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Bioluminescent System of Luminous Fungus Mycena Lux-Coeli

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Bioluminescent System of Luminous Fungus Mycena Lux-Coeli Mushroom Science and Biotechnology, Vol. 27(2) 61-66, 2019 Copyright © 2019, Japanese Society of Mushroom Science and Biotechnology 61 Regular Paper Bioluminescent system of luminous fungus Mycena lux-coeli Katsunori TERANISHI Graduate School of Bioresources, Mie University, 1577 Kurimamachiya, Tsu, Mie 514-8507, Japan （Received 20 May 2019 / Accepted 2 July 2019） Abstract Bioluminescence is of chemical, biological and ecological interest. Currently, greater than 80 fungal bioluminescent species have been documented. The chemical mechanisms of Mycena lux-coeli biolumines- cence are still not clear. In this study, a bioluminescent system was identified in M. lux-coeli pileus gills. Bioluminescence in living gills was induced by addition of trans-3-hydroxyhispidin (1), and the induced bioluminescence exhibited a lmax of 525 nm, which was in agreement with that of natural bioluminescence. The light-producing enzyme from 1 was partially purified from M. lux-coeli gills. Trans-3-hydroxyhispidin- induced bioluminescence and natural bioluminescence were not affected by the addition of trans-3-hydroxy- hispidin analogue 2, which did not contain a hydroxyl group at the C-3 position of the phenyl group in 1, but were significantly inhibited by the addition of trans-3-hydroxyhispidin analogue 3, which did not contain two hydroxyl groups at the C-3 and C-4 positions of the phenyl group in 1. The characteristics of 1-induced bioluminescence were consistent with those of natural bioluminescence. This study concluded that 1 is a bioluminescent substrate for the natural bioluminescence of M. lux-coeli. Key words: Bioluminescence, Chemiluminescence, Fungus, Mycena lux-coeli, Trans-3-hydroxyhispidin in luminous fungi, but it has not yet been demonstrated Introduction that 1 is the luciferin in natural bioluminescence. In 2017, ‘Bioluminescence’, referring to the production and Kaskova et al. reported an in vitro chemiluminescence emission of light by living organisms, occurs sporadically study on an energy excitation mechanism via the oxida- in organisms1) and has been a target of scientific tion of 1 using water-insoluble luciferase partially purified study by several scientists for decades2). More than 80 from Neonothopanus gardneri or N. nambi and found that 1 bioluminescent species have been documented as of is converted into a light emitter (oxyluciferin) via a high- 2016 in the Kingdom Fungi3). In 1959 － 1962, Airth et energy endoperoxide intermediate (Fig. 1)9). Recently, al. have examined NAD(P)H-dependent luminescence Kotlobay et al. reported the genes responsible for the 1-de- using cold- and hot-water extracts obtained from the pendent luminescence enzymes of some bioluminescent mycelia of a bioluminescent fungus Armillaria mellea fungi, including N. nambi, N. gardneri, Armillaria mellea, and suggested that a bioluminescent substrate (luciferin), and Mycena citricolor10). Their report indicates that these a water-soluble enzyme, a water-insoluble enzyme bioluminescent fungi possess 1-dependent luminescence (luciferase), molecular oxygen, and NAD(P)H are required systems and does not prove that 1 is luciferin in natural for light production4-6). However, after this study, useful bioluminescence. Then, when 1 is a substrate for in vitro results related to luciferin and luciferase have not been chemiluminescence, it has to be evaluated whether this reported for half a century, possibly because of the compound is a substrate for natural bioluminescence. instability and trace levels of the components involved in Mycena lux-coeli is a bioluminescent fungal species light production. In 2012, Oliveira et al. examined in vitro that is distributed in the warm regions of Japan, and chemiluminescence using cold and hot aqueous extracts its fruiting bodies can mainly be found on decaying from some bioluminescent fungi tissue and reported Castanopsis sieboldii trees in June or September11). In that all known bioluminescent fungal lineages share the nature, its pileus gills continuously emit green light, which luciferin-luciferase reaction shown by Airth’s group, while can be easily observed by the naked eye in the dark, for specific luciferin and luciferase were not indicated7). In 2 days at ～25℃ (Fig. 2). Chemical studies related to the 2015, Purtov et al. reported chemiluminescence (not chemical mechanisms underlying the bioluminescence bioluminescence) is produced via the reaction between of M. lux-coeli have not been reported. In this study, trans-3-hydroxyhispidin (1) as a chemiluminescent sub- the bioluminescent system of M. lux-coeli pileus gills is strate and molecular oxygen in