Advertisement

The Protein Journal

, Volume 36, Issue 6, pp 502–512 | Cite as

Arginine Kinases from the Precious Corals Corallium rubrum and Paracorallium japonicum: Presence of Two Distinct Arginine Kinase Gene Lineages in Cnidarians

  • Tomoka Matsuo
  • Daichi Yano
  • Kouji Uda
  • Nozomu Iwasaki
  • Tomohiko Suzuki
Article

Abstract

The cDNA sequence of arginine kinase (AK) from the precious coral Corallium rubrum was assembled from transcriptome sequence data, and the deduced amino acid sequence of 364 residues was shown to conserve the structural features characteristic of AK. Based on the amino acid sequence, the DNA coding C. rubrum AK was synthesized by overlap extension PCR to prepare the recombinant enzyme. The following kinetic parameters were determined for the C. rubrum enzyme: K a Arg (0.10 mM), K ia Arg (0.79 mM), K a ATP (0.23 mM), K ia ATP (2.16 mM), and k cat (74.3 s−1). These are comparable with the kinetic parameters of other AKs. However, phylogenetic analysis suggested that the C. rubrum AK sequence has a distinct origin from that of other known cnidarian AKs with unusual two-domain structure. Using oligomers designed from the sequence of C. rubrum AK, the coding region of genomic DNA of another coral Paracorallium japonicum AK was successfully amplified. Although the nucleotide sequences differed between the two AKs at 14 positions in the coding region, all involved synonymous substitutions, giving the identical amino acid sequence. The P. japonicum AK gene contained one intron at a unique position compared with other cnidarian AK genes. Together with the observations from phylogenetic analysis, the comparison of exon/intron organization supports the idea that two distinct AK gene lineages are present in cnidarians. The difference in the nucleotide sequence between the coding regions of C. rubrum and P. japonicum AKs was 1.28%, which is twice that (0.54%) of mitochondrial DNA, is consistent with the general observation that the mitochondrial genome evolves slower than the nuclear one in cnidarians.

Keywords

Phosphagen kinase Arginine kinase Kinetic parameter Corallium rubrum Paracorallium japonicum 

