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Novel therapeutic agents from the bacterial symbionts of Brazilian invertebrates

Grant number: 13/50954-0
Support Opportunities:BIOTA-FAPESP Program - Thematic Grants
Duration: July 01, 2014 - September 30, 2020
Field of knowledge:Biological Sciences - Microbiology - Organic Chemistry
Convênio/Acordo: John E. Fogarty International Center (FIC/NIH)
Principal Investigator:Mônica Tallarico Pupo
Grantee:Mônica Tallarico Pupo
Principal researcher abroad: Jon Clardy
Institution abroad: Harvard University, Cambridge, United States
Host Institution: Faculdade de Ciências Farmacêuticas de Ribeirão Preto (FCFRP). Universidade de São Paulo (USP). Ribeirão Preto , SP, Brazil
Pesquisadores principais:
Adriano Defini Andricopulo
Associated grant(s):16/50492-5 - Metabolic processes in the cooperative microbial symbionts of Brazilian membracids, AP.R SPRINT
Associated scholarship(s):19/16559-3 - Biosynthetic studies of bioactive macrolactone polyketide from Streptomyces sp. ICBG311, BP.MS
19/19099-3 - Genomic analysis of antibiotic-producing Pseudonocardia associated with Attini ants, BP.TT
18/17502-2 - Natural products involved in the symbiosis between Amycolatopsis and attine ants, BP.MS
+ associated scholarships 18/03650-0 - Analysis of steroids produced by symbiotic fungi isolated from the stingless bees' rearing cell, BP.MS
18/19128-0 - Isolation, preservation and cultivation of microbial strains associated with social insects, BP.TT
18/03747-3 - Analysis of natural products involved in the interactions between Pseudonocardia and Escovopsis associated with Trachymyrmex ants using molecular networking, BP.MS
17/01188-4 - Relationship of the protozoan Crithidia spp with bacterioma associated with the stingless bee Melipona scutellaris: chemical, ecological and pharmacological studies, BP.PD
16/15872-1 - Identification of natural antiparasitic products produced by insect–bacterial symbiosis, BP.PD
15/16415-0 - Metabolic potential of fungus-garden microbiomes of Attini ants, BP.MS
15/04901-8 - Natural products from microorganisms associated with stingless bees: chemical, ecological and pharmacological studies, BP.DD
15/01001-6 - Discovering bacterial symbionts diversity associated with ants in different Brazilian biomes, BP.PD
15/01272-0 - Microbial strains: preservation, cultivation, extracts preparation, antibiotic screening and chemical profiling of extracts, BP.TT
14/14095-6 - Bacterial symbionts isolated from fungus-growing ants collected in remaining hotspots of biodiversity in São Paulo State as sources of antiparasitic compounds, BP.DD - associated scholarships


