the Biological Activities and Characterization of Bioactive Constituents of Ophiorrhiza rugosa var. prostrata (D.Don) & Mondal Leaves through In Vivo, In Vitro, and In Silico approaches. Mol 24:1367. https://doi.org/10.3390/molecules24071367

Chandrasekharan M, Kannathasan K, Venkatesalu V (2008) Antimicrobial activity of fatty acid methyl esters of some members of chenopodiaceae. Z Naturforsch C J Biosci 63:331-6. https://doi.org/10.1515/znc-2008-5-604

Lima LA, Johann S, Cisalpino PS, Pimenta LP, Boaventura MA (2011) In vitro antifungal activity of fatty acid methyl esters of the seeds of Annona cornifolia A.St.-Hil. (Annonaceae) against pathogenic fungus Paracoccidioides brasiliensis. Rev Soc Bras Med Trop 44:777-80. https://doi.org/10.1590/s0037-86822011000600024

Ali A, Javaid A, Shoaib A (2016) GC-MS analysis and antifungal activity of methanolic root extract. Planta Daninha. https://doi.org/10.1590/s0100-83582017350100046

Hussein HM, Hameed IH, Ibraheem OA (2016) Antimicrobial activity and spectral chemical analysis of methanolic leaves extract of Adiantum capillus-veneris using GC-MS and FT-IR Spectroscopy. Int J Pharmacogn Phytochem Res 8:369-385

Abdalha AA, Mekawey AAI (2013) Antimicrobial susceptibility of certain fungal and bacterial strains to dodecanamide and quinazolinone derivatives. World Appl Sci J 24:312-319. https://doi.org/10.5829/idosi.wasj.2013.24.03.509

Mojid MA, Jae H (2014) Antibacterial and antiyeast compounds from marine-derived bacteria. Mar Drugs 12:2913–2921. https://doi.org/10.3390/md12052913

Jayalakshmi M, Vanitha V, Pushpabharathi N (2018) Biochemical screening of Penaeus vannamei shell waste by liquid chromatography-tandem mass spectrometry. Asian J Chem 30:1311-1316. https://doi.org/10.14233/ajchem.2018.21229

Gómez OC, Luiz JHH (2018) Endophytic fungi isolated from medicinal plants: future prospects of bioactive natural products from Tabebuia/Handroanthus endophytes. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-018-9344-3




DOI: https://doi.org/10.34117/bjdv7n1-257

Refbacks

  • There are currently no refbacks.