Evolution of bioluminescence in Anthozoa with emphasis on Octocorallia.

Bioluminescence is a widespread phenomenon that has evolved multiple times across the tree of life, converging among diverse fauna and habitat types. The ubiquity of bioluminescence, particularly in marine environments where it is commonly used for communication and defense, highlights the adaptive value of this trait, though the evolutionary origins and timing of emergence remain elusive for a majority of luminous organisms. Anthozoan cnidarians are a diverse group of animals with numerous bioluminescent species found throughout the world's oceans, from shallow waters to the light-limited deep sea where bioluminescence is particularly prominent. This study documents the presence of bioluminescent Anthozoa across depth and explores the diversity and evolutionary origins of bioluminescence among Octocorallia-a major anthozoan group of marine luminous organisms. Using a phylogenomic approach and ancestral state reconstruction, we provide evidence for a single origin of bioluminescence in Octocorallia and infer the age of occurrence to around the Cambrian era, approximately 540 Ma-setting a new record for the earliest timing of emergence of bioluminescence in the marine environment. Our results further suggest this trait was largely maintained in descendants of a deep-water ancestor and bioluminescent capabilities may have facilitated anthozoan diversification in the deep sea.

14-3-3 proteins are luciferases candidate proteins from lanternfish Diaphus watasei.

The lanternfish is a deep-sea fish with ventral-lateral and head photophores. It uses its ventral-lateral photophores to camouflage its ventral silhouette, a strategy called counterillumination. The bioluminescent reaction of lanternfish involves coelenterazine as a substrate luciferin but the enzyme catalyzing the bioluminescent reaction has not been identified. We report a candidate enzyme of luciferase from lanternfish Diaphus watasei. We purified the luciferase and performed SDS-PAGE analysis resulted in two bands corresponding to the activity, and following mass spectrometry analysis detected three 14-3-3 proteins of which functions is known to exhibit protein-protein interactions. The molecular weights and isoelectric points of the 14-3-3 proteins were almost consistent with the luciferase properties. The addition of two 14-3-3 binding compounds, R18 peptide and fusicoccin, resulted in the inhibition of the luciferase activity. However, the two 14-3-3 recombinant proteins showed very slight luminescence activity. These results suggested that the 14-3-3 proteins are candidate luciferases of D. watasei.

Acquisition of bioluminescent trait by non-luminous organisms from luminous organisms through various origins.

Bioluminescence is a natural light emitting phenomenon that occurs due to a chemical reaction between luciferin and luciferase. It is primarily an innate and inherited trait in most terrestrial luminous organisms. However, most luminous organisms produce light in the ocean by acquiring luminous symbionts, luciferin (substrate), and/or luciferase (enzyme) through various transmission pathways. For instance, coelenterazine, a well-known luciferin, is obtained by cnidarians, crustaceans, and deep-sea fish through multi-level dietary linkages from coelenterazine producers such as ctenophores, decapods, and copepods. In contrast, some non-luminous Vibrio bacteria became bioluminescent by obtaining lux genes from luminous Vibrio species by horizontal gene transfer. Various examples detailed in this review show how non-luminescent organisms became luminescent by acquiring symbionts, dietary luciferins and luciferases, and genes. This review highlights three modes (symbiosis, ingestion, and horizontal gene transfer) that allow organisms lacking genes for autonomous bioluminescent systems to obtain the ability to produce light. In addition to bioluminescence, this manuscript discusses the acquisition of other traits such as pigments, fluorescence, toxins, and others, to infer the potential processes of acquisition.

Biochemical characteristics and gene expression profiles of two paralogous luciferases from the Japanese firefly Pyrocoelia atripennis (Coleoptera, Lampyridae, Lampyrinae): insight into the evolution of firefly luciferase genes.

Two paralogous genes of firefly luciferase, Luc1 and Luc2, have been isolated from the species in two subfamilies, Luciolinae and Photurinae, of the family Lampyridae. The gene expression profiles have previously been examined only in the species of Luciolinae. Here we isolated Luc1 and Luc2 genes from the Japanese firefly Pyrocoelia atripennis. This is the first report of the presence of both Luc1 and Luc2 genes in the species of the subfamily Lampyrinae and of the exon-intron structure of Luc2 in the family Lampyridae. The luminescence of both gene products peaked at 547 nm under neutral buffer conditions, and the spectrum of Luc1, but not Luc2, was red-shifted under acidic conditions, as observed for Luc2 in the Luciolinae species. The semi-quantitative reverse transcription-polymerase chain reaction suggested that Luc1 was expressed in lanterns of all the stages except eggs, while Luc2 was expressed in the non-lantern bodies of eggs, prepupae, pupae, and female adults. These expression profiles are consistent with those in the Luciolinae species. Considering the distant phylogenetic relationship between Lampyrinae and Luciolinae in Lampyridae, we propose that fireflies generally possess two different luciferase genes and the biochemical properties and gene expression profiles for each paralog are conserved among lampyrid species.

Identification and characterization of the Luc2-type luciferase in the Japanese firefly, Luciola parvula, involved in a dim luminescence in immobile stages.