An International Cooperative Biodiversity Group (ICBG) with an interdisciplinary leadership team of physicians, pharmacologists, evolutionary biologists, and chemists will discover and develop therapeutic agents produced by Brazilian symbiotic bacteria. The team will target three therapeutic areas: 1) infectious fungal pathogens, 2) Chagas disease and leishmaniasis, and 3), cancers of the blood-all three of which represent major threats to human health that need to be addressed with new therapeutic agents. This ICBG has focused screening platforms for all three diseases that will perform all the required steps from primary screens through in vivo mouse model studies. The ICBG will focus on identifying useful natural products from bacterial symbionts of social insects in Brazil, such as fungus-growing ants. Fungus-growing ants have specialized bacterial symbionts that provide chemical defenses against pathogenic fungi that threaten their communities. The ecological role of the bacterially produced chemical defenses - killing pathogenic fungi but sparing the fungal gardens and the ' insect host - matches the therapeutic requirements for antifungal, anticancer, and antiprotozoal agents. Our discovery efforts will make extensive use of cutting-edge technology and genomic approaches. Bacteria will be micro-cultured for high-throughput primary phenotypic screens, and priority strains will be re-cultured for secondary screens and dereplication. All bacterial strains will be genotyped (16S), and strains advancing along pipelines will have their genomes sequenced and subjected to bioinformatic analysis. In addition, the ICBG will undertake major efforts to catalog Brazil's microbial diversity, train Brazilian scientists, and support the development of drug discovery in the country. (AU)

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Scientific publications (30)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
BRUNETTI, ANDRES E.; BUNK, BOYKE; LYRA, MARIANA L.; FUZO, CARLOS A.; MARANI, MARIELA M.; SPROEER, CATHRIN; HADDAD, CELIO F. B.; LOPES, NORBERTO P.; OVERMANN, JOERG. olecular basis of a bacterial-amphibian symbiosis revealed by comparative genomics, modeling, and functional testin. ISME Journal, v. 16, n. 3, . (20/02207-5, 13/50954-0, 17/26162-8, 17/23725-1, 14/20915-6)
FUKUDA, TAISE T. H.; HELFRICH, ERIC J. N.; MEYERS, EMILY; MELO, WEILAN G. P.; VAN ARNAM, ETHAN B.; ANDES, DAVID R.; CURRIE, CAMERON R.; PUPO, MONICA T.; CLARDY, JON. Specialized Metabolites Reveal Evolutionary History and Geographic Dispersion of a Multilateral Symbiosis. ACS CENTRAL SCIENCE, v. 7, n. 2, p. 292-299, . (17/17305-0, 15/26349-5, 15/01001-6, 13/50954-0)
BAE, MUNHYUNG; MEVERS, EMILY; PISHCHANY, GLEB; WHALEY, SARAH G.; ROCK, CHARLES O.; ANDES, DAVID R.; CURRIE, CAMERON R.; PUPO, MONICA T.; CLARDY, JON. Chemical Exchanges between Multilateral Symbionts. ORGANIC LETTERS, v. 23, n. 5, p. 1648-1652, . (13/50954-0)
MENEGATTI, CARLA; FUKUDA, TAISE T. H.; PUPO, MONICA T.. Chemical Ecology in Insect-microbe Interactions in the Neotropics. Planta Medica, v. 87, n. 01/02, p. 38-48, . (16/15576-3, 13/07600-3, 13/50954-0, 15/26349-5)
BATISTA, JULIANA H.; LEAL, FERNANDA C.; FUKUDA, TAISE T. H.; ALCOFORADO DINIZ, JULIANA; ALMEIDA, FAUSTO; PUPO, MONICA T.; DA SILVA NETO, JOSE F.. Interplay between two quorum sensing-regulated pathways, violacein biosynthesis and VacJ/Yrb, dictates outer membrane vesicle biogenesis in Chromobacterium violaceum. ENVIRONMENTAL MICROBIOLOGY, v. 22, n. 6, . (18/01388-6, 18/25445-9, 13/50954-0, 15/26349-5)
