Evolution of the diverse array of phosphagen systems present in annelids

• Published in: Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2009, Vol.152 (1), p.60-66
• Main Authors: Suzuki, Tomohiko, Uda, Kouji, Adachi, Masamitsu, Sanada, Hiroshi, Tanaka, Kumiko, Mizuta, Chisa, Ishida, Keiko, Ellington, W. Ross
• Format: Article
• Language: English
• Subjects: Animals; Annelida - enzymology; Annelids; Arginine kinase; Creatine kinase; Creatine Kinase - genetics; Cytoplasm - enzymology; Evolution, Molecular; Exons; Glycocyamine kinase; Introns; Lombricine kinase; Mitochondrial Proteins; Phosphotransferases (Nitrogenous Group Acceptor) - genetics; Protein Isoforms - genetics; Substrate Specificity; Taurocyamine kinase
• ISSN: 1096-4959; 1879-1107
• DOI: 10.1016/j.cbpb.2008.09.087

Annelids as a group express a variety of phosphagen kinases including creatine kinase (CK), glyocyamine kinase (GK), lombricine kinase (LK), taurocyamine kinase (TK) and a unique arginine kinase (AK) restricted to annelids. In prior work, we have determined and compared the intron/exon organization of the annelid genes for cytoplasmic GK, LK, AK, and mitochondrial TK and LK (MiTK and MiLK, respectively), and found that these annelid genes, irrespective of cytoplasmic or mitochondrial, have the same 8-intron/9-exon organization strikingly similar to mitochondrial CK (MiCK) genes. These results support the view that the MiCK gene is basal and ancestral to the phosphagen kinases unique to annelids. To gain a greater understanding of the evolutionary processes leading to the diversity of annelid phosphagen kinases, we determined for the first time the intron/exon organization of a cytoplasmic CK gene from a polychaete as well as that of another polychaete MiCK gene. These gene structures, coupled with a phylogenetic analyses of annelid enzymes and assessment of the fidelity of substrate specificity of some these phosphagen kinases, provide insight into the pattern of radiation of the annelid enzymes. Annelid phosphagen kinases appeared to have diverged in the following order (earliest first): (1) cytoplasmic AK, LK and TK, (2) GK, and (3) mitochondrial MiLK and MiTK. Interestingly, phylogenetic analyses showed that the above phosphagen kinases appear to be basal to all CK isoforms (mitochondrial, cytoplasmic and flagellar CKs). This somewhat paradoxical placement of CKs most likely reflects a higher rate of evolution and radiation of the annelid-specific LK, TK and GK genes than the CK isoform genes.