Abbreviations

AK

Arginine kinase

CK

Creatine kinase

SRA

Sequence read archive

Notes

Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology, Japan to TS (15K07151) and NI (17K07274).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Bayer FM, Cairns SD (2003) A new genus of the scleraxonian family Coralliidae (Octocorallia: Gorgonacea). Proc Biol Soc Wash 116:222–228Google Scholar
  2. 2.
    Iwasaki N, Suzuki T (2010) Biology of precious coral. In: Iwasaki N (ed) Biohistory of precious coral. Tokai University Press, Tokyo, pp 3–25Google Scholar
  3. 3.
    Simpson A, Watling L (2011) Precious corals (Family Coralliidae) from Northwestern Atlantic Seamounts. J Mar Biol Assoc UK 91:369–382CrossRefGoogle Scholar
  4. 4.
    Iwasaki N, Fujita T, Bavestrello G, Cattaneo-Vietti R (2012) Morphometry and population structure of non-harvested and harvested populations of the Japanese red coral (Paracorallium japonicum) off Amami Island, southern Japan. Mar Fresh Res 63:468–474CrossRefGoogle Scholar
  5. 5.
    Nonaka M, Mizuk K, Iwasaki N (2012) Descriptions of two new species and designation of three neotypes of Japanese Coralliidae from recently discovered specimens that were collected by Kishinouye, and the introduction of a statistical approach to sclerite abundance and size. Zootaxa 3428:1–67Google Scholar
  6. 6.
    Kishinouye K (1903) Preliminary note on the Coralliidae of Japan. Zool Anz 26:623–626Google Scholar
  7. 7.
    Seki K (1991) Study of precious coral diver survey with open circuit air SCUBA diving at 108 m. Ann Physiol Anthropol 10:89–192CrossRefGoogle Scholar
  8. 8.
    Tsounis G, Rossi S, Gili JM, Arntz W (2006) Population structure of an exploited benthic cnidarian: the case study of red coral (Corallium rubrum L.). Marine Biol 149:1059–1070CrossRefGoogle Scholar
  9. 9.
    Cattaneo-Vietti R, Bavestrello G (2010) Sustainable use and conservation of precious coral in the Mediterranean. In: Iwasaki N (ed) Biohistory of precious coral. Tokai University Press, Tokyo, pp 3–25Google Scholar
  10. 10.
    Chang SK, Yang YC, Iwasaki N (2013) Whether to employ trade controls or fisheries management to conserve precious corals (Coralliidae) in the Northern Pacific Ocean. Mar Policy 39:144–153CrossRefGoogle Scholar
  11. 11.
    Pratlong M, Haguenauer A, Chabrol O, Klopp C, Pontarotti P, Aurelle D (2015) The red coral (Corallium rubrum) transcriptome: a new resource for population genetics and local adaptation studies. Mol Ecol Resour 15:1205–1215CrossRefGoogle Scholar
  12. 12.
    Uda K, Komeda Y, Koyama H, Koga K, Fujita T, Iwasaki N, Suzuki T (2011) Complete mitochondrial genomes of two Japanese precious corals, Paracorallium japonicum and Corallium konojoi (Cnidaria, Octocorallia, Coralliidae): notable differences in gene arrangement. Gene 476:27–37CrossRefGoogle Scholar
  13. 13.
    Uda K, Komeda Y, Fujita T, Iwasaki N, Bavestrello G, Giovine M, Cattaneo-Vietti R, Suzuki T (2013) Complete mitochondrial genomes of the Japanese pink coral (Corallium elatius) and the Mediterranean red coral (Corallium rubrum): a reevaluation of the phylogeny of the family Coralliidae based on molecular data. Comp Biochem Physiol D 8:209–219Google Scholar
  14. 14.
    Tu T-H, Dai C-F, Jeng M-S (2015) Phylogeny and systematics of deep-sea precious corals (Anthozoa: Octocorallia: Coralliidae). Mol Phylogenet Evol 84:173–184CrossRefGoogle Scholar
  15. 15.
    Robin Y (1974) Phosphagens and molecular evolution in worms. Biosystems 6:255–269CrossRefGoogle Scholar
  16. 16.
    Morrison JF (1973) Arginine kinase and other invertebrate guanidino kinases. In: Boyer PC (ed) The enzymes. Academic Press, New York, pp 457–486Google Scholar
  17. 17.
    Ellington WR (2001) Evolution and physiological roles of phosphagen systems. Annu Rev Physiol 63:289–325CrossRefGoogle Scholar
  18. 18.
    Uda K, Fujimoto N, Akiyama Y, Mizuta K, Tanaka K, Ellington WR, Suzuki T (2006) Evolution of the arginine kinase gene family. Comp Biochem Physiol D 1:209–218Google Scholar
  19. 19.
    Ellington WR, Suzuki T (2006) Evolution and divergence of creatine kinases. In: Vial C (ed) Molecular anatomy and physiology of proteins—creatine kinase. NovaScience, New York, pp 1–26Google Scholar
  20. 20.
    Andrews LD, Graham J, Snider MJ, Fraga D (2008) Characterization of a novel bacterial arginine kinase from Desulfotalea psychrophila. Comp Biochem Physiol B 150:312–319CrossRefGoogle Scholar
  21. 21.
    Suzuki T, Soga S, Inoue M, Uda K (2013) Characterization and origin of bacterial arginine kinases. Int J Biol Macromol 57:273–277CrossRefGoogle Scholar
  22. 22.
    Suzuki T, Kawasaki Y, Furukohri T (1997) Evolution of phosphagen kinase. Isolation, characterization and cDNA-derived amino acid sequence of two-domain arginine kinase from the sea anemone Anthopleura japonicus. Biochem J 328:301–306CrossRefGoogle Scholar
  23. 23.
    Suzuki T, Yamamoto Y (2000) Gene structure of two-domain arginine kinases from Anthopleura japonicus and Pseudocardium sachalinensis. Comp Biochem Physiol B 127:513–518CrossRefGoogle Scholar