BRUNETTI, ANDRES E.; LYRA, MARIANA L.; MELO, WEILAN G. P.; ANDRADE, LAURA E.; PALACIOS-RODRIGUEZ, PABLO; PRADO, BARBARA M.; HADDAD, CELIO F. B.; PUPO, MONICA T.; LOPES, NORBERTO P.. Symbiotic skin bacteria as a source for sex-specific scents in frogs. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, v. 116, n. 6, p. 2124-2129, . (17/23725-1, 14/20915-6, 13/50741-7, 17/26162-8, 13/50954-0, 14/50265-3, 15/01001-6)
LI, HONGJIE; SOSA-CALVO, JEFFREY; HORN, HEIDI A.; PUPO, MONICA T.; CLARDY, JON; RABELING, CHRISTIAN; SCHULTZ, TED R.; CURRIE, CAMERON R.. Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, v. 115, n. 42, p. 10720-10725, . (13/50954-0)
RODRIGUEZ-HERNANDEZ, DIEGO; MELO, WEILAN G. P.; MENEGATTI, CARLA; LOURENZON, VITOR B.; DO NASCIMENTO, FABIO S.; PUPO, MONICA T.. Actinobacteria associated with stingless bees biosynthesize bioactive polyketides against bacterial pathogens. NEW JOURNAL OF CHEMISTRY, v. 43, n. 25, p. 10109-10117, . (17/01188-4, 13/50954-0, 14/17620-4, 16/15576-3, 15/01001-6, 18/07153-0)
ORTEGA, HUMBERTO E.; BATISTA, JR., JOAO M.; MELO, WEILAN G. P.; DE PAULA, GABRIELA T.; PUPO, MONICA T.. Structure and Absolute Configuration of Secondary Metabolites from Two Strains of Streptomyces chartreusis Associated with Attine Ants. Journal of the Brazilian Chemical Society, v. 30, n. 12, SI, p. 2672-2680, . (15/07089-2, 13/50954-0, 14/25222-9, 14/14095-6, 17/05920-1, 15/01001-6)
ORTEGA, HUMBERTO E.; FERREIRA, LEONARDO L. G.; MELO, WEILAN G. P.; OLIVEIRA, ANA LIGIA L.; RAMOS ALVARENGA, RENE F.; LOPES, NORBERTO P.; BUGNI, TIM S.; ANDRICOPULO, ADRIANO D.; PUPO, MONICA T.. Antifungal compounds from Streptomyces associated with attine ants also inhibit Leishmania donovani. PLoS Neglected Tropical Diseases, v. 13, n. 8, . (13/07600-3, 13/50954-0, 15/01001-6, 14/14095-6, 16/15872-1, 16/20154-0)
PUPO, MONICA T.; CURRIE, CAMERON R.; CLARDY, JON. Microbial Symbionts of Insects are the Focus of the First International Cooperative Biodiversity Group (ICBG) in Brazil. Journal of the Brazilian Chemical Society, v. 28, n. 3, SI, p. 393-401, . (13/50954-0)
CHAGAS, FERNANDA OLIVEIRA; PESSOTTI, RITA DE CASSIA; CARABALLO-RODRIGUEZ, ANDRES MAURICIO; PUPO, MONICA TALLARICO. Chemical signaling involved in plant-microbe interactions. CHEMICAL SOCIETY REVIEWS, v. 47, n. 5, p. 1652-1704, . (11/12910-6, 08/09540-0, 13/07600-3, 13/50954-0, 12/21803-1)
CHEVRETTE, MARC G.; CARLSON, CAITLIN M.; ORTEGA, HUMBERTO E.; THOMAS, CHRIS; ANANIEV, GENE E.; BARNS, KENNETH J.; BOOK, ADAM J.; CAGNAZZO, JULIAN; CARLOS, CAMILA; FLANIGAN, WILL; et al. The antimicrobial potential of Streptomyces from insect microbiomes. NATURE COMMUNICATIONS, v. 10, . (14/14095-6, 15/01001-6, 13/50954-0)
BARCOTO, MARIANA O.; CARLOS-SHANLEY, CAMILA; FAN, HUAN; FERRO, MILENE; NAGAMOTO, NILSON S.; BACCI, JR., MAURICIO; CURRIE, CAMERON R.; RODRIGUES, ANDRE. Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment. SCIENTIFIC REPORTS, v. 10, n. 1, . (12/25299-6, 15/16415-0, 19/03746-0, 16/02767-5, 13/50954-0, 17/04824-9)