Nocturnal Japanese fireflies, Luciola parvula, emit from their lanterns a yellow light, one of the most red-shifted colors found among fireflies. Previously, we isolated and characterized two different types of luciferase gene, Luc1 and Luc2, from the fireflies Luciola cruciata and Luciola lateralis; Luc1 is responsible for the green-yellow luminescence of larval and adult lanterns, whereas Luc2 is responsible for the dim greenish glow of eggs and pupal bodies. The biological role of firefly lanterns in adults is related to sexual communication, but why the eggs and pupae glow remains uncertain. In this study, we isolated the gene Luc2 from L. parvula, and compared its expression profiles and enzymatic characteristics with those of Luc1. A semi-quantitative reverse transcription polymerase chain reaction showed that Luc1 was predominantly expressed in larvae, prepupae, pupae and adults, whereas Luc2 was expressed in eggs, prepupae, pupae and adult females. Enzymatic analyses showed that the luminescent color of Luc1 matches the visual sensitivity of L. parvula eyes, whereas that of Luc2 is very different from it. These results suggest that the biological role of Luc2 expressed in immobile stages is not intraspecific communication.

Contribution to the taxonomy of Lobellini (Collembola: Neanurinae) and investigations on luminous Collembola from Japan.

Lobella sauteri was redescribed based on the lectotype and specimens obtained from the type locality Bugenji, Yokohama, Kanagawa, as the true identity of the luminous Collembola, Lobella sp. Lobella sauteri has morphological traits characteristic of the genus currently called Telobella. As L. sauteri is the type species of Lobella, the genus Telobella was synonymised with Lobella according to the principle of priority, and the genus Lobella was redefined to include both the species previously assigned to Telobella and those previously assigned to Lobella. A new species Lobella monstrum sp. nov. was described and new combinations were proposed for certain species in Lobellini. Light-emitting capacity was confirmed in L. sauteri and newly reported in Lobella yambaru comb. nov. Vitronura giselae and Vitronura kunigamiensis.

Investigating the diversity of bioluminescent marine worm Polycirrus (Annelida), with description of three new species from the Western Pacific.

Bioluminescence, a phenomenon observed widely in organisms ranging from bacteria to metazoans, has a significant impact on the behaviour and ecology of organisms. Among bioluminescent organisms, Polycirrus, which has unique emission wavelengths, has received attention, and advanced studies such as RNA-Seq have been conducted, but they are limited to a few cases. In addition, accurate species identification is difficult due to lack of taxonomic organization. In this study, we conducted comprehensive taxonomic survey of Japanese Polycirrus based on multiple specimens from different locations and described as three new species: Polycirrus onibi sp. nov., P. ikeguchii sp. nov. and P. aoandon sp. nov. The three species can be distinguished from the known species based on the following characters: (i) arrangement of mid-ventral groove, (ii) arrangement of notochaetigerous segments, (iii) type of neurochaetae uncini, and (iv) arrangement of nephridial papillae. By linking the bioluminescence phenomenon with taxonomic knowledge, we established a foundation for future bioluminescent research development. We also provide a brief phylogenetic tree based on cytochrome c oxidase subunit I (COI) sequences to discuss the evolution of bioluminescence and the direction of future research.

Kleptoprotein bioluminescence: Parapriacanthus fish obtain luciferase from ostracod prey.

Through their diet, animals can obtain substances essential for imparting special characteristics, such as toxins in monarch butterflies and luminescent substances in jellyfishes. These substances are typically small molecules because they are less likely to be digested and may be hard for the consumer to biosynthesize. Here, we report that Parapriacanthus ransonneti, a bioluminescent fish, obtains not only its luciferin but also its luciferase enzyme from bioluminescent ostracod prey. The enzyme purified from the fish's light organs was identical to the luciferase of Cypridina noctiluca, a bioluminescent ostracod that they feed upon. Experiments where fish were fed with a related ostracod, Vargula hilgendorfii, demonstrated the specific uptake of the luciferase to the fish's light organs. This "kleptoprotein" system allows an organism to use novel functional proteins that are not encoded in its genome and provides an evolutionary alternative to DNA-based molecular evolution.

Evidence for de novo Biosynthesis of the Luminous Substrate Coelenterazine in Ctenophores.

Coelenterazine is a key substrate involved in marine bioluminescence which is used for light-production by at least nine phyla. Some luminous animals, such as the hydromedusa Aequorea, lack the ability to produce coelenterazine endogenously and instead depend on dietary sources. Little is known about the source organisms or the metabolic process of coelenterazine biosynthesis. Here, we present evidence that ctenophores are both producers and suppliers of coelenterazine in marine ecosystems. Using biochemical assays and mass spectrometry analyses, we detected coelenterazine from cultured ctenophores fed with a non-luminous coelenterazine-free diet. We propose that ctenophores are an emerging model organism to study coelenterazine biosynthesis and the origins of bioluminescence.

Firefly genomes illuminate parallel origins of bioluminescence in beetles.

Fireflies and their luminous courtships have inspired centuries of scientific study. Today firefly luciferase is widely used in biotechnology, but the evolutionary origin of bioluminescence within beetles remains unclear. To shed light on this long-standing question, we sequenced the genomes of two firefly species that diverged over 100 million-years-ago: the North American Photinus pyralis and Japanese Aquatica lateralis. To compare bioluminescent origins, we also sequenced the genome of a related click beetle, the Caribbean Ignelater luminosus, with bioluminescent biochemistry near-identical to fireflies, but anatomically unique light organs, suggesting the intriguing hypothesis of parallel gains of bioluminescence. Our analyses support independent gains of bioluminescence in fireflies and click beetles, and provide new insights into the genes, chemical defenses, and symbionts that evolved alongside their luminous lifestyle.