[en] Bacterial resistance to antibiotics is a serious public health problem that needs new antibacterial compounds for control. Fungi, including resupinated fungi, are a potential source to discover new bioactive compounds efficient again to bacteria resistant to antibiotics. The inhibitory capacity against the bacterial species was statistically evaluated. All the species (basidiomata and strains) were molecularly characterized with the ITS1-5.8S-ITS2 barcoding marker. The strains Ceraceomyces sp., Fuscoporia sp., Gloeocystidiellum sp., Oliveonia sp., Phanerochaete sp., and Xenasmatella sp. correspond to resupinate Basidiomycetes, and only the strain Hypocrea sp. is an Ascomycete, suggesting contamination to the basidiome of Tulasnella sp. According to the antagonistic test, only the Gloeocystidiellum sp. strain had antibacterial activity against the bacterial species Escherichia coli of clinical interest. Statistically, Gloeocystidiellum sp. was significantly (<0.001) active against two E. coli pathotypes (O157:H7 and ATCC 25922). Contrarily, the antibacterial activity of fungi against other pathotypes of E. coli and other strains such as Serratia sp. was not significant. The antibacterial activity between 48 and 72 h increased according to the measurement of the inhibition halos. Because of this antibacterial activity, Gloeocystidiellum sp. was taxonomically studied in deep combined morphological and molecular characterization (ITS1-5.8S-ITS2; partial LSU D1/D2 of nrDNA). A new species Gloeocystidiellum lojanense, a resupinate and corticioid fungus from a tropical montane rainforest of southern Ecuador, with antibacterial potential against E. coli, is proposed to the science.
Jaramillo-Riofrío, Andrea ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Microbial Systems Ecology and Evolution MS2E, Biodiversity of Tropical Ecosystems BIETROP Research Groups, Departamento de Ciencias de la Salud, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Loja 1101608, Ecuador ; Département de Biologie, Ecologie et Evolution, Université de Liège, Quai Van Beneden, BE-4000 Liège, Belgium
Decock, Cony; Mycothèque de l'Université Catholique de Louvain (MUCL, BCCM), Earth and Life Institute-Microbiology (ELIM), Université Catholique de Louvain, Croix du Sud 2 bte L7.05.06, BE-1348 Louvain-la-Neuve, Belgium
Suárez, Juan Pablo ; Microbial Systems Ecology and Evolution MS2E, Biodiversity of Tropical Ecosystems BIETROP Research Groups, Departamento de Ciencias de la Salud, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Loja 1101608, Ecuador
Benítez, Ángel ; Microbial Systems Ecology and Evolution MS2E, Biodiversity of Tropical Ecosystems BIETROP Research Groups, Departamento de Ciencias de la Salud, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Loja 1101608, Ecuador
Castillo Cabello, Gabriel ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution
Cruz, Darío ; Microbial Systems Ecology and Evolution MS2E, Biodiversity of Tropical Ecosystems BIETROP Research Groups, Departamento de Ciencias de la Salud, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Loja 1101608, Ecuador ; Instituto Nacional de Biodiversidad INABIO, Quito 17078976, Ecuador
Language :
English
Title :
Screening of Antibacterial Activity of Some Resupinate Fungi, Reveal Gloeocystidiellum lojanense sp. nov. (Russulales) against E. coli from Ecuador.
ARES - Académie de Recherche et d'Enseignement Supérieur [BE] ULiège - Université de Liège [BE] UCL - Université Catholique de Louvain [BE] UTPL - Universidad Técnica Particular de Loja [EC]
Funding text :
This research was funded by Académie de Recherche et d’enseignement supérieur (ARES), Université de Liège, Université Catholique de Louvain and Universidad Técnica Particular de Loja, grant number.