CHAGAS, FERNANDA O.; RUZZINI, ANTONIO C.; BACHA, V, LARISSA; SAMBORSKYY, MARKYIAN; CONTI, RAPHAEL; PESSOTTI, RITA C.; DE OLIVEIRA, LUCIANA G.; CLARDY, JON; PUPO, MONICA T.. Genome Sequence of Streptomyces sp. Strain RTd22, an Endophyte of the Mexican Sunflower. MICROBIOLOGY RESOURCE ANNOUNCEMENTS, v. 4, n. 4, . (13/07600-3, 08/09540-0, 13/50954-0, 09/17695-6, 08/00812-7, 11/06209-3, 11/12910-6, 11/11703-7)
PALUDO, CAMILA R.; MENEZES, CRISTIANO; SILVA-JUNIOR, EDUARDO A.; VOLLET-NETO, AYRTON; ANDRADE-DOMINGUEZ, ANDRES; PISHCHANY, GLEB; KHADEMPOUR, LILY; DO NASCIMENTO, FABIO S.; CURRIE, CAMERON R.; KOLTER, ROBERTO; et al. Stingless Bee Larvae Require Fungal Steroid to Pupate. SCIENTIFIC REPORTS, v. 8, . (12/22487-6, 12/24204-1, 13/07600-3, 13/50954-0, 13/04092-7, 14/23532-0)
SILVA-JUNIOR, EDUARDO A.; RUZZINI, ANTONIO C.; PALUDO, CAMILA R.; NASCIMENTO, FABIO S.; CURRIE, CAMERON R.; CLARDY, JON; PUPO, MONICA T.. Pyrazines from bacteria and ants: convergent chemistry within an ecological niche. SCIENTIFIC REPORTS, v. 8, . (12/22487-6, 12/24204-1, 15/25301-9, 14/24330-2, 13/50954-0, 13/04092-7)
DA SILVA-JUNIOR, EDUARDO AFONSO; PALUDO, CAMILA RAQUEL; VALADARES, LOHAN; LOPES, NORBERTO PEPORINE; DO NASCIMENTO, FABIO SANTOS; PUPO, MONICA TALLARICO. Aflatoxins produced by Aspergillus nomius ASR3, a pathogen isolated from the leaf-cutter ant Atta sexdens rubropilosa. REVISTA BRASILEIRA DE FARMACOGNOSIA-BRAZILIAN JOURNAL OF PHARMACOGNOSY, v. 27, n. 4, p. 529-532, . (12/24204-1, 13/50954-0, 13/04092-7, 12/22487-6)
ORTEGA, HUMBERTO E.; BATISTA, JR., JOAO M.; MELO, WEILAN G. P.; CLARDY, JON; PUPO, MONICA T.. Absolute configurations of griseorhodins A and C. Tetrahedron Letters, v. 58, n. 50, p. 4721-4723, . (15/07089-2, 14/25222-9, 15/01001-6, 13/50954-0)
PALUDO, CAMILA R.; RUZZINI, EANTONIO C.; SILVA-JUNIOR, EDUARDO A.; PISHCHANY, GLEB; CURRIE, CAMERON R.; NASCIMENTO, FABIO S.; KOLTER, ROBERTO G.; CLARDY, JON; PUPO, MONICA T.. Whole-Genome Sequence of Bacillus sp. SDLI1, Isolated from the Social Bee Scaptotrigona depilis. MICROBIOLOGY RESOURCE ANNOUNCEMENTS, v. 4, n. 2, . (12/22487-6, 12/24204-1, 13/07600-3, 13/50954-0, 13/04092-7, 14/23532-0)
RIES, LAURE N. A.; PARDESHI, LAKHANSING; DONG, ZHICLIANG; TAN, KAELING; STEENWYK, JACOB L.; COLABARDINI, ANA CRISTINA; FERREIRA FILHO, JAIRE A.; DE CASTRO, PATRICIA A.; SILVA, LILIAN P.; PREITE, NYCOLAS W.; et al. The Aspergillus fumigatus transcription factor RglT is important for gliotoxin biosynthesis and self-protection, and virulence. PLOS PATHOGENS, v. 16, n. 7, . (17/14159-2, 17/21983-3, 18/25217-6, 17/07536-4, 17/01188-4, 13/50954-0, 14/00789-6, 13/07937-8, 16/07870-9, 19/09278-8, 16/03322-7)
MENEGATTI, CARLA; DA PAIXAO MELO, WEILAN GOMES; CARRAO, DANIEL BLASCKE; MORAES DE OLIVEIRA, ANDERSON RODRIGO; DO NASCIMENTO, FABIO SANTOS; LOPES, NORBERTO PEPORINE; PUPO, MONICA TALLARICO. Paenibacillus polymyxa Associated with the Stingless Bee Melipona scutellaris Produces Antimicrobial Compounds against Entomopathogens. Journal of Chemical Ecology, v. 44, n. 12, p. 1158-1169, . (09/54098-6, 14/17620-4, 13/50954-0, 14/50265-3, 15/01001-6)
