A putative chordate luciferase from a cosmopolitan tunicate indicates convergent bioluminescence evolution across phyla

Tessler, Michael; Gaffney, Jean P.; Oliveira, Anderson G.; Guarnaccia, Andrew; Dobi, Krista C.; Gujarati, Nehaben A.; Galbraith, Moira; Mirza, Jeremy D.; Sparks, John S.; Pieribone, Vincent A.; Wood, Robert J.; Gruber, David F.

doi:10.1038/s41598-020-73446-w

Title: A putative chordate luciferase from a cosmopolitan tunicate indicates convergent bioluminescence evolution across phyla

Journal Article · 19 October 2020 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-020-73446-w · OSTI ID:1678786

Tessler, Michael; Gaffney, Jean P.; Oliveira, Anderson G.; Guarnaccia, Andrew; Dobi, Krista C.; Gujarati, Nehaben A.; Galbraith, Moira; Mirza, Jeremy D.; Sparks, John S.; Pieribone, Vincent A.; Wood, Robert J.; Gruber, David F.

Abstract Pyrosomes are tunicates in the phylum Chordata, which also contains vertebrates. Their gigantic blooms play important ecological and biogeochemical roles in oceans. Pyrosoma , meaning “fire-body”, derives from their brilliant bioluminescence. The biochemistry of this light production is unknown, but has been hypothesized to be bacterial in origin. We found that mixing coelenterazine—a eukaryote-specific luciferin—with Pyrosoma atlanticum homogenate produced light. To identify the bioluminescent machinery, we sequenced P. atlanticum transcriptomes and found a sequence match to a cnidarian luciferase (RLuc). We expressed this novel luciferase (PyroLuc) and, combined with coelenterazine, it produced light. A similar gene was recently predicted from a bioluminescent brittle star, indicating that RLuc-like luciferases may have evolved convergently from homologous dehalogenases across phyla (Cnidaria, Echinodermata, and Chordata). This report indicates that a widespread gene may be able to functionally converge, resulting in bioluminescence across animal phyla, and describes and characterizes the first putative chordate luciferase.

View Journal Article

Cite

Export

Save

Research Organization:: New York Univ. (NYU), NY (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0014377

OSTI ID:: 1678786

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 10; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (47)