Mir M. Rasool U. Aisha S. Alshehri B. Hamadani S. Human pathogenic microbes (bacterial and fungal) and associated diseases Hum. Pathog. Microbes 2022 1 30 10.1016/B978-0-323-96127-1.00002-4
Lagadinou M. Onisor M. Rigas A. Musetescu D. Gkentzi D. Assimakopoulos S. Panos G. Marangos M. Antimicrobial properties on non-antibiotic drugs in the era of increased bacterial resistance Antibiotics 2020 9 107 10.3390/antibiotics9030107
Zhang F. Cheng W. The mechanism of bacterial resistance and potential bacteriostatic strategies Antibiotics 2022 11 1215 10.3390/antibiotics11091215
Mena Y. Ramírez L. Arango Á. Actividad antibacteriana y antioxidante del hongo Phanerochaete spp Inf. Tecnol. 2021 32 69 78 10.4067/S0718-07642021000100069
Pérez Guerrero P. Galán Sánchez F. Gutiérrez Saborido D. Guerrero Lozano I. Infecciones por enterobacterias Med.-Programa Form. Médica Contin. Acreditado 2014 11 3276 3282 10.1016/S0304-5412(14)70768-1
Janda J. Abbott S. The changing face of the family Enterobacteriaceae (Order: “Enterobacterales”): New members, taxonomic issues, geographic expansion, and new diseases and disease syndromes Clin. Microbiol. Rev. 2021 34 e00174-20 10.1128/CMR.00174-20 33627443
Staley Z. He D. Edge T. Persistence of fecal contamination and pathogenic Escherichia coli O157:H7 in snow and snowmelt J. Great Lakes Res. 2017 43 248 254 10.1016/j.jglr.2017.01.006
Uprety S. Dangol B. Nakarmi P. Dhakal I. Sherchan S. Shisler J. Jutla A. Amarasiri M. Sano D. Nguyen T. Assessment of microbial risks by characterization of Escherichia coli presence to analyze the public health risks from poor water quality in Nepal Int. J. Hyg. Environ. Health 2020 226 113484 10.1016/j.ijheh.2020.113484
Morosini M. del Campo R. Urinary tract infections and antimicrobial resistance Rev. Clín. Esp. 2019 219 149 150 10.1016/j.rce.2018.12.003
Centers for Disease Control and Prevention (CDC) “Vital signs: Carbapenem-resistant Enterobacteriaceae.” MMWR Morb. Mortal. Wkly. Rep. 2013 62 165 170
Monteiro A. Cardoso J. Guerra N. Ribeiro E. Viegas C. Cabo Verde S. Sousa-Uva A. Exposure and health effects of bacteria in healthcare units: An overview Appl. Sci. 2022 12 1958 10.3390/app12041958
Shen S. Qu X. Zhang W. Li J. Lv Z. Infection against infection: Parasite antagonism against parasites, viruses and bacteria Infect. Dis. Poverty 2019 8 1 12 10.1186/s40249-019-0560-6
Pulingam T. Parumasivam T. Gazzali A. Sulaiman A. Chee J. Lakshmanan M. Chin C. Sudesh K. Antimicrobial resistance: Prevalence, economic burden, mechanisms of resistance and strategies to overcome Eur. J. Pharm. Sci. 2022 170 106103 10.1016/j.ejps.2021.106103
Morrill H. Pogue J. Kaye K. LaPlante K. Treatment options for carbapenem-resistant Enterobacteriaceae infections Open Forum Infect. Dis. 2015 2 ofv050 10.1093/ofid/ofv050
Ciabuschi F. Lindahl O. The decline of innovation in the antibiotics industry and the global threat of antibiotic resistance: When entrepreneurial efforts are not enough Entrep. Ind. Life Cycle 2018 205 229 10.1007/978-3-319-89336-5_9
Singh D. Thapa S. Mahawar H. Kumar D. Geat N. Singh S. Prospecting potential of endophytes for modulation of biosynthesis of therapeutic bioactive secondary metabolites and plant growth promotion of medicinal and aromatic plants Antonie Van Leeuwenhoek 2022 115 699 730 10.1007/s10482-022-01736-6
Kamaruzaman N. Mohd Noor N. Radin Mohamed R. Al-Gheethi A. Ponnusamy S. Sharma A. Vo D. Applicability of bio-synthesized nanoparticles in fungal secondary metabolites products and plant extracts for eliminating antibiotic-resistant bacteria risks in non-clinical environments Environ. Res. 2022 209 112831 10.1016/j.envres.2022.112831
Hyde K. Tennakoon D. Jeewon R. Bhat D. Maharachchikumbura S. Rossi W. Leonardi M. Lee H. Mun H. Houbraken J. et al. Fungal diversity notes 1036–1150: Taxonomic and phylogenetic contributions on genera and species of fungal taxa Fungal Divers. 2019 96 1 242 10.1007/s13225-019-00429-2