ORTEGA, HUMBERTO E.; LOURENZON, VITOR B.; CHEVRETTE, MARC G.; FERREIRA, LEONARDO L. G.; ALVARENGA, RENE F. RAMOS; MELO, WEILAN G. P.; VENANCIO, TIAGO; CURRIE, CAMERON R.; ANDRICOPULO, ADRIANO D.; BUGNI, TIM S.; et al. Antileishmanial macrolides from ant-associated Streptomyces sp. ISID311. Bioorganic & Medicinal Chemistry, v. 32, . (13/25658-9, 16/17614-0, 14/14095-6, 13/50954-0, 19/16559-3, 13/07600-3, 16/20154-0)
FUKUDA, TAISE T. H.; PEREIRA, CAMILA F.; MELO, WEILAN G. P.; MENEGATTI, CARLA; ANDRADE, PAULO H. M.; GROPPO, MILTON; LACAVA, PAULO T.; CURRIE, CAMERON R.; PUPO, MONICA T.. Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis. FRONTIERS IN MICROBIOLOGY, v. 12, . (17/17305-0, 16/26230-0, 16/15576-3, 13/50954-0, 19/19099-3, 15/26349-5, 15/01001-6)
MENEGATTI, CARLA; LOURENZON, VITOR BRUNO; RODRIGUEZ-HERNANDEZ, DIEGO; DA PAIXAO MELO, WEILAN GOMES; GOMES FERREIRA, LEONARDO LUIZ; ANDRICOPULO, ADRIANO DEFINI; DO NASCIMENTO, FABIO SANTOS; PUPO, MONICA TALLARICO. Meliponamycins: Antimicrobials from Stingless Bee-Associated Streptomyces sp.. Journal of Natural Products, v. 83, n. 3, SI, p. 610-616, . (14/17620-4, 13/07600-3, 16/15576-3, 18/07153-0, 17/01188-4, 13/50954-0, 15/01001-6)
FUKUDA, TAISE T. H.; CASSILLY, CHELSI D.; GERDT, JOSEPH P.; HENKE, MATTHEW T.; HELFRICH, ERIC J. N.; MEVERS, EMILY. Research Tales from the Clardy Laboratory: Function-Driven Natural Product Discovery. Journal of Natural Products, v. 83, n. 3, SI, p. 744-755, . (15/26349-5, 13/50954-0)
BETANCUR, LUZ A.; FORERO, ABEL M.; VINCHIRA-VILLARRAGA, DIANA M.; CARDENAS, JUAN D.; ROMERO-OTERO, ADRIANA; CHAGAS, FERNANDA O.; PUPO, MONICA T.; CASTELLANOS, LEONARDO; RAMOS, FREDDY A.. NMR-based metabolic profiling to follow the production of anti- phytopathogenic compounds in the culture of the marine strain Streptomyces sp. PNM-9. MICROBIOLOGICAL RESEARCH, v. 239, . (13/50954-0)
DE PAULA, GABRIELA TONINATO; MENEZES, CRISTIANO; PUPO, MONICA TALLARICO; ROSA, CARLOS AUGUSTO. Stingless bees and microbial interactions. CURRENT OPINION IN INSECT SCIENCE, v. 44, p. 41-47, . (18/03650-0, 13/50954-0)
PALUDO, CAMILA RAQUEL; PISHCHANY, GLEB; ANDRADE-DOMINGUEZ, ANDRES; SILVA-JUNIOR, EDUARDO AFONSO; MENEZES, CRISTIANO; NASCIMENTO, FABIO SANTOS; CURRIE, CAMERON R.; KOLTER, ROBERTO; CLARDY, JON; PUPO, MONICA TALLARICO. Microbial community modulates growth of symbiotic fungus required for stingless bee metamorphosis. PLoS One, v. 14, n. 7, . (13/07600-3, 13/50954-0, 12/24204-1, 15/25301-9, 12/22487-6, 14/23532-0)
FRANCOEUR, CHARLOTTE B.; MAY, DANIEL S.; THAIRU, MARGARET W.; HOANG, DON Q.; PANTHOFER, OLIVIA; BUGNI, TIM S.; PUPO, MONICA T.; CLARDY, JON; PINTO-TOMAS, ADRIAN A.; CURRIE, CAMERON R.. Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis. Applied and Environmental Microbiology, v. 87, n. 14, . (13/50954-0)

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