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Electronic chemiexcitation in biological systems: bioluminescence and photochemistry in the dark

Grant number: 17/22501-2
Support type:Research Projects - Thematic Grants
Duration: October 01, 2018 - September 30, 2023
Field of knowledge:Biological Sciences - Biophysics - Radiology and Photobiology
Principal researcher:Etelvino José Henriques Bechara
Grantee:Etelvino José Henriques Bechara
Home Institution: Instituto de Química (IQ). Universidade de São Paulo (USP). São Paulo , SP, Brazil
Pesquisadores principais:
Cassius Vinicius Stevani
Assoc. researchers:Anderson Garbuglio de Oliveira
Associated scholarship(s):20/04082-5 - Quenching of triplet acetone by alkylated sorbates, esterified or peptide derivatives, BP.IC
20/16000-3 - Functional characterization of candidate genes for the biological clock of Neonothopanus gardneri and its relationship with bioluminescence, BP.DD
19/26503-5 - Equisetumpyrone detection and characterization of H3H-like enzymes in plants, BP.IC
+ associated scholarships 19/26510-1 - Influence of light on growth and bioluminescence of the fungus Neonothopanus gardneri, BP.TT
19/24515-6 - Sources, targets and biological responses of triplet species and singlet oxygen: pathogenicity and quenching, BP.PD
19/21782-3 - Caffeic Acid Cycle (CAC) in fungal bioluminescence: luciferin antioxidant effect, oxyluciferin recycling and oxidative stress, BP.DD
19/12605-0 - Bioluminescence of Fungi, Millipede and Marine Organisms: Chemical and Biological Aspects, BP.PD
19/11458-4 - Generation of singlet oxygen by the oxidation of formylhydrazines found in fungi, BP.IC
19/01029-9 - Bioluminescent fungal cultures & ecological studies of the fungus-animal interaction, BP.TT
18/25842-8 - Sources, Targets and Biological Responses of Triplet Species and Singlet Oxygen: Pathogenicity and Quenching., BP.PD - associated scholarships

Abstract

Light, molecular oxygen, and free radicals are the essence of life... for the good and the evil. They provide energy and matter for living beings, but charge a high price - diseases, ageing, death -, via electron-transfer reactions and electronic photo- and chemiexcitation of molecules. Our project concerns these processes through the study of the molecular nature of living lights (bioluminescence, BL) and typical photochemical reactions that proceed in the absence of light when driven by electronically excited products ('photo'chemistry in the dark). Chemical mechanisms, biological functions and technological uses of BL fungi and marine animals will be investigated. In the BL field, we plan to elucidate the luciferin/luciferase systems, biological functions, ecological role, phylogeny, and details of mechanisms of light emission. Preliminary data point to complex coadjuvant enzymes and co-factors like hydroxylase and NAD(P)H in fungi, photoprotein and Fe(II) in the worm-like species. Phylogenetic connections among North-American, Asian, and Brazilian fungus species will be identified. Interestingly, all fungi use the polyphenol hispidin as the luciferin (3-hydroxyhispidin) precursor, which also occurs in ferns like horsetail (Equisetum sp.). BL inhibitors and activators can be harnessed to develop analytical tools for biological samples and imaging modified organisms. The puzzling occurrence of typical photoproducts in vegetal and animal tissues not exposed to light, and the detection of weakly emissive excited products (e.g., triplet carbonyls and singlet oxygen) in peroxidase-catalyzed reactions and lipoperoxidations, prompted Cilento and White to advance the "photo(bio)chemistry in the dark" theory. Triplet carbonyls are long-lived and display diradical behavior, thereby can travel across cell sites, hit diverse targets, cause chemical damage, and trigger biological responses. Among our interests are chemical damage to hemeproteins like horseradish peroxidase (HRP), cytochrome c, myoglobin, and hemoglobin when acting as peroxidases on substrates capable of generating triplet carbonyls. Methylated and long chain linear sorbate esters and peptide-derivatives (cell-penetrating peptides) will be tested as triplet quenchers in vitro and in cell cultures. Accordingly, ethyl sorbate blocks the formation of DNA pyrimidine dimers to a significant extent long after UV irradiation of melanin-rich melanocyte cultures as we have previously reported. On the other hand, we predict production of singlet oxygen and toxic aldehydes initiated by peroxynitrite Michael addition to acrolein, an air and fried food contaminant implicated in ageing-related diseases. Another probable source of singlet oxygen to be studied are formylhydrazine derivatives - potentially lethal toxins found in the mushroom genus Gyromitra - under oxidation by peroxynitrite or HRP/H2O2. The rationale underlying the latter two proposals is the intermediacy of geminal hydrogen atom-bearing vinylperoxyl and formylperoxyl radicals, the necessary condition for the singlet oxygen-generating Russell reaction. Singlet oxygen oxidizes fatty acids, proteins and DNA leading to adverse and, paradoxically, beneficial cell signaling responses. Our project will accumulate knowledge underlying the chemiexcitation field and analytical tools, and will foster international collaborations. (AU)

