Functional and Evolutionary Implications of the Distribution of Phosphagens in Primitive-Type Spermatozoa.

Abstract

External fertilization is considered to be the primitive condition in metazoans. The spermatozoa of such