Mechanism and color modulation of fungal bioluminescence

Study of fungal bioluminescence mechanisms generates development of a multicolor enzymatic chemiluminescence system. Bioluminescent fungi are spread throughout the globe, but details on their mechanism of light emission are still scarce. Usually, the process involves three key components: an oxidizable luciferin substrate, a luciferase enzyme, and a light emitter, typically oxidized luciferin, and called oxyluciferin. We report the structure of fungal oxyluciferin, investigate the mechanism of fungal bioluminescence, and describe the use of simple synthetic α-pyrones as luciferins to produce multicolor enzymatic chemiluminescence. A high-energy endoperoxide is proposed as an intermediate of the oxidation of the native luciferin to the oxyluciferin, which is a pyruvic acid adduct of caffeic acid. Luciferase promiscuity allows the use of simple α-pyrones as chemiluminescent substrates.

[1]  T. Wilson.  CHEMILUMINESCENCE FROM THE ENDOPEROXIDE OF 1,4‐DIMETHOXY‐9,10‐DIPHENYLANTHRACENE , 1969, Photochemistry and photobiology.

[2]  P. Di Mascio,et al.  Generation of cholesterol carboxyaldehyde by the reaction of singlet molecular oxygen [O2 (1Delta(g))] as well as ozone with cholesterol. , 2009, Chemical research in toxicology.

[3]  W. Robinson,et al.  Design, synthesis, and biological evaluation of novel hybrid dicaffeoyltartaric/diketo acid and tetrazole-substituted L-chicoric acid analogue inhibitors of human immunodeficiency virus type 1 integrase. , 2010, Journal of medicinal chemistry.

[4]  Cassius Vinicius Stevani,et al.  Evidence that a single bioluminescent system is shared by all known bioluminescent fungal lineages. , 2012, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[5]  M. J. Cormier,et al.  Primary structure of the Aequorea victoria green-fluorescent protein. , 1992, Gene.

[6]  Bioluminescent fungi from Peninsular Malaysia—a taxonomic and phylogenetic overview , 2014, Fungal Diversity.

[7]  S. E. Medvedeva,et al.  The Chemical Basis of Fungal Bioluminescence. , 2015, Angewandte Chemie.

[8]  E. Bechara,et al.  Dioxygen NIR FT-Emission (1Δ g → 3Σ− g ) and Raman Spectra of 1,4-Dimethylnaphthalene Endoperoxide: A Source of Singlet Molecular Oxygen , 1992 .

[9]  Jianghong Rao,et al.  Biosensing and imaging based on bioluminescence resonance energy transfer. , 2009, Current opinion in biotechnology.

[10]  K. Eidne,et al.  Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET) , 2006, Nature Methods.

[11]  G. Schuster.  Chemiluminescence of organic peroxides. Conversion of ground-state reactants to excited-state products by the chemically initiated electron-exchange luminescence mechanism , 1979 .

[12]  J. W. Hastings,et al.  Chemistries and colors of bioluminescent reactions: a review. , 1996, Gene.

[13]  R. Airth,et al.  The isolation of catalytic components required for cell-free fungal bioluminescence. , 1962, Archives of biochemistry and biophysics.

[14]  Dan S. Tawfik,et al.  Enzyme promiscuity: a mechanistic and evolutionary perspective. , 2010, Annual review of biochemistry.

[15]  E. Bechara.  Bioluminescence: A Fungal Nightlight with an Internal Timer , 2015, Current Biology.

[16]  C. R. Correia,et al.  Heck–Matsuda Arylation as a Strategy to Access Kavalactones Isolated from Polygala sabulosa, Piper methysticum, and Analogues , 2012 .

[17]  W. Baader,et al.  Chemiluminescence efficiency of catalyzed 1,2-dioxetanone decomposition determined by steric effects. , 2015, The Journal of organic chemistry.

[18]  W. Baader,et al.  Solvent cage effects: basis of a general mechanism for efficient chemiluminescence. , 2013, The Journal of organic chemistry.

[19]  Cassius Vinicius Stevani,et al.  Studies on the Mechanism of the Excitation Step in Peroxyoxalate Chemiluminescence , 2000 .

[20]  D. Reinhardt,et al.  From the firefly bioluminescence to the dioxetane-based (AMPPD) chemiluminescence immunoassay: a retroanalysis , 1996 .

[21]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[22]  A. Varvoglis,et al.  Preparation of [hydroxy(((+)-10-camphorsulfonyl)oxy)iodo]benzene and its reactivity toward carbonyl compounds , 1990 .

[23]  A. Becke,et al.  Density-functional exchange-energy approximation with correct asymptotic behavior. , 1988, Physical review. A, General physics.

[24]  R. Pérez-Ruíz,et al.  Steric Enhancement of the Chemiluminescence of Luminols. , 2015, Chemistry.

[25]  S. Hober,et al.  Pyrosequencing: history, biochemistry and future. , 2006, Clinica chimica acta; international journal of clinical chemistry.

[26]  R. Pleixats,et al.  Functionalization at C‐5 and at the C‐6 methyl group of 4‐methoxy‐6‐methyl‐2‐pyrone , 1982 .

[27]  Cassius Vinicius Stevani,et al.  Circadian Control Sheds Light on Fungal Bioluminescence , 2015, Current Biology.

[28]  W. Adam,et al.  Cyclic peroxides. 86. .alpha.-Pyrone endoperoxides. Synthesis, thermal decomposition, and chemiluminescence , 1979 .

[29]  J. W. Hastings,et al.  Bioluminescence: Living Lights, Lights for Living , 2013 .

[30]  Cassius Vinicius Stevani,et al.  Studies on the chemiexcitation step in peroxyoxalate chemiluminescence using steroid-substituted activators. , 2002, Luminescence : the journal of biological and chemical luminescence.

[31]  Anderson G. Oliveira,et al.  Bioluminescência de fungos: distribuição, função e mecanismo de emissão de luz , 2013 .

[32]  C. Cramer,et al.  Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. , 2009, The journal of physical chemistry. B.

[33]  W. Baader,et al.  Revision of singlet quantum yields in the catalyzed decomposition of cyclic peroxides. , 2012, The Journal of organic chemistry.

[34]  Cassius Vinicius Stevani,et al.  Neonothopanus gardneri: a new combination for a bioluminescent agaric from Brazil , 2011, Mycologia.

[35]  M. Grabolle,et al.  Relative and absolute determination of fluorescence quantum yields of transparent samples , 2013, Nature Protocols.