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Scientific publications (14)
(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)
RAMOS, LUIZ D.; MANTOVANI, MARIANA C.; SARTORI, ADRIANO; DUTRA, FERNANDO; STEVANI, CASSIUS V.; BECHARA, ETELVINO J. H.. Aerobic co-oxidation of hemoglobin and aminoacetone, a putative source of methylglyoxal. Free Radical Biology and Medicine, v. 166, p. 178-186, . (19/24515-6, 17/22501-2)
CALDAS, LHAIS A.; SOARES, DOUGLAS M. M.; MENOLLI, NELSON JR JR; STEVANI, V, CASSIUS; SARTORELLI, PATRICIA. etabolomics of the wild mushroom Gymnopilus imperialis (Agaricomycetes, Basidiomycota) by UHPLC-HRMS/MS analysis and molecular networ. FUNGAL BIOLOGY, v. 126, n. 2, p. 132-138, . (18/15677-0, 17/22501-2, 16/24985-4, 19/12605-0, 18/25646-4)
VIEIRA JUNIOR, WAGNER GONCALVES; CENTEIO CARDOSO, ROSSANA VEVIANA; FERNANDES, ANGELA; FERNANDES RODRIGUES FERREIRA, ISABEL CRISTINA; BARROS, LILLIAN; PARDO-GIMENEZ, ARTURO; MENDEL SOARES, DOUGLAS MORAES; STEVANI, CASSIUS VINICIUS; ZIED, DIEGO CUNHA. nfluence of strains and environmental cultivation conditions on the bioconversion of ergosterol and vitamin D-2 in the sun mushroo. Journal of the Science of Food and Agriculture, v. 102, n. 4, . (18/21492-2, 17/22501-2, 19/00419-8, 19/12605-0)
RAMOS, LUIZ D.; PRADO, FERNANDA M.; STEVANI, V, CASSIUS; DI MASCIO, PAOLO; BECHARA, ETELVINO J. H.. l-Tryptophan Interactions with the Horseradish Peroxidase-Catalyzed Generation of Triplet Acetone. Photochemistry and Photobiology, v. 97, n. 2, . (17/22501-2, 12/12663-1, 13/07937-8, 19/24515-6)
SOARES, DOUGLAS M. M.; ATUM, SAMIR V. F.; BECHARA, ETELVINO J. H.; SETUBAL, JOAO C.; STEVANI, CASSIUS V.; FREIRE, RENATO S.. Exploring the Microbiota of the Guarapiranga Water Reservoir With Long-Read Sequencing Technology. FRONTIERS IN MARINE SCIENCE, v. 8, . (19/12605-0, 17/22501-2)
RAFAELA LOPES FALASCHI; GRANT A. JOHNSON; CASSIUS VINICIUS STEVANI. The new species Neoceroplatus betaryiensis nov. sp. (Diptera: Keroplatidae) from Neotropical Region. Papéis Avulsos de Zoologia (São Paulo), v. 59, . (17/22501-2, 13/16885-1)
GALEAZZO, GABRIELA A.; MIRZA, JEREMY D.; DORR, FELIPE A.; PINTO, ERNANI; STEVANI, V, CASSIUS; LOHRMANN, KARIN B.; OLIVEIRA, ANDERSON G.. Characterizing the Bioluminescence of the Humboldt Squid, Dosidicus gigas (d'Orbigny, 1835): One of the Largest Luminescent Animals in the World. Photochemistry and Photobiology, v. 95, n. 5, p. 1179-1185, . (17/26279-2, 14/18541-0, 17/22501-2, 17/07677-7)