Pyrosome consumption by benthic organisms during blooms in the northeast Pacific and Gulf of Mexico Archer, Stephanie K.; Kahn, Amanda S.; Leys, Sally P. Ecology, Vol. 99, Issue 4 https://doi.org/10.1002/ecy.2097	journal	January 2018
Range expansion of tropical pyrosomes in the northeast Pacific Ocean Sutherland, Kelly R.; Sorensen, Hilarie L.; Blondheim, Olivia N. Ecology, Vol. 99, Issue 10 https://doi.org/10.1002/ecy.2429	journal	July 2018
The origin, diversity, and structure function relationships of insect luciferases Viviani, V. R. Cellular and Molecular Life Sciences, Vol. 59, Issue 11 https://doi.org/10.1007/PL00012509	journal	November 2002
Species-specific bioluminescence facilitates speciation in the deep sea Davis, Matthew P.; Holcroft, Nancy I.; Wiley, Edward O. Marine Biology, Vol. 161, Issue 5 https://doi.org/10.1007/s00227-014-2406-x	journal	February 2014
Widespread occurrence of coelenterazine in marine bioluminescence Shimomura, Osamu; Inoue, Shoji; Johnson, Frank H. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 65, Issue 2 https://doi.org/10.1016/0305-0491(80)90044-9	journal	January 1980
Presence of coelenterazine in non-bioluminescent marine organisms Shimomura, Osamu Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 86, Issue 2 https://doi.org/10.1016/0305-0491(87)90306-3	journal	January 1987
DspA from Strongylocentrotus purpuratus: The first biochemically characterized haloalkane dehalogenase of non-microbial origin Fortova, Andrea; Sebestova, Eva; Stepankova, Veronika Biochimie, Vol. 95, Issue 11 https://doi.org/10.1016/j.biochi.2013.07.025	journal	November 2013
Evolving haloalkane dehalogenases Janssen, Dick B. Current Opinion in Chemical Biology, Vol. 8, Issue 2 https://doi.org/10.1016/j.cbpa.2004.02.012	journal	April 2004
Ultra-gentle soft robotic fingers induce minimal transcriptomic response in a fragile marine animal Tessler, Michael; Brugler, Mercer R.; Burns, John A. Current Biology, Vol. 30, Issue 4 https://doi.org/10.1016/j.cub.2020.01.032	journal	February 2020
Crystal Structures of the Luciferase and Green Fluorescent Protein from Renilla reniformis Loening, Andreas Markus; Fenn, Timothy David; Gambhir, Sanjiv Sam Journal of Molecular Biology, Vol. 374, Issue 4 https://doi.org/10.1016/j.jmb.2007.09.078	journal	December 2007
Phylogenomics offers resolution of major tunicate relationships Kocot, Kevin M.; Tassia, Michael G.; Halanych, Kenneth M. Molecular Phylogenetics and Evolution, Vol. 121 https://doi.org/10.1016/j.ympev.2018.01.005	journal	April 2018
The bioluminescence emission spectra of Pyrosoma atlanticum, P. spinosum (Tunicata), Euphausia tenera (Crustacea) and Gonostoma sp. (Pisces) Swift, Elijah; Biggley, William H.; Napora, Theodore A. Journal of the Marine Biological Association of the United Kingdom, Vol. 57, Issue 3 https://doi.org/10.1017/S0025315400025170	journal	August 1977
Light-Emitting Dehalogenases: Reconstruction of Multifunctional Biocatalysts Chaloupkova, Radka; Liskova, Veronika; Toul, Martin ACS Catalysis, Vol. 9, Issue 6 https://doi.org/10.1021/acscatal.9b01031	journal	April 2019
Properties and reaction mechanism of the bioluminescence system of the deep-sea shrimp Oplophorus gracilorostris Shimomura, Osamu; Masugi, Takashi; Johnson, Frank H. Biochemistry, Vol. 17, Issue 6 https://doi.org/10.1021/bi00599a008	journal	March 1978
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran Nature Protocols, Vol. 8, Issue 8 https://doi.org/10.1038/nprot.2013.084	journal	July 2013
A Dexterous, Glove-Based Teleoperable Low-Power Soft Robotic Arm for Delicate Deep-Sea Biological Exploration Phillips, Brennan T.; Becker, Kaitlyn P.; Kurumaya, Shunichi Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33138-y	journal	October 2018
Quantification of bioluminescence from the surface to the deep sea demonstrates its predominance as an ecological trait Martini, Séverine; Haddock, Steven H. D. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep45750	journal	April 2017
1001 lights: luciferins, luciferases, their mechanisms of action and applications in chemical analysis, biology and medicine Kaskova, Zinaida M.; Tsarkova, Aleksandra S.; Yampolsky, Ilia V. Chemical Society Reviews, Vol. 45, Issue 21 https://doi.org/10.1039/C6CS00296J	journal	January 2016
Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Lorenz, W. W.; McCann, R. O.; Longiaru, M. Proceedings of the National Academy of Sciences, Vol. 88, Issue 10 https://doi.org/10.1073/pnas.88.10.4438	journal	May 1991
Bioluminescence and the Pelagic Visual Environment Widder, Edith Marine and Freshwater Behaviour and Physiology, Vol. 35, Issue 1-2 https://doi.org/10.1080/10236240290025581	journal	January 2002
Unconventional signalling in tunicates Mackie, G. O. Marine and Freshwater Behaviour and Physiology, Vol. 26, Issue 2-4 https://doi.org/10.1080/10236249509378939	journal	September 1995
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Glowing Worms: Biological, Chemical, and Functional Diversity of Bioluminescent Annelids Verdes, Aida; Gruber, David F. Integrative and Comparative Biology, Vol. 57, Issue 1 https://doi.org/10.1093/icb/icx017	journal	June 2017
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku340	journal	April 2014
ANISEED 2017: extending the integrated ascidian database to the exploration and evolutionary comparison of genome-scale datasets Brozovic, Matija; Dantec, Christelle; Dardaillon, Justine Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1108	journal	November 2017