  24. 24.
    Tada H, Nishimura Y, Suzuki T (2008) Cooperativity in the two-domain arginine kinase from the sea anemone Anthopleura japonicus. Int J Biol Macromol 42:46–51CrossRefGoogle Scholar
  25. 25.
    Tada H, Suzuki T (2010) Cooperativity in the two-domain arginine kinase from the sea anemone Anthopleura japonicus. II. Evidence from site-directed mutagenesis studies. Int J Biol Macromol 47:250–254CrossRefGoogle Scholar
  26. 26.
    Uda K, Ellington WR, Suzuki T (2012) A diverse array of creatine kinase and arginine kinase isoform genes is present in the starlet sea anemone Nematostella vectensis, a cnidarian model system for studying developmental evolution. Gene 497:214–227CrossRefGoogle Scholar
  27. 27.
    Hoover DM, Lubkowski J (2002) DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res 30:e43CrossRefGoogle Scholar
  28. 28.
    Ellington WR (1989) Phosphocreatine represents a thermodynamic and functional improvement over other muscle phosphagens. J Exp Biol 143:177–194Google Scholar
  29. 29.
    Morrison JF, James E (1965) The mechanism of the reaction catalyzed by adenosine triphosphate–creatine phosphotransferase. Biochem J 97:37–52CrossRefGoogle Scholar
  30. 30.
    Cleland WW (1979) Statistical analysis of enzyme kinetic data. Methods Enzymol 63:103–138CrossRefGoogle Scholar
  31. 31.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  32. 32.
    Zhou G, Somasundaram T, Blanc E, Parthasarathy G, Ellington WR, Chapman MS (1998) Transition state structure of arginine kinase: implications for catalysis of bimolecular reactions. Proc Natl Acad Sci USA 95:8449–8454CrossRefGoogle Scholar
  33. 33.
    Suzuki T, Fukuta H, Nagato H, Umekawa M (2000) Arginine kinase from Nautilus pompilius, a living fossil. Site-directed mutagenesis studies on the role of amino acid residues in GS (guanidino specificity) region. J Biol Chem 275:23884–23890CrossRefGoogle Scholar
  34. 34.
    Edmiston PL, Schavolt KL, Kersteen EA, Moore NR, Borders CL (2001) Creatine kinase: a role for arginine-95 in creatine binding and active site organization. Biochim Biophys Acta 1546:291–298CrossRefGoogle Scholar
  35. 35.
    Tanaka K, Suzuki T (2004) Role of amino acid residue 95 in substrate specificity of phosphagen kinases. FEBS Lett 573:78–82CrossRefGoogle Scholar
  36. 36.
    Yano D, Suzuki T, Hirokawa S, Fuke K, Suzuki T (2017) Characterization of four arginine kinases in the ciliate Paramecium tetraurelia: investigation on the substrate inhibition mechanism. Int J Biol Macromol 101:653–659CrossRefGoogle Scholar
  37. 37.
    Michibata J, Okazaki N, Motomura S, Uda K, Fujiwara S, Suzuki T (2014) Two arginine kinases of Tetrahymena pyriformis: characterization and localization. Comp Biochem Physiol B 171:34–41CrossRefGoogle Scholar
  38. 38.
    Suzuki T, Kanou Y (2014) Two distinct arginine kinases in Neocaridina denticulata: psychrophilic and mesophilic enzymes. Int J Biol Macromol 67:433–438CrossRefGoogle Scholar
  39. 39.
    Wu QY, Li F, Zhu WJ, Wang XY (2007) Cloning, expression, purification, and characterization of arginine kinase from Locusta migratoria manilensis. Comp Biochem Physiol B 148:355–362CrossRefGoogle Scholar
  40. 40.
    Yano D, Mimura S, Uda K, Suzuki T (2016) Arginine kinase from Myzostoma cirriferum, a basal member of annelids. Comp Biochem Physiol B 198:73–78CrossRefGoogle Scholar
  41. 41.
    Fujimoto N, Tanaka K, Suzuki T (2005) Amino acid residues 62 and 193 play the key role in regulating the synergism of substrate binding in oyster arginine kinase. FEBS Lett 579:1688–1692CrossRefGoogle Scholar
  42. 42.
    Engel PC (1992) Specificity constants in the context of protein engineering of two-substrate enzymes. Biochem J 284:604–605CrossRefGoogle Scholar
  43. 43.
    Cornish-Bowden A (1993) Enzyme specificity in reactions of more than one co-substrate. Biochem J 291:323–324CrossRefGoogle Scholar
  44. 44.
    Conejo M, Bertin M, Pomponi SA, Ellington WR (2008) The early evolution of thephosphagen kinases–insights from choanoflagellate and poriferan arginine kinases. J Mol Evol 66:11–20CrossRefGoogle Scholar
  45. 45.
    Naito Y, Riggs CK, Vandergon TL, Riggs AF (1991) Origin of a “bridge” intron in the gene for a two-domain globin. Proc Natl Acad Sci USA 88:6672–6676CrossRefGoogle Scholar
  46. 46.
    Suzuki T, Kawasaki Y, Unemi Y, Nishimura Y, Soga T, Kamidochi K, Yazawa Y, Furukohri T (1998) Gene duplication and fusion have occurred frequently in the evolution of phosphagen kinases—a two-domain arginine kinase from the clam Pseudocardium sachalinensis. Biochim Biophys Acta 1388:253–259CrossRefGoogle Scholar
  47. 47.
    Shearer TL, van Oppen MJ, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Tomoka Matsuo
    • 1
  • Daichi Yano
    • 1
  • Kouji Uda
    • 1
  • Nozomu Iwasaki
    • 2
  • Tomohiko Suzuki
    • 1
  1. 1.Laboratory of Biochemistry, Faculty of Science and TechnologyKochi UniversityKochiJapan
  2. 2.Faculty of Geo-Environment ScienceRissho UniversityKumagayaJapan

Personalised recommendations