GONCALVES, LETICIA C. P.; MASSARI, JULIO; LICCIARDI, SAYMON; PRADO, FERNANDA M.; LINARES, EDLAINE; KLASSEN, ALINE; TAVARES, MARINA F. M.; AUGUSTO, OHARA; DI MASCIO, PAOLO; BECHARA, ETELVINO J. H.. Singlet oxygen generation by the reaction of acrolein with peroxynitrite via a 2-hydroxyvinyl radical intermediate. Free Radical Biology and Medicine, v. 152, p. 83-90, . (18/25842-8, 12/12663-1, 13/07937-8, 17/27059-6, 17/22501-2)
FALASCHI, RAFAELA L.; AMARAL, DANILO T.; SANTOS, ISAIAS; DOMINGOS, ADAO H. R.; JOHNSON, GRANT A.; MARTINS, ANA G. S.; VIROOMAL, IMRAN B.; POMPEIA, SERGIO L.; MIRZA, JEREMY D.; OLIVEIRA, ANDERSON G.; et al. Neoceroplatus betaryiensis nov. sp. (Diptera: Keroplatidae) is the first record of a bioluminescent fungus-gnat in South America. SCIENTIFIC REPORTS, v. 9, . (10/05426-8, 17/22501-2, 13/16885-1)
MORAES, V, GABRIELA; HANNON, MARY COLLEEN; SOARES, DOUGLAS M. M.; STEVANI, V, CASSIUS; SCHULZE, ANJA; OLIVEIRA, ANDERSON G.. Bioluminescence in Polynoid Scale Worms (Annelida: Polynoidae). FRONTIERS IN MARINE SCIENCE, v. 8, . (20/07600-7, 18/22304-5, 17/22501-2, 19/12605-0, 19/25086-1)
VENTURA, FERNANDA F.; MENDES, LUIZ F.; OLIVEIRA, ANDERSON G.; BAZITO, REINALDO C.; BECHARA, ETELVINO J. H.; FREIRE, RENATO S.; STEVANI, V, CASSIUS. Evaluation of Phenolic Compound Toxicity Using a Bioluminescent Assay with the Fungus Gerronema viridilucens. Environmental Toxicology and Chemistry, v. 39, n. 8, . (17/22501-2, 13/16885-1)
ZIED, DIEGO C.; VIEIRA JUNIOR, WAGNER G.; SOARES, DOUGLAS M. M.; STEVANI, V, CASSIUS; DIAS, EUSTAQUIO S.; IOSSI, MATHEUS R.; PARDO-GIMENEZ, ARTURO. Overview of four Agaricus subrufescens strains used in the last 15 years in Brazil and other countries and current potential materials for the future. MYCOLOGICAL PROGRESS, v. 20, n. 8, p. 953-966, . (17/22501-2, 18/21492-2)
NOBREGA, BIANCA B.; SOARES, DOUGLAS M. M.; ZAMUNER, CAIO K.; STEVANI, V, CASSIUS. Optimized methodology for obtention of high-yield and-quality RNA from the mycelium of the bioluminescent fungus Neonothopanus gardneri. Journal of Microbiological Methods, v. 191, . (20/16000-3, 19/12605-0, 19/21782-3, 17/22501-2)
MIRZA, JEREMY D.; MIGOTTO, ALVARO E.; YAMPOLSKY, ILIA V.; DE MORAES, GABRIELA V.; TSARKOVA, ALEKSANDRA S.; OLIVEIRA, ANDERSON G.. Chaetopterus variopedatusBioluminescence: A Review of Light Emission within a Species Complex. Photochemistry and Photobiology, v. 96, n. 4, p. 768-778, . (17/26279-2, 14/18541-0, 18/17857-5, 17/22501-2)

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