the presence of a water- reported. insoluble enzyme prepared from bioluminescent mycelia Materials and Methods of Neonothopanus nambi (Fig. 1)8). This is the first study to indicate a ‘candidate’ for the bioluminescent system 1. Fruiting bodies Fruiting bodies of M. lux-coeli were collected from decaying Castanopsis. sieboldii trees in the forest of *Corresponding author. E-mail: [email protected] Owase, Mie, Japan, from June 2015 － 2018. The gills 62 Vol.27 No. 2 Fig. 1. Chemical mechanism of fungal bioluminescence reported by Purtov et al.8) and Kaskova et al.9) and chemical structures of 2 and 3. were carefully disconnected from the fresh pileus for use Fig. 2. Bioluminescence of fresh fruiting body of Mycena lux-coeli. Left in experiments. and right photographs were recorded under white light and in the 2. Chemicals dark, respectively. The right photograph was recorded using a digital camera in the dark at 20℃ and － 70% relative humidity, Trans-3-hydroxyhispidin (1), its analogues 2 and 3 with settings of ISO 1600; f2.8; and 6-s exposure time. (new compound), and oxyluciferin 4 were chemically synthesized according to a previously reported method9). many), and the spots were visualized with a UV lamp (254 Solutions of these compounds in 10 mM phosphate buffer nm). Preparative chromatography was performed on BW- (pH 7.0) were used. 6 － 10% Mg(OMe)2 in MeOH and BBr3 200 silica gel columns (Fuji Silysia, Aichi, Japan). in CH2Cl2 were purchased from Sigma Aldrich Co. (St. 4. Chemical synthesis of 3 Louis, MO, USA). Other chemicals were purchased from A mixture of benzaldehyde (0.19 g, 1.79 mmol), Wako Pure Chemical Industries Ltd. (Osaka, Japan). 3,4-dimethoxy-6-methyl-2H-pyran-2-one (0.2 g,1.18 9) 3. General experimental procedures for chemical synthesis mmol) and 6 － 10% Mg(OCH3)2 in CH3OH (10 mL) was Melting points were determined using an ASONE stirred 64 h at 25℃. Aqueous 1 mol/L HCl (20 mL) ATM-01 apparatus and were uncorrected. IR data were was added to the resulting mixture and diluted with obtained using an FT/IR 410 spectrometer (JASCO Corp., water (30 mL) and CH2Cl2 (50 mL) and the solution was Tokyo, Japan). UV−vis spectra were obtained with a V-530 extracted with CH2Cl2. The CH2Cl2 layers were dried 1 13 DS spectrometer (JASCO Corp.). H and C NMR spectra with anhydrous Na2SO4 and evaporated under reduced were measured at 20℃ on a JNM-A500 spectrometer pressure. The resulting residue was adsorbed on a silica 1 (JEOL, Tokyo, Japan) operating at 500 MHz for H NMR gel column in CH2Cl2 and eluted with the same solvent. and 125 MHz for 13C NMR. TMS was used as the internal The eluent was evaporated under reduced pressure and standards for DMSO-d6. Chemical shift values and Et2O was added to the residue to afford crystals of 6-[(1E)- coupling constants are reported as δ(ppm) and J (Hz), re- 2-phenylethenyl]-3,4-dimethoxy-2H-pyran-2-one (0.079 g, spectively. Mass analyses were carried out in positive ESI 26% yield from 3,4-dimethoxy-6-methyl-2H-pyran-2-one). mode using a ZQ 4000 mass spectrometer (Waters Corpo- MP: 147 － 148℃. Rf: 0.33 (CH2Cl2). IR (KBr): 3083, 1688, −1 ration, Milford, MA, USA). HRMS analysis was performed 1643, 1543, 1356, 1206, 1152, 1016, 963 cm . UV/Vis lmax using an LTQ Orbitrap Velos EDT Ultimate 3000 system (DMSO) nm (log ε): 374 (4.27). 1H NMR (500 MHz, DMSO- and Xcalibur version 2.2 SPI (Thermo Fisher Scientific Inc., d6): 3.68 (3H, s, CH3), 3.95 (3H, s, CH3), 6.77 (1H, s, CH), 7.03 MA., USA) in ESI mode. Elemental analyses were achieved (1H, d, J = 16.5 Hz, CH), 7.27 (1H, d, J = 16.5 Hz, CH), 7.36 (1H, with a Yanaco CHNCORDER MT-3 instrument. HPLC t, J = 7.32 Hz, CH), 7.42 (2H, t, J = 7.32 Hz, CH), 7.64 (2H, d, J 13 analyses were carried out using a Gulliver HPLC system = 7.32 Hz, CH). C NMR (125 MHz, DMSO-d6): 57.18 (CH3), (JASCO Corp.) equipped with a photodiode array (PDA) 59.47 (CH3), 98.59 (CH), 119.49 (CH), 127.19 (C), 127.33 (CH), detector MD-910 (JASCO Corp.). A Cosmosil MSII-5C18 128.98 (CH), 129.23 (CH), 133.26 (CH), 135.29 (C), 154.31 column (4.6 mm × 150 mm; Nacalai Tesque, Inc., Kyoto, (C), 159.28 (C), 159.79 (C). MS (ESI): m/z (%) = 259 [M + H+] Japan) was used and the mobile phase was a mixture of (100), 281 [M + Na+] (53). HRMS-ESI: m/z [M + H+] calcd aqueous 10 mM formic acid (A) and 10 mM formic acid/ for C15H14O4 + H: 259.0970; found: 259.0974. Anal. Calcd CH3OH (B) for the HPLC analyses. The flow rate was 0.8 for C15H14O4: C, 69.76; H, 5.46%. Found: C, 69.64; H, 5.49%. mL/min starting with 100% A followed by a linear gradi- 6-[(1E)-2-Phenylethenyl]-3,4-dimethoxy-2H-pyran- ent reaching 100% B at 30 min. Thin-layer chromatogra- 2-one (36 mg, 0.14 mmol) was added to BBr3 in CH2Cl2 phy was performed on Merck Kieselgel 60 F254 plates ( 1 mol/L, 4 mL) at −80℃ and stirred at 25℃ for 40 h.
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