Pyrosoma atlanticum (Tunicata, Thaliacea): grazing impact on phytoplankton standing stock and role in organic carbon flux Drits, Alexander V.; Arashkevich, Elena G.; Semenova, Tatjana N. Journal of Plankton Research, Vol. 14, Issue 6 https://doi.org/10.1093/plankt/14.6.799	journal	January 1992
A monograph of the order Pyrosomatida (Tunicata, Thaliacea) van Soest, R. W. M. Journal of Plankton Research, Vol. 3, Issue 4 https://doi.org/10.1093/plankt/3.4.603	journal	January 1981
Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output Loening, A. M. Protein Engineering Design and Selection, Vol. 19, Issue 9 https://doi.org/10.1093/protein/gzl023	journal	July 2006
A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence Delroisse, Jérôme; Ullrich-Lüter, Esther; Blaue, Stefanie Open Biology, Vol. 7, Issue 4 https://doi.org/10.1098/rsob.160300	journal	April 2017
A photoactivatable green-fluorescent protein from the phylum Ctenophora Haddock, Steven H. D.; Mastroianni, Nadia; Christianson, Lynne M. Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1685 https://doi.org/10.1098/rspb.2009.1774	journal	December 2009
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/gce.2010.5676129	conference	November 2010
Structure-function studies on the active site of the coelenterazine-dependent luciferase from Renilla Woo, Jongchan; Howell, Matthew H.; von Arnim, Albrecht G. Protein Science, Vol. 17, Issue 4 https://doi.org/10.1110/ps.073355508	journal	April 2008
Stimulation of Bioluminescence in Dinoflagellates by red Light Sweeney, Beatrice M.; Fork, David C.; Satoh, Kazuhiko Photochemistry and Photobiology, Vol. 37, Issue 4 https://doi.org/10.1111/j.1751-1097.1983.tb04499.x	journal	April 1983
An unprecedented taxonomic revision of a model organism: the paradigmatic case of Ciona robusta and Ciona intestinalis Gissi, Carmela; Hastings, Kenneth E. M.; Gasparini, Fabio Zoologica Scripta, Vol. 46, Issue 5 https://doi.org/10.1111/zsc.12233	journal	February 2017
Bacterial Origin of Luminescence in Marine Animals Leisman, G.; Cohn, D. H.; Nealson, K. H. Science, Vol. 208, Issue 4449 https://doi.org/10.1126/science.208.4449.1271	journal	June 1980
Bacterial bioluminescence: its control and ecological significance. Nealson, K. H.; Hastings, J. W. Microbiological Reviews, Vol. 43, Issue 4 https://doi.org/10.1128/MMBR.43.4.496-518.1979	journal	January 1979
Bioluminescence in the Sea Haddock, Steven H. D.; Moline, Mark A.; Case, James F. Annual Review of Marine Science, Vol. 2, Issue 1 https://doi.org/10.1146/annurev-marine-120308-081028	journal	January 2010
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
The origins of marine bioluminescence: turning oxygen defence mechanisms into deep-sea communication tools. Rees, J. F.; de Wergifosse, B.; Noiset, O. Journal of Experimental Biology, Vol. 201, Issue 8 https://doi.org/10.1242/jeb.201.8.1211	journal	April 1998
The transcriptome of the Bermuda fireworm Odontosyllis enopla (Annelida: Syllidae): A unique luciferase gene family and putative epitoky-related genes Brugler, Mercer R.; Aguado, M. Teresa; Tessler, Michael PLOS ONE, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pone.0200944	journal	August 2018
Marine Leech Anticoagulant Diversity and Evolution Tessler, Michael; Marancik, David; Champagne, Donald Journal of Parasitology, Vol. 104, Issue 3 https://doi.org/10.1645/17-64	journal	June 2018
Patterns of Stimulated Bioluminescence in Two Pyrosomes (Tunicata: Pyrosomatidae) Bowlby, M. R.; Widder, E. A.; Case, J. F. The Biological Bulletin, Vol. 179, Issue 3 https://doi.org/10.2307/1542326	journal	December 1990
Grazing by Pyrosoma atlanticum (Tunicata, Thaliacea) in the south Indian Ocean Perissinotto, R.; Mayzaud, P.; Nichols, Pd Marine Ecology Progress Series, Vol. 330 https://doi.org/10.3354/meps330001	journal	January 2007
Mass deposition event of Pyrosoma atlanticum carcasses off Ivory Coast (West Africa) Lebrato, M.; Jones, D. O. B. Limnology and Oceanography, Vol. 54, Issue 4 https://doi.org/10.4319/lo.2009.54.4.1197	journal	May 2009
An unusual bloom of the tunicate, Pyrosoma atlanticum , in southern Taiwan Kuo, Chao-Yang; Fan, Tung-Yung; Li, Hsing-Hui Bulletin of Marine Science, Vol. 91, Issue 3 https://doi.org/10.5343/bms.2014.1090	journal	July 2015
Luciferin production and luciferase transcription in the bioluminescent copepod Metridia lucens Tessler, Michael; Gaffney, Jean P.; Crawford, Jason M. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5506	journal	January 2018

Similar Records

Luciferase of the Japanese syllid polychaete Odontosyllis umdecimdonta

Journal Article · 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23105739

Kotlobay, Alexey A.; Ziganshin, Rustam; Bannikov, Artyom; +2 more

Brominated Luciferins Are Versatile Bioluminescent Probes

Journal Article · 2016 · ChemBioChem: a European journal of chemical biology · OSTI ID:1423816

Steinhardt, Rachel C.; Rathbun, Colin M.; Krull, Brandon T.; +8 more

Energy transfer protein in coelenterate bioluminescence

Journal Article · 1978 · J. Biol. Chem.; (United States) · OSTI ID:5099673

Ward, W W; Cormier, M J

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: A putative chordate luciferase from a cosmopolitan tunicate indicates convergent bioluminescence evolution across phyla

Citation Formats

References (47)

Similar Records

Related Subjects