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Evolution of Bioluminescence in Marine Planktonic Copepods

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Evolution of Bioluminescence in Marine Planktonic Copepods Evolution of Bioluminescence in Marine Planktonic Copepods Yasuhiro Takenaka,*,1 Atsushi Yamaguchi,2 Naoki Tsuruoka,3 Masaki Torimura,4 Takashi Gojobori,5 and Yasushi Shigeri*,1 1Health Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ikeda, Osaka, Japan 2Faculty of Fisheries Science, Hokkaido University, Hakodate, Japan 3International Patent Organism Depositary (IPOD), National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan 4Research Institute for Environmental Management Technology, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan 5Laboratory for DNA Data Analysis, Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka, Japan *Corresponding author: E-mail: [email protected]; [email protected]. Associate editor: Adriana Briscoe Research article Abstract Copepods are the dominant taxa in zooplankton communities of the ocean worldwide. Although bioluminescence of Downloaded from certain copepods has been known for more than a 100 years, there is very limited information about the structure and evolutionary history of copepod luciferase genes. Here, we report the cDNA sequences of 11 copepod luciferases isolated from the superfamily Augaptiloidea in the order Calanoida. Highly conserved amino acid residues in two similar repeat sequences were confirmed by the multiple alignment of all known copepod luciferases. Copepod luciferases were classified into two groups of Metridinidae and Heterorhabdidae/Lucicutiidae families based on phylogenetic analyses, with http://mbe.oxfordjournals.org/ confirmation of the interrelationships within the Calanoida using 18S ribosomal DNA sequences. The large diversity in the specific activity of planktonic homogenates and copepod luciferases that we were able to express in mammalian cultured cells illustrates the importance of bioluminescence as a protective function against predators. We also discuss the relationship between the evolution of copepod bioluminescence and the aspects of their ecological characteristics, such as swimming activity and vertical habitat. Key words: copepoda, luciferase, zooplankton, crustacean, phylogenetic analysis. Introduction the superfamily, Augaptiloidea. Concerning bioluminescence at (D) Hokkaido U Med on May 15, 2012 behavior other than calanoid copepods, that of tiny pseudo- Copepods are the most numerous taxa of zooplankton fauna planktonic poecilostomatoid Oncaea spp. is only notable in the ocean worldwide. Their bioluminescent abilities and (Herring et al. 1993). One reason for the limited information characteristics have been investigated for over a 100 years (Giesbrecht 1895; Clarke et al. 1962; Haddock et al. 2010). on copepod bioluminescence is that correct copepod iden- Luminescence of calanoid copepods is produced by glandu- tification is very difficult. In addition to the species identifi- lar cells in the luminous glands, which are largely located on cation challenges, zooplankton sampling, especially in deep thecaudalramiandlegs(fig. 1), although their number and water, requires special equipment, including large-sized location vary considerably among families. Most of the lumi- plankton nets, to collect sufficient numbers of specimens. nous species reported to date belong to the superfamily Au- Furthermore, macro- and microscopic detection of weak gaptiloidea, which contains the families Arietellidae, and flash-type bioluminescence from tiny copepods is also Augaptilidae, Heterorhabdidae, Lucicutiidae, Metridinidae, difficult, especially if the specimen was damaged during the and Nullosetigeridae (Herring 1988). Within these families, collection or manipulation by an investigator. Therefore, a de- the luminescent behavior of Metridinidae and most Hetero- vice, such as a luminometer, to detect weak bioluminescence rhabdidae, Lucicutiidae, and Augaptilidae are well known of zooplankton is needed. (Herring 1988). Based on a previous cladistic analysis of mor- One strong piece of evidence for the presence of biolu- phological features, the Augaptiloidea is believed to have di- minescence in a particular organism is the molecular iden- verged very early in the evolution of calanoid copepods tification and functional analysis of luciferase, which is the (Bradford-Grieve et al. 2010). Except for the Augaptiloidea enzyme directly involved in producing luminescence in an superfamily, a single species in Megacalanoidea (Megacala- organism. In 2002, the luciferase gene was cloned from cal- nus princeps) was reported as luminous (Herring 1988) with anoid Gaussia princeps (family Metridinidae), which is a large very limited evidence, and it remains unverified. It is also un- (;10 mm) gray-black–pigmented copepod usually found in clear whether species in other superfamilies, such as Centro- the mesopelagic zone (at the depths from 200 to 1,000 m) pagoidea, Clausocalanoidea, and Eucalanoidea, are luminous. (Verhaegen and Christopoulos 2002). A novel feature of This indicates that among the ten calanoid superfamilies, Gaussia luciferase (GLuc) is its relatively small size (;20 bioluminescent copepods are found almost exclusively in kDa) and secreted luminescence, not only in planktonic © The Author 2012. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: [email protected] Mol. Biol. Evol. 29(6):1669–1681. 2012 doi:10.1093/molbev/mss009 Advance Access publication January 12, 2012 1669 Takenaka et al. · doi:10.1093/molbev/mss009 MBE a BFP filter pair (excitation at 387/28 nm, emission at 430 nm), and cooled CCD camera (VB-7010; Keyence). Luminescence Assay for Zooplankton Homogenate Frozen specimens were transferred into 150 llof20mM Tris–HCl (pH 8.0) with 10 mM MgCl2 and an appropriate amount of Complete Protease Inhibitor Cocktail (Roche Applied Science, Japan) and thoroughly homogenized in FIG.1.(A) Fluorescent microscopic image of bioluminescent Copepoda, Metridia pacifica, illuminated with ultraviolet. Arrow- a 1.5-ml microtube using a plastic pestle (As one, Japan). heads indicate the position of putative luminous glands on head. (B) The homogenate was centrifuged at 15,000 rpm for 5 min, Bright-field and fluorescent image of M. pacifica. Putative luminous and the supernatant was used for the luminescence assay glands were on the legs and abdomen adjacent to the head. and determination of protein concentration. Lumines- cence activity was measured by mixing 5 ll of zooplankton lysate and 10 llof1ng/ll coelenterazine in 20 mM Tris– expression but also when expressed in mammalian and in- HCl (pH 8.0), with 50 mM MgCl2, followed by 10 s of count- ing. Protein concentration was determined by the Bradford sect cells, with robust stability and great luminescent activity. Downloaded from GLuc catalyzes the oxidation of a luciferin called coelenter- method (Bradford 1976). azine to produce the light. Luciferase genes have also been Sequencing and Analyses of Zooplankton found in Metridia longa (MLuc) (Markova et al. 2004)and Ribosomal RNA Genes Metridia pacifica (MpLuc1 and MpLuc2) (Takenaka et al. Nuclear ribosomal RNA (rRNA) sequences were searched 2008), both of which belong to the Metridinidae family just and obtained from GenBank. If they were not available in http://mbe.oxfordjournals.org/ as G. princeps does. These GLuc-homologues also react with database, we cloned and sequenced as follows. The speci- the substrate coelenterazine to produce light. The biolumi- mens fixed in 100% ethanol were transferred into 200 llof nescence in these species was confirmed by identification Buffer ATL (DNeasy Tissue Kit; Qiagen, Japan) containing and functional analysis of their luciferases. 2 lg/ll of proteinase K and thoroughly homogenized in In this study, we isolated and characterized novel luciferase 1.5-ml microtubes using a plastic pestle (As one). Genomic genes from five species of calanoid copepods and conducted DNAwaspurifiedusingaDNeasyTissueKit(Qiagen,Japan) the quantitative analyses of copepod bioluminescence using according to the manufacturer’s instructions. The primers zooplankton homogenates and recombinant luciferases. By to amplify the 18S rRNA genes were 21F, 5#-ATCTGGTT- at (D) Hokkaido U Med on May 15, 2012 quantitative measurements, we could reveal the presence GATCCTGCCAGT-3# and 1778R, 5#-AATGATCCTTCCG- or absence of luminescence of unverified species with con- CAGGTTC-3#. The thermal cycling conditions for the firmation of verified ones. Furthermore, we compared the polymerase chain reaction (PCR) amplification were 98 °C luminous intensity of homogenates among calanoid super- for 2 min for denaturation, followed by 30 cycles of 98 °C families and those of luciferases among genera in Augaptiloi- for 10 s for denaturation, 52 °C for 15 s for annealing, and dea to infer the defensive function and molecular evolution 68 °C for 90 s for extension. PCR products were purified with of copepod bioluminescence. AMPure (Beckman Coulter, Japan), and both strands were Materials and Methods sequenced with the BigDye Terminator v3.1 Cycle Sequencing Kit using a 3130xl Genetic Analyzer (Applied Biosystems, Collection of the Copepods Japan) following the manufacturer’s instructions. The Zooplankton samples were collected with vertical tows of sequencing primers were used according to an earlier a closing net (60 cm mouth diameter, 100 lm mesh) from protocol (Kurtzman and Robnett 2003). The trimmed 18S
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