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Evolution of the Cytoplasmic and Mitochondrial Phosphagen Kinases Unique to Annelid Groups

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Abstract

Creatine kinase (CK) is a member of a group of phosphoryl transfer enzymes called phosphagen kinases that play a key role in cellular energy transactions in animals. Three CK isoform gene families are known—cytoplasmic CK (CK), flagellar CK (fCK), and mitochondrial CK (MiCK). Each of the isoforms has a unique gene structure (intron/exon organization). A broad array of other phosphagen kinases is present in animals. Some of these enzymes are found only in annelids and closely related groups including glyocyamine kinase (GK), lombricine kinase (LK), taurocyamine kinase (TK), and a unique arginine kinase (AK) restricted to annelids. Phylogenetic analyses of these annelid phosphagen kinases indicate that they appear to have evolved from a CK-like ancestor. To gain a greater understanding of the relationship of the CK isoforms to the annelid enzymes, we have determined the intron/exon organization of the genes for the following phosphagen kinases: Eisenia LK, Sabellastarte AK, and Arenicola mitochondrial TK (MiTK). Analysis of genomic database for the polychaete Capitella sp. yielded two putative LK genes [cytoplasmic LK and mitochondrial LK (MiLK)]. The intron/exon organization of these genes was compared with available data for cytoplasmic and mitochondrial CKs, and an annelid GK. Surprisingly, these annelid genes, irrespective of whether they are cytoplasmic (LK, AK, and GK) or mitochondrial (MiTK and MiLK), had the same 8-intron/9-exon organization and were strikingly similar to MiCK genes sharing seven of eight splice junctions. These results support the view that the MiCK gene is basal and ancestral to the phosphagen kinases unique to annelids.

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Abbreviations

CK:

cytoplasmic creatine kinase

fCK:

flagellar creatine kinase

MiCK:

mitochondrial creatine kinase

TK:

cytoplasmic taurocyamine kinase

MiTK:

mitochondrial taurocyamine kinase

LK:

cytoplasmic lombricine kinase

MiLK:

mitochondrial lombricine kinase

GK:

glycocyamine kinase

AK:

arginine kinase

HTK:

hypotaurocyamine kinase

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Acknowledgments

We thank Daisuke Yamashita for his help at an early stage of this work. This work was supported by grant-in-aids for scientific research in Japan to T. S. (17570062) and by the US National Science Foundation grants IOB-0130024 and IOB-0542236 to W. R. E.

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Authors and Affiliations

  1. Laboratory of Biochemistry, Kochi University, Kochi, 780-8520, Japan

    Kumiko Tanaka, Kouji Uda, Mayumi Shimada, Ken-ichi Takahashi & Tomohiko Suzuki

  2. Department of Environment and Life Sciences, Kyorin University School of Health Science, Tokyo, 192-8505, Japan

    Shinobu Gamou

  3. Institute of Molecular Biophysics and Department of Biological Science, Florida State University, Tallahassee, Florida, 32306-4370, USA

    W. Ross Ellington

Authors
  1. Kumiko Tanaka
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  2. Kouji Uda
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  3. Mayumi Shimada
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  4. Ken-ichi Takahashi
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  5. Shinobu Gamou
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  6. W. Ross Ellington
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  7. Tomohiko Suzuki
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Correspondence to Tomohiko Suzuki.

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Tanaka, K., Uda, K., Shimada, M. et al. Evolution of the Cytoplasmic and Mitochondrial Phosphagen Kinases Unique to Annelid Groups. J Mol Evol 65, 616–625 (2007). https://doi.org/10.1007/s00239-007-9046-4

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  • DOI: https://doi.org/10.1007/s00239-007-9046-4

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