Kleptoprotein Bioluminescence: Fish Obtain Luciferase from Ostracod Prey

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2020 Jan 15

PMID 31934625

Citations 8

Authors

Manabu Bessho-Uehara

Naoyuki Yamamoto

Shuji Shigenobu

Hitoshi Mori

Keiko Kuwata

Yuichi Oba

Affiliations

Soon will be listed here.

Abstract

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 , 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 , a bioluminescent ostracod that they feed upon. Experiments where fish were fed with a related ostracod, , 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.

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References

Haneda Y, Johnson F . THE LUCIFERIN-LUCIFERASE REACTION IN A FISH, PARAPRIACANTHUS BERYCIFORMIS, OF NEWLY DISCOVERED LUMINESCENCE. Proc Natl Acad Sci U S A. 1958; 44(2):127-9. PMC: 335376. DOI: 10.1073/pnas.44.2.127. View

Lovmo S, Speth M, Repnik U, Koppang E, Griffiths G, Hildahl J . Translocation of nanoparticles and Mycobacterium marinum across the intestinal epithelium in zebrafish and the role of the mucosal immune system. Dev Comp Immunol. 2016; 67:508-518. DOI: 10.1016/j.dci.2016.06.016. View

Thacker C, Roje D . Phylogeny of cardinalfishes (Teleostei: Gobiiformes: Apogonidae) and the evolution of visceral bioluminescence. Mol Phylogenet Evol. 2009; 52(3):735-45. DOI: 10.1016/j.ympev.2009.05.017. View

Davis M, Sparks J, Smith W . Repeated and Widespread Evolution of Bioluminescence in Marine Fishes. PLoS One. 2016; 11(6):e0155154. PMC: 4898709. DOI: 10.1371/journal.pone.0155154. View

Thompson E, Nagata S, Tsuji F . Cloning and expression of cDNA for the luciferase from the marine ostracod Vargula hilgendorfii. Proc Natl Acad Sci U S A. 1989; 86(17):6567-71. PMC: 297885. DOI: 10.1073/pnas.86.17.6567. View

Morin J . Based on a review of the data, use of the term 'cypridinid' solves the Cypridina/Vargula dilemma for naming the constituents of the luminescent system of ostracods in the family Cypridinidae. Luminescence. 2009; 26(1):1-4. DOI: 10.1002/bio.1178. View

Oba Y, Furuhashi M, Bessho M, Sagawa S, Ikeya H, Inouye S . Bioluminescence of a firefly pupa: involvement of a luciferase isotype in the dim glow of pupae and eggs in the Japanese firefly, Luciola lateralis. Photochem Photobiol Sci. 2013; 12(5):854-63. DOI: 10.1039/c3pp25363e. View

Haddock S, Moline M, Case J . Bioluminescence in the sea. Ann Rev Mar Sci. 2010; 2:443-93. DOI: 10.1146/annurev-marine-120308-081028. View

Petschenka G, Agrawal A . Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc Biol Sci. 2015; 282(1818):20151865. PMC: 4650158. DOI: 10.1098/rspb.2015.1865. View

10.

Fuglem B, Jirillo E, Bjerkas I, Kiyono H, Nochi T, Yuki Y . Antigen-sampling cells in the salmonid intestinal epithelium. Dev Comp Immunol. 2010; 34(7):768-74. DOI: 10.1016/j.dci.2010.02.007. View

11.

Ratnasingham S, Hebert P . bold: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes. 2008; 7(3):355-364. PMC: 1890991. DOI: 10.1111/j.1471-8286.2007.01678.x. View

12.

Maeda T, Hirose E, Chikaraishi Y, Kawato M, Takishita K, Yoshida T . Algivore or phototroph? Plakobranchus ocellatus (Gastropoda) continuously acquires kleptoplasts and nutrition from multiple algal species in nature. PLoS One. 2012; 7(7):e42024. PMC: 3404988. DOI: 10.1371/journal.pone.0042024. View

13.

Johnson F, Sugiyama N, Shimomura O, Saiga Y, Haneda Y . Crystalline luciferin from a luminescent fish, Parapriacanthus beryciformes. Proc Natl Acad Sci U S A. 1961; 47:486-9. PMC: 221477. DOI: 10.1073/pnas.47.4.486. View

14.

Fu L, Niu B, Zhu Z, Wu S, Li W . CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012; 28(23):3150-2. PMC: 3516142. DOI: 10.1093/bioinformatics/bts565. View

15.

Haneda Y, Tsuji F, Sugiyama N . Luminescent systems in apogonid fishes from the Philippines. Science. 1969; 165(3889):188-90. DOI: 10.1126/science.165.3889.188. View

16.

Winchell C, Sullivan J, Cameron C, Swalla B, Mallatt J . Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol. 2002; 19(5):762-76. DOI: 10.1093/oxfordjournals.molbev.a004134. View

17.

Kishi Y, Matsuura S, Inoue S, Shimomura O, Goto T . Luciferin and luciopterin isolated from the Japanese firefly, Luciola cruciata. Tetrahedron Lett. 1968; (24):2847-50. DOI: 10.1016/s0040-4039(00)75644-9. View

18.

McELROY W, CHASE A . Purification of Cypridina luciferase. J Cell Comp Physiol. 1951; 38(3):401-8. DOI: 10.1002/jcp.1030380308. View

19.

Hase K, Kawano K, Nochi T, Pontes G, Fukuda S, Ebisawa M . Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature. 2009; 462(7270):226-30. DOI: 10.1038/nature08529. View

20.

Haddock S, Rivers T, Robison B . Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence. Proc Natl Acad Sci U S A. 2001; 98(20):11148-51. PMC: 58698. DOI: 10.1073/pnas.201329798. View