The Chemical Basis of Fungal Bioluminescence

Abstract

Many species of fungi naturally produce light, a phenomenon known as bioluminescence, however, the fungal substrates used in the chemical reactions that produce light have not been reported. We identified the fungal compound luciferin 3‐hydroxyhispidin, which is biosynthesized by oxidation of the precursor hispidin, a known fungal and plant secondary metabolite. The fungal luciferin does not share structural similarity with the other eight known luciferins. Furthermore, it was shown that 3‐hydroxyhispidin leads to bioluminescence in extracts from four diverse genera of luminous fungi, thus suggesting a common biochemical mechanism for fungal bioluminescence.

Two forms of substrate for the bioluminescent reaction in three species of basidiomycetes

“…The hot extracts are obtained by heat treatment of homogenised fungal biomass at high temperatures (80-100°C), which leads to denaturation of luciferase and other enzymes involved in luminescence while preserving the substrate for luminescent reactionluciferin. Interestingly, the hot extracts prepared from nonluminous fungi can also CONTACT Andrey E. Burov aeburov@ict.nsc.ru stimulate the light emission, thus implying that the substrate or its precursor is not specific for luminous species (Purtov et al 2015;Puzyr et al 2016Puzyr et al , 2017. There are known several successful attempts that demonstrated the fungal bioluminescence in vitro using the classical luciferin/luciferase test (Airth and McElroy 1959;Airth and Foerster 1962;Kamzolkina et al 1983Kamzolkina et al , 1984Oliveira and Stevani 2009;Oliveira et al 2012;Oba et al 2017).…”

“…The bisnoryangonin and hispidin are common among fungi of the Pholiota genus (Velisek and Cejpek 2011). Their presence in the fruiting bodies of Pholiota squarrosa as in vitro bioluminescence activating substances was recently confirmed (Purtov et al 2015;Puzyr et al 2016Puzyr et al , 2017. However, none of the Pholiota fungi is luminous (Chew et al 2015).…”

“…There is opinion that the mycelium of most or even all Armillaria species is luminescent (Desjardin et al 2008). There were no data available in the open literature that any of Armillaria members contain hispidin (or its analogues) until this substance was detected in A. borealis as a precursor of luciferin (Purtov et al 2015).…”

Purificação e caracterização de enzimas envolvidas na bioluminescência de fungos

“…Além disso, o tempo despendido (48 h) na obtenção de soluções parcialmente puras foi reduzido pela metade. Esta descoberta, somada à presença da hispidina e da luciferina em fungos não bioluminescentes (Nambudiri et al, 1974;Purtov et al, 2015)…”

Detecção e quantificação de derivados e intermediários de hispidina em fungos bioluminescentes e plantas por LC-MS/MS

“…A retomada desses testes pelo nosso grupo de pesquisa já nos anos 2000, conseguiu reproduzir os testes de Airth Foerster, indicando que se tratava realmente de uma reação enzimática (Oliveira & Stevani 2009). Em 2015, o substrato (3-hidróxihispidina, a luciferina) da luciferase envolvida na reação de emissão de luz foi caracterizado (Purtov et al 2015), que era um dos objetivos da proposta inicial deste trabalho. A hispidina, a molécula precursora da luciferina, é uma substância que pode ser encontrada em diversos fungos orelha-depau e em plantas, como Piperaceae (família da pimenta do reino), Zingiberaceae (família do gengibre e cúrcuma) e Equisetales (família da cavalinha).…”