Firefly genomes illuminate parallel origins of bioluminescence in beetles

Fallon, Timothy R.; Lower, Sarah E.; Chang, Ching-Ho; Bessho-Uehara, Manabu; Martin, Gavin J.; Bewick, Adam J.; Behringer, Megan G; Debat, Humberto Julio; Wong, Isaac; Day, John C.; Suvorov, Anton; Silva, Christian J.; Stanger‐Hall, Kathrin F.; Hall, David W.; Schmitz, Robert J.; Nelson, David R.; Lewis, Sara M.; Shigenobu, Shuji; Bybee, Seth; Larracuente, Amanda M.; Oba, Yuichi; Weng, Jing‐Ke

doi:10.7554/elife.36495

Cited by 113 publications

(95 citation statements)

References 286 publications

(446 reference statements)

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“…Although a second copy of luz and cyp450 were found in M. sanguinolenta , they showed much lower expression (2 and 3 transcripts per million (TPM), respectively) than those in the cluster (282 and 138 TPM, respectively). The remaining OGs upregulated in mycelia showing higher bioluminescence included genes involved in ABC transporters and Aceyl-CoA synthetases which also showed a predicted function in metabolic adaptations to bioluminescence in firefly and glowworm 43,44 . ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Mycena genomes resolve the evolution of fungal bioluminescence

Lee

Lin

et al. 2020

Preprint

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24Mushroom-forming fungi in the order Agaricales represent an independent origin of 25 bioluminescence in the tree of life, yet the diversity, evolutionary history, and timing of 26 the origin of fungal luciferases remain elusive. We sequenced the genomes and 27transcriptomes of five bonnet mushroom species (Mycena spp.), a diverse lineage 28comprising the majority of bioluminescent fungi. We show that bioluminescence 29 evolved in the common ancestor of Mycena spp. and the marasmioid clade of 30Agaricales and was maintained through at least 160 million years of evolution. We 31revealed Mycena exhibit two-speed genomes and resolve how the luciferase cluster was 32 derived by duplication and translocation, frequently rearranged and lost in most Mycena 33 species, but conserved in the Armillaria lineage. Luciferase cluster members were co-34 expressed across developmental stages, with highest expression in fruiting body caps 35and stipes, suggesting fruiting-related adaptive functions. Our results contribute to 36 understanding a de novo origin of bioluminescence and the corresponding gene cluster 37 in a diverse group of enigmatic fungal species. 38

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Section: Resultsmentioning

confidence: 99%

Mycena genomes resolve the evolution of fungal bioluminescence

Lee

Lin

et al. 2020

Preprint

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“…repository, project ID MTBLS698 (https://www.ebi.ac.uk/metabolights/MTBLS698) 10 for the analysis of luminescent and non-luminescent tissue of beetle species 10 . Data were collected on a Thermo Q-Exactive Orbitrap using data dependent acquisition (DDA) with polarity switching using a C18 column 10 . A single file generated from the hemolymph of an adult male Photinus Pyralis beetle was selected (Ppyr_hemolymph_extract.mzML).…”

Section: Lc-ms/ms Firefly Metabolights Data Source Lc-ms/ms Data Wasmentioning

confidence: 99%

“…A single file generated from the hemolymph of an adult male Photinus Pyralis beetle was selected (Ppyr_hemolymph_extract.mzML). The positive ion mode analysis was previously carried out using MZmine (v2.30) with MS 2 similarity search and published using the parameters described in section 4.6 of the supplementary information 10 . The positive ion data for Ppyr_hemolymph_extract.mzML was reanalyzed here with MZmine2 (v2.53) using the same settings.…”

Section: Lc-ms/ms Firefly Metabolights Data Source Lc-ms/ms Data Wasmentioning

confidence: 99%

“…In this study, we demonstrate the effectiveness of hierarchically clustering MS/MS spectra for the discovery of underlying ion profiles to identify or classify unknown metabolites. A previously published dataset of firefly predator defense lucibufagin compounds 10 was reanalysed using dynamic binning and hierarchical clustering, and results were compared to the gold standard web-based Feature Based Molecular Networking (FBMN) module of GNPS. We provide the techniques used as a simple but effective workflow, BioDendro (https://github.com/ ccdmb/BioDendro), that users with minimal coding skills can easily use and customize to identify core fragmentation patterns.…”

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Hierarchical clustering of MS/MS spectra from the firefly metabolome identifies new lucibufagin compounds