Purvis A. Hector A. Getting the measure of biodiversity Nature 2000 405 212 219 10.1038/35012221
Baldrian P. Větrovský T. Lepinay C. Kohout P. High-throughput sequencing view on the magnitude of global fungal diversity Fungal Divers. 2021 114 539 547 10.1007/s13225-021-00472-y
Sidorova I.I. Velikanov L.L. Bioactive substances of agaricoid basidiomycetes and their possible role in regulation of myco- and microbiota structure in soils of forest ecosystems. I. Antibiotic activity of water extracts from basidioms of several dominant agaricoid basidiomycetes Mikol. Fitopatol. 2000 34 11 17
Kumar V. Prasher I. Antimicrobial potential of endophytic fungi isolated from Dillenia indica L. and identification of bioactive molecules produced by Fomitopsis meliae (Undrew.) Murril Nat. Prod. Res. 2022 36 1 5 10.1080/14786419.2022.2043855 35220841
Alkhulaifi M. Awaad A. AL-Mudhayyif H. Alothman M. Alqasoumi S. Zain S. Evaluation of antimicrobial activity of secondary metabolites of fungi isolated from Sultanate Oman soil Saudi Pharm. J. 2019 27 401 405 10.1016/j.jsps.2018.12.009 30976184
Karwehl S. Stadler M. Exploitation of fungal biodiversity for discovery of novel antibiotics Curr. Top. Microbiol. Immunol. 2016 303 338 10.1007/82_2016_496
Venturini M. Rivera C. Gonzalez C. Blanco D. Antimicrobial activity of extracts of edible wild and cultivated mushrooms against foodborne bacterial strains J. Food Prot. 2008 71 1701 1706 10.4315/0362-028X-71.8.1701
Winnie C.S. Stephen A.I. Josphat C.M. Antimicrobial activity of basidiomycetes fungi isolated from a Kenyan tropical forest Afr. J. Biotechnol. 2019 18 112 123 10.5897/AJB2018.16660
Batallas-Molina R. Moya-Marcalla G.F. Navas Muñoz D. Listado de la colección de hongos (Ascomycota y Basidiomycota) del Herbario Nacional del Ecuador (QCNE) del Instituto Nacional de Biodiversidad (INABIO) Av. Cienc. Ing. 2021 12 38 71
Cruz D. Suárez J. Piepenbring M. Morphological revision of Tulasnellaceae, with two new species of Tulasnella and new records of Tulasnella spp. for Ecuador Nova Hedwig. 2016 102 279 338 10.1127/nova_hedwigia/2015/0304
Gates G. Goyes P. Gundogdu F. Cruz J. Ratkowsky D. Small plot surveying reveals high fungal diversity in the Ecuadorian Amazon–A case study Curr. Res. Environ. Appl. Mycol. 2021 11 16 36 10.5943/cream/11/1/2
Læssøe T. Petersen J.H. Svampelivet på ækvator Svampe 2008 58 1 53
Cruz D. Suárez J. Kottke I. Piepenbring M. Oberwinkler F. Defining species in Tulasnella by correlating morphology and nrDNA ITS-5.8S sequence data of basidiomata from a tropical Andean forest Mycol. Prog. 2011 10 229 238 10.1007/s11557-010-0692-3
Cruz D. Suárez J. Kottke I. Piepenbring M. Cryptic species revealed by molecular phylogenetic analysis of sequences obtained from basidiomata of Tulasnella Mycol. Progress 2014 106 708 722 10.3852/12-386 24874921
Toapanta-Alban C. Ordoñez M. Barnes C. Blanchette R. Taxonomy of the major rhizomorphic species of the “Melanopus group” within Polyporaceae in Yasuní National Park, Ecuador PLoS ONE 2021 16 e0254567 10.1371/journal.pone.0254567 34347816
Toapanta-Alban C. Ordoñez M. Blanchette R. New findings on the biology and ecology of the Ecuadorian Amazon fungus Polyporus leprieurii var. yasuniensis J. Fungi 2022 8 203 10.3390/jof8020203
Sárközy A. Kúsz N. Zomborszki Z. Csorba A. Papp V. Hohmann J. Vanyolos A. Isolation and characterization of chemical constituents from the Poroid Medicinal Mushroom Porodaedalea chrysoloma (Agaricomycetes) and their antioxidant activity Int. J. Med. Mushrooms 2020 22 125 131 10.1615/IntJMedMushrooms.2020033698 32479001
Gamboa-Trujillo P. Wartchow F. Cerón-Martinez C. Andi D. Uwinjin P. Grefa G. Entza M. Chimbo E. Chimbo J. Payaguaje J. et al. Edible mushrooms of Ecuador: Consumption, myths and implications for conservation Ethnobot. Res. Appl. 2019 18 1 15 10.32859/era.18.38.1-15
