Firefly genomes illuminate parallel origins of bioluminescence in beetles

Abstract

SummaryFireflies are among the best-studied of the bioluminescent organisms. Despite longterm interest in the biochemistry, neurobiology, and evolution of firefly flash signals and the widespread biotechnological applications of firefly luciferase, only a limited set of genes related to this complex trait have been described. To investigate the genetic basis of firefly bioluminescence, we generated a high-quality reference genome for the Big Dipper firefly Photinus pyralis, from which the first laboratory luciferase was cloned, using long-read (PacBio), short-read (Illumina), and Hi-C sequencing technologies. To facilitate comparative genomics, we also generated short-read genome assemblies for a Japanese firefly Aquatica lateralis and a bioluminescent click beetle, Ignelater luminosus. Analyses of these genomic datasets supports at least two independent gains of luminescence in beetles, and provides new insights into the evolution of beetle bioluminescence and chemical defenses that likely co-evolved over their 100 million years of evolution.

Enzymatic promiscuity and the evolution of bioluminescence

“…These differences could reflect divergence of a common luciferase, or convergent evolution of two or more distinct ancestral enzymes to achieve light emission with d ‐luciferin. Complete genomes for different bioluminescent beetle species are now available, and analysis of these genomes adds credence to the latter theory: The luciferases for fireflies and click beetles both arose from separate duplication events of ancestral ACSLs, which independently converged on luciferase activity with d ‐luciferin .…”

“…recently demonstrated that l ‐luciferin can be synthesized in neutral buffer conditions under air atmosphere at room temperature, enzymes likely mediate in vivo d ‐luciferin metabolism . To establish the identities of the enzymes responsible for luciferin metabolism, recent studies have focused on characterization of the transcriptome of fireflies . These studies have uncovered several candidate enzymes that could presumably function in these reactions and have high expression in lantern tissue .…”

“…To establish the identities of the enzymes responsible for luciferin metabolism, recent studies have focused on characterization of the transcriptome of fireflies . These studies have uncovered several candidate enzymes that could presumably function in these reactions and have high expression in lantern tissue . Furthermore, bioluminescence occurs in the peroxisomes of firefly lantern cells.…”

“…This makes bioluminescence particularly suited to dark environments such as the night sky and the depths of the ocean. Bioluminescence has evolved multiple times in nature, with distinct luciferases and luciferins that accomplish light emission using unique protein and chemical scaffolds .…”

Advances in bioluminescence imaging: new probes from old recipes

“…Transcriptome profiling revealed multiple conserved genes that are likely involved in the de novo synthesis of D-luciferin. [13] Related efforts to elucidate coelenterazine biosynthesis have also been reported. [14]…”