Functional and evolutionary implications of the distribution of phosphagens in primitive-type spermatozoa

External fertilization is considered to be the primitive condition in metaz oans. The spermatozoa of such organisms typically display a common primitiv e-type morphology that is present in a range of phyla. These spermatozoa ar e extremely polarized cells in that the site of ATP synthesis (mitochondria in midpiece) is located at large diffusion distances from the ATP sink (dy nein ATPases in the flagellum). Spermatozoa of polychaetes, sipunculids, ec hiuroids, echinoderms, and tunicates contain the phosphagen creatine phosph ate or express the corresponding phosphagen kinase creatine kinase(or both) , even when other phosphagens/phosphagen kinases are present in somatic tis sues and eggs. The selective expression of the creatine kinase system in th ese sperma tozoa may be related to potential advantages in the cellular tra nsport of energy. To evaluate this possibility, we compared the efficacy of the major phosphagen systems for cellular transport of energy. We used a f acilitated diffusion model for spatial ATP buffering, taking into account r elative differences in diffusivity and thermodynamic poise. At low ratios o f [total phosphagen pool]/ [total adenine nucleotide pool] (CG+P/C-Ad ratio ), creatine phosphate carried a higher fraction of total high-energy phosph ate (J) than the other phosphagens. However, J values for all phosphagens w ere greater than 0.9, and these differences disappeared as the CG+P/C-Ad ra tio was increased. Thus, the functional benefit of using CP, rather than ot her phosphagens, in energy transport is quite limited. The creatine kinase system became associated with primitive-type spermatozoa early in metazoan evolution. This association is not necessarily related to inherent advantag es of this phosphagen system for buffering of ATP, but may be linked to his torical events in the evolution of the cell phenotype.