Andrade J.M. Malagón O. Piepenbring M. Armijos C. Etnomicología y valor nutricional de macrohongos silvestres de la comunidad indígena Saraguro en el Sur del Ecuador Boletin Soc. Micológica Madr. 2012 36 193 201
Benítez Á. Cruz D. Vega M. González L. Jaramillo N. López F. Aguirre Z. Briófitos y hongos (liquenizados y no liquenizados) del Parque Universitario Francisco Vivar Castro, Loja, Ecuador Bosques Latid. Cero 2021 11 1 18 10.54753/blc.v11i2.1102
Kuhar F. Furci G. Drechsler-Santos E. Pfister D. Delimitation of Funga as a valid term for the diversity of fungal communities: The Fauna, Flora & Funga proposal (FF&F) IMA Fungus 2018 9 A71 A74 10.1007/BF03449441
Binder M. Hibbett D. Larsson K. Larsson E. Langer E. Langer G. The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes) Syst. Biodivers. 2005 3 113 157 10.1017/S1477200005001623
Piepenbring M. López F. Cáceres O. Colaboradores escondidos–La Importancia de los Hongos en los Ecosistemas Información para Educación Ambiental Puente Biol. 2019 8 57 91
Hallenberg N. Ryberg M. Nilsson R. Wood A. Wu S. Pseudolagarobasidium (Basidiomycota): On the reinstatement of a genus of parasitic, saprophytic, and endophytic resupinate fungi Botany 2008 86 1319 1325 10.1139/B08-088
Mosquera-Espinosa A. Bayman P. Prado G. Gómez-Carabalí A. Otero J. The double life of Ceratobasidium: Orchid mycorrhizal fungi and their potential for biocontrol of Rhizoctonia solani sheath blight of rice Mycologia 2013 105 141 150 10.3852/12-079
Sánchez-García M. Ryberg M. Khan F. Varga T. Nagy L. Hibbett D. Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi Proc. Natl. Acad. Sci. USA 2020 117 32528 32534 10.1073/pnas.1922539117 33257574
Silva S. Melo B. Santos M. Rios R. Santos C. Júnior K. Maranhão F. Santos T. Fraga A. Endophytic fungi: Benefits for plants and biotechnological potential Res. Soc. Dev. 2022 11 e9211427008 10.33448/rsd-v11i4.27008
Homeier J. Werner F.A. Gradstein S.R. Potential vegetation and floristic composition of Andean forests in South Ecuador, with a focus on the RBSF Gradients in a Tropical Mountain Ecosystem of Ecuador: Ecological Studies Beck E. Bendix J. Kottke I. Makeschin F. Mosandl R. Springer Berlin/Heidelberg, Germany 2008 87 100 10.1007/978-3-540-73526-7
Homeier J. Hertel D. Camenzind T. Cumbicus N.L. Maraun M. Martinson G.O. Poma L.N. Rillig M.C. Sandmann D. Scheu S. et al. Tropical Andean forests are highly susceptible to nutrient inputs-rapid effects of experimental N and P addition to an Ecuadorian montane forest PLoS ONE 2012 7 e47128 10.1371/journal.pone.0047128
Bendix J. Rollenbeck R. Göttlicher D. Cermak J. Cloud occurrence and cloud properties in Ecuador Clim. Res. 2006 30 133 147 10.3354/cr030133
Xing J.-H. Song J. Decock C. Cui B.-K. Morphological characters and phylogenetic analysis reveal a new species within the Ganoderma lucidum complex from South Africa Phytotaxa 2016 226 115 224 10.11646/phytotaxa.266.2.5
Wu S.H. Studies on Gloeocystidiellum sensu lato (Basidiomycotina) in Taiwan Mycotaxon 1996 58 1 68
Larsson K.H. Ryvarden L. Corticioid fungi of Europe Fungiflora 2021 1 253 257
Esquemas de Color Hexagonal, Pesquisa de Pintura, Paletas de Colores y Conversions Available online: https://encycolorpedia.es/ (accessed on 11 July 2022)
White T. Bruns T. Lee S. Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics PCR Protoc. 1990 18 315 322
Katoh K. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform Nucleic Acids Res. 2002 30 3059 3066 10.1093/nar/gkf436 12136088
Müller K. Quandt D. Müller J. Neinhuis C. PhyDE-Phylogenetic Data Editor. Program Distributed by the Authors, Version 10.0 2005 Available online: https://www.phyde.de (accessed on 2 May 2022)
Tamura K. Stecher G. Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11 Mol. Biol. Evol. 2021 38 3022 3027 10.1093/molbev/msab120 33892491
