Sulfoluciferin is Biosynthesized by a Specialized Luciferin Sulfotransferase in Fireflies.

Firefly luciferin is a specialized metabolite restricted to fireflies (family Lampyridae) and other select families of beetles (order Coleoptera). Firefly luciferin undergoes luciferase-catalyzed oxidation to produce light, thereby enabling the luminous mating signals essential for reproductive success in most bioluminescent beetles. Although firefly luciferin and luciferase have become widely used biotechnological tools, questions remain regarding the physiology and biochemistry of firefly bioluminescence. Here we report sulfoluciferin to be an in vivo derivative of firefly luciferin in fireflies and report the cloning of luciferin sulfotransferase (LST) from the North American firefly Photinus pyralis. LST catalyzes the production of sulfoluciferin from firefly luciferin and the sulfo-donor PAPS. Sulfoluciferin is abundant in several surveyed firefly genera as well as in the bioluminescent elaterid beetle Pyrophorus luminosus at a low level. We propose that sulfoluciferin could serve as a luciferin storage molecule in fireflies and that LST may find use as a new tool to modulate existing biotechnological applications of the firefly bioluminescent system.

[1]  D. Hall,et al.  Variation in opsin genes correlates with signalling ecology in North American fireflies , 2015, Molecular ecology.

[2]  Tomoko Suzuki,et al.  Identification of 3-enol sulfate of Cypridina luciferin, Cypridina luciferyl sulfate, in the sea-firefly Cypridina (Vargula) hilgendorfii , 2014 .

[3]  M. James,et al.  Enzyme kinetics of conjugating enzymes: PAPS sulfotransferase. , 2014, Methods in molecular biology.

[4]  Y. Oba,et al.  Biosynthesis of Firefly Luciferin in Adult Lantern: Decarboxylation of ʟ-Cysteine is a Key Step for Benzothiazole Ring Formation in Firefly Luciferin Synthesis , 2013, PloS one.

[5]  Bruce R Branchini,et al.  Crystal structure of firefly luciferase in a second catalytic conformation supports a domain alternation mechanism. , 2012, Biochemistry.

[6]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[7]  K. Hattori,et al.  Cloning, Expression, and Characterization of Cytosolic Sulfotransferase Isozymes from Drosophila melanogaster , 2008, Bioscience, biotechnology, and biochemistry.

[8]  Y. Ohmiya,et al.  Stereoisomeric bio‐inversion key to biosynthesis of firefly d‐luciferin , 2006, FEBS letters.

[9]  O. Shimomura Bioluminescence: Chemical Principles and Methods , 2006 .

[10]  K Gomi,et al.  Oxyluciferin, a Luminescence Product of Firefly Luciferase, Is Enzymatically Regenerated into Luciferin* , 2001, The Journal of Biological Chemistry.

[11]  A. Lundin Use of firefly luciferase in ATP-related assays of biomass, enzymes, and metabolites. , 2000, Methods in enzymology.

[12]  L. Kricka,et al.  Bioluminescence and chemiluminescence literature. 1994 Literature: Part I. , 1994, Journal of bioluminescence and chemiluminescence.

[13]  O. Shimomura,et al.  Structure of dinoflagellate luciferin and its enzymic and nonenzymic air-oxidation products , 1989 .

[14]  R. Geiger,et al.  Synthesis and Characterization of Luciferin Derivatives for Use in Bioluminescence Enhanced Enzyme Immunoassays. New Ultrasensitive Detection Systems for Enzyme Immunoassays, I. , 1987, Journal of clinical chemistry and clinical biochemistry. Zeitschrift fur klinische Chemie und klinische Biochemie.

[15]  K. Wood,et al.  Transient and Stable Expression of the Firefly Luciferase Gene in Plant Cells and Transgenic Plants , 1986, Science.

[16]  K. Wood,et al.  Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[17]  W. Jakoby,et al.  Phenol sulfotransferases. , 1979, The Journal of biological chemistry.

[18]  T. Goto,et al.  Squid bioluminescence III. Isolation and structure of Watasenia luciferin , 1976 .

[19]  M. J. Cormier,et al.  Studies on the bioluminescence of Renilla reniformis. VII. Conversion of luciferin into luciferyl sulfate by luciferin sulfokinase. , 1970, Biochemistry.

[20]  Y. Kishi,et al.  Cypridina bioluminescence III total synthesis of luciferin , 1966 .

[21]  Emil H. White,et al.  THE STRUCTURE AND SYNTHESIS OF FIREFLY LUCIFERIN , 1961 .