Yuichi Oba, Dr.
Associate Professor of Chubu University
Visiting Associate Professor of Nagoya University
BIOLUMINESCENCE AND ITS EVOLUTION:
Luminescent animals occur in 11 phyla and their luminescence systems have evolved independently. So then what is the origin of “Luciferase” enzyme? Where “Luciferin” substrate comes from? The evolutionary process for their curious chemistries remains largely unknown (1, 2). I am focusing on the biochemistry of luminescent animals and its evolutionary aspects using biochemistry, molecular biology, and analytical chemistry.
I and my co-workers has been shown that the luciferase in fireflies (Lampyridae, Coleoptera) was originated from “fatty acyl-CoA synthetase”, an enzyme involving in beta-oxidation (3-5). Recently, we demonstrated that changes in a few amino acids of fatty acyl-CoA synthetase in non-luminous beetle give significant luminescence activity (6). This result indicates that special catalytic activity of new enzyme is readily evolvable from unrelated common enzyme by small number of substitution steps.
With regard to the origin of luciferins, we showed that luciferin in sea-firefly (Cypridina hilgendorfii) is biosynthesized from three amino acids (Typ, Arg, Ile) (7,8), coelenterazine (luciferins and luminescence chromophore of photoproteins in various marine luminous organisms, such as jellyfishes and crustaceans) is biosynthesized from 2 Tyr and 1 Phe in the deep-sea copepod, Metridia pacifica (9), and firefly luciferin from 1,4-hydroquinone and 2 Cys in the Japanese firefly Luciola lateralis (10). Luciferins are very specialized substrate for luminescence. But these our results show that some luciferins are biosynthesized from usual materials such as alpha-amino acids.
Molecular phylogenetic analyses of luminous beetles have also been performed. The result suggests that luminescence in the some species of click beetle (Elateridae) evolved once in the subfamily Agrypninae and common ancestor of Elateridae was probably non-luminous (11). In contrast, the family Lampyridae is the monophyletic group and the common ancestor of Lampyridae was luminous (12).
We found that fireflies possess two different genes of luciferase. One is responsible for the yellow-luminescence of lantern in larvae and adult, on the other hand, another is responsible for the dim green-luminescence of egg and whole body of pupae. Phylogenetic analysis revealed that these two luciferase genes were originated at the basal position of the family Lampyridae by gene duplication (13, 14).
We determined with Russian Academy of Science that fungal pre-luciferin is ‘hispidin’ (6-(3,4-dihydroxystyryl)-4-hydroxy-2-pyrone). We showed that luminous mushrooms emit continuous green light by the enzymatic reaction of 3-hydroxy hispidin (luciferin) and undetermined luciferase (15).
Now, I join in the Japanese DNA barcode of life project (http://www.jboli.org/en/). My tasks are the construction of barcoding database on Japanese Elateridae (16) and Japanese luminous animals (17).
- Oba Y, Branham MA, Fukatsu T (2011) The terrestrial bioluminescent animals of Japan. Zool. Sci.(review) 28: 771-789.
- Oba, Y. (2014) Insect Bioluminescence in the Post-Molecular Biology Era. pp. 88-114. In: Hoffman, K. H. (Ed.) Insect Molecular Biology and Ecology. CRC Press, Florida.
- Oba Y, Ojika M, Inouye S (2003) Firefly luciferase is a bifunctional enzyme: ATP-dependent monooxygenase and a long chain fatty acyl-CoA synthetase. FEBS Lett.540: 251-254.
- Oba Y, Sato M, Ohta Y, Inouye S (2006) Identification of paralogous genes of firefly luciferase in the Japanese firefly, Luciola cruciata. Gene368: 53-60.
- Oba Y (2009) On the origin of beetle luminescence. In “Bioluminescence in Focus- A Collection of Illuminating Essays” Ed by VB Meyer-Rochow, Research Signpost, Kerala, India, pp 277-290.
- Oba Y, Iida K, Inouye S (2009) Functional conversion of fatty acyl-CoA synthetase to firefly luciferase by site-directed mutagenesis: A key substitution responsible for luminescence activity. FEBS Lett.583: 2004-2008.
- Oba Y, Kato S, Ojika M, Inouye S (2002) Biosynthesis of luciferin in the sea firefly, Cypridina hilgendorfii: L-Tryptophan is a component in Cypridina luciferin. Tetrahedron Lett.43: 2389-2392.
- Kato S, Oba Y, Ojika M, Inouye S (2004) Identification of the biosynthetic units of Cypridina luciferin in Cypridina (Vargula) hilgendorfii by LC/ESI-TOF-MS. Tetrahedron60: 11427-11434.
- Oba Y, Kato S, Ojika M, Inouye S (2009) Biosynthesis of coelenterazine in the deep-sea copepod, Metridia pacifica. Biochem. Biophys. Res. Commun.390: 684-688.
- Oba Y, Yoshida N, Kanie S, Ojika M, Inouye S. (2013) Biosynthesis of firefly luciferin in adult lantern: decarboxylation of L-cysteine is a key step for benzothiazole ring formation in firefly luciferin. PLOS ONE 8: e84023.
- Sagegami-Oba R, Oba Y, Ohira H (2007) Phylogenetic relationships of click beetles (Coleoptera: Elateridae) inferred from 28S ribosomal DNA: Insights into the evolution of bioluminescence in Elateridae. Mol. Phylogenet. Evol.42: 410-421.
- Sagegami-Oba R, Takahashi N, Oba Y (2007) The evolutionary process of bioluminescence and aposematism in cantharoid beetles (Coleoptera: Elateroidea) inferred by the analysis of 18S ribosomal DNA. Gene400: 104-113.
- Oba Y, Mori N, Yoshida M, Inouye S. (2010) Identification and characterization of a luciferase isotype in the Japanese firefly, Luciola cruciata, involving in the dim glow of firefly eggs. Biochemistry 49: 10788-10795.
- Oba Y, Furuhashi M, Bessho M, Sagawa S, Ikeya H, Inouye S. (2013) Bioluminescence of a firefly pupa: involvement of a luciferase isotype in the dim glow of pupae and eggs in the Japanese firefly, Luciola lateralis. Photochem. Photobiol. Sci. 12: 854-863.
- Purtov KV, Petushkov VN, Baranov MS, Mineev KS, Rodionova NS, Kaskova ZM, Tsarkova AS, Petunin AI, Bondar VS, Rodicheva EK, Medvedeva SE, Oba Y, Oba Y, Arseniev AS, Lukyanov S, Gitelson JI, Yampolsky IV (2015) The chemical basis of fungal bioluminescence. Angew. Chem. 54: 8124-8128.
- Oba Y, Ohira H, Murase Y, Moriyama A, Kumazawa Y (2015) DNA barcoding of Japanese click beetles (Coleoptera, Elateridae). PLOS ONE 10: e0116612.
- Oba Y, Schultz TD (2014) Eco-Evo Bioluminescence on Land and in the Sea. pp. 3-36. In: Thouand, G and Marks, R. (Eds.). Bioluminescence: Fundamentals and Applications in Biotechnology Vol. 1. Springer, Heidelberg.