Gorjón S. Hallenberg N. Some new species and a first checklist of corticioid fungi (Basidiomycota) from Chile Mycol. Prog. 2012 12 185 192 10.1007/s11557-012-0824-z
Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J. Mol. Evol. 1980 16 111 120 10.1007/BF01731581
CLSI Performance Standards for Antimicrobial Susceptibility Testing CLSI Supplement M100 Clinical and Laboratory Standards Institute Wayne, PA, USA 2022 978-1-68440-135-2
CLSI Performance Standards for Antimicrobial Disk Susceptibility Tests CLSI Standard M02 Clinical and Laboratory Standards Institute Wayne, PA, USA 2018 1-56238-835-5
CLSI Methods for Dilution Antimicrobial Susceptibility Test for Bacteria that Grow Aerobically CLSI Standard M07 Clinical and Laboratory Standards Institute Wayne, PA, USA 2018 1-56238-837-1
RStudio Team RStudio: Integrated Development for R RStudio, PBC Boston, MA, USA 2020
Larsson E. Hallenberg N. Species delimitation in the Gloeocystidiellum porosum-clavuligerum complex inferred from compatibility studies and nuclear rDNA sequence data Mycologia 2001 93 907 914 10.1080/00275514.2001.12063225
Larsson E. Larsson K.H. Phylogenetic relationships of russuloid basidiomycetes with emphasis on aphyllophoralean taxa Mycologia 2003 95 1037 1065 10.1080/15572536.2004.11833020
Telleria M. Dueñas M. Melo I. Beltrán-Tejera E. Rodríguez-Armas J. Salcedo I. Martín M. Gloeocystidiellum kenyense in Azores and Madeira Mycotaxon 2012 119 337 343 10.5248/119.337
Miller S. Larsson E. Larsson K. Verbeken A. Nuytinck J. Perspectives in the new Russulales Mycologia 2006 98 960 970 10.1080/15572536.2006.11832625
Nilsson R. Kristiansson E. Ryberg M. Hallenberg N. Larsson K. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification Evol. Bioinform. 2008 4 193 201 10.4137/EBO.S653
Shah C. Baral R. Bartaula B. Shrestha L. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance BMC Microbiol. 2019 19 204 10.1186/s12866-019-1587-3 31477018
Miranda-Estrada L. Ruíz-Rosas M. Molina-López J. Parra-Rojas I. González-Villalobos E. Castro-Alarcón N. Relationship between virulence factors, resistance to antibiotics and phylogenetic groups of uropathogenic Escherichia coli in two locations in Mexico Enferm. Infecc. Microbiol. Clin. 2017 35 426 433 10.1016/j.eimc.2016.02.021 27048964
Iguchi A. Nagaya Y. Pradel E. Ooka T. Ogura Y. Katsura K. Kurokawa K. Oshima K. Hattori M. Parkhill J. et al. Genome evolution and plasticity of Serratia marcescens, an important multidrug-resistant nosocomial pathogen Genome Biol. Evol. 2014 6 2096 2110 10.1093/gbe/evu160 25070509
Suay I. Arenal F. Asensio F.J. Basilio A. Angeles Cabello M. Teresa Díez M. García J.B. González del Val A. Gorrochategui J. Hernández P. et al. Screening of basidiomycetes for antimicrobial activities Antonie Van Leeuwenhoek 2000 78 129 140 10.1023/A:1026552024021
Rosa L. Machado K. Jacob C. Capelari M. Rosa C. Zani C. Screening of Brazilian basidiomycetes for antimicrobial activity Memórias Instituto Oswaldo Cruz 2003 98 967 974 10.1590/S0074-02762003000700019
Kohler A. Kuo A. Nagy L.G. Morin E. Barry K.W. Buscot F. Canbäck B. Choi C. Cichocki N. Clum A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists Nat. Genet. 2015 47 410 415 10.1038/ng.3223
Barros L. Calhelha R. Vaz J. Ferreira I. Baptista P. Estevinho L. Antimicrobial activity and bioactive compounds of Portuguese wild edible mushrooms methanolic extracts Eur. Food Res. Technol. 2006 225 151 156 10.1007/s00217-006-0394-x
Jørgensen P.M. León-Yánez S. Catalogue of the vascular plants of Ecuador Monogr. Syst. Bot. Mo. Bot. Gard. 1999 75 1 1182 0915279606
Megadiverse Countries Definition Biodiversity A-Z Available online: https://www.biodiversitya-z.org/content/megadiverse-countries (accessed on 17 September 2022)
Hawksworth D. Lücking R. Fungal diversity revisited: 2.2 to 3.8 million species Fungal Kingd. 2017 5 79 95 10.1128/microbiolspec.FUNK-0052-2016