Rawlinson

Jones

Rakshit

et al. 2020

Sci Rep

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Metabolite identification is the greatest challenge when analysing metabolomics data, as only a small proportion of metabolite reference standards exist. clustering MS/MS spectra is a common method to identify similar compounds, however interrogation of underlying signature fragmentation patterns within clusters can be problematic. Previously published high-resolution LC-MS/MS data from the bioluminescent beetle (Photinus pyralis) provided an opportunity to mine new specialized metabolites in the lucibufagin class, compounds important for defense against predation. We aimed to 1) provide a workflow for hierarchically clustering MS/MS spectra for metabolomics data enabling users to cluster, visualise and easily interrogate the identification of underlying cluster ion profiles, and 2) use the workflow to identify key fragmentation patterns for lucibufagins in the hemolymph of P. pyralis. Features were aligned to their respective MS/MS spectra, then product ions were dynamically binned and resulting spectra were hierarchically clustered and grouped based on a cutoff distance threshold. Using the simplified visualization and the interrogation of cluster ion tables the number of lucibufagins was expanded from 17 to a total of 29.

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“…Tree topologies of the molecular phylogeny of luciferase genes were consistent with nuclear/mitochondrial gene trees 2 . To trace back the evolution of firefly luciferase properties, we targeted seven key ancestral genes corresponding to the ancestral luciferase of Elateroidea (AncElat), the ancestral luciferase of 'cantharoids' (AncCanth), the ancestral luciferase of Lampyridae (AncLamp), the ancestral Luc1-type luciferase of Lampyridae (AncLuc1; genomic analyses had shown that fireflies possess two different types of luciferase gene, Luc1-type and Luc2-type, generated by gene duplication occurring at the basal position of the lineage in Lampyridae) 5,8,11 , the ancestral Luc2-type luciferase of Lampyridae (AncLuc2), the ancestral Luc1-type luciferase in Lampyrinae, a major subfamily of Lampyridae (AncLampn1), and the ancestral Luc1-type luciferase of Luciolinae, another major subfamily (AncLucin1) ( Fig. 1b; Table 1; Extended Data Fig.…”

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confidence: 99%

Resurrecting the ancient glow

Oba

Konishi

Yano

et al. 2019

Preprint

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The colour of firefly bioluminescence is primarily determined by the structure of the enzyme luciferase 1 . To date, firefly luciferase genes have been isolated from over 30 extant species producing light ranging in colour from deep-green to orange-yellow. We have reconstructed ancestral firefly luciferase genes and characterised the enzymatic properties of the recombinant proteins in order to predict ancestral firefly light emission. Results showed that the synthetic luciferase for the last common firefly ancestor exhibited green light. All known firefly species are bioluminescent in the larval stages 2 , with a common shared ancestor arising approximately 100 Mya 3 . Combined, our findings propose within the Cretaceous forest the common ancestor of contemporary fireflies emitted green light, most likely for aposematic display from nocturnal predation.Over the centuries the bioluminescence of fireflies has attracted much attention as a charming seasonal sight, particularly in Asia, and recently as a useful diagnostic tool in the biomedical sciences 4 . It is proposed that firefly bioluminescence originated as an aposematic warning display toward predators, and later acquired a role in sexual communication for many firefly species 2 .Fireflies belong to the beetle family Lampyridae; composed of 7 subfamilies containing around 2,000 recognized species around the world 2 . Luminescent beetles are additionally found in the families Phengodidae, Rhagophthalmidae and Elateridae. It has been considered that Phengodidae and Rhagophthalmidae are sister groups of the 2 Lampyridae ('cantharoid' group) and share a common origin of bioluminescence; conversely bioluminescence in Elateridae evolved independently of the cantharoid group 5 .The molecular system of bioluminescence is shared among these four families: the chemical structure of the luminescent substrate, D-luciferin, is considered identical for all luminescent beetles, and the luminescence reaction is catalyzed by homologous luciferases (> 48% AA identity) in the presence of O 2 , ATP, and Mg 2+ (Fig. 1a) 5 .Despite the commonality in enzymatic reaction and components, luminescence colour can vary widely between species. The European glowworm Lampyris noctiluca, for example, emits green light, the North American Big Dipper firefly Photinus pyralis yellow-green light, and the Japanese lesser firefly Luciola parvula orange-yellow light.The differences in luminescence colour is considered to be the consequence of evolutional strategies for warning predators and attracting mating partners more effectively 2,6 .

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Firefly genomes illuminate parallel origins of bioluminescence in beetles

Cited by 113 publications

References 286 publications

Mycena genomes resolve the evolution of fungal bioluminescence

Mycena genomes resolve the evolution of fungal bioluminescence

Hierarchical clustering of MS/MS spectra from the firefly metabolome identifies new lucibufagin compounds

Resurrecting the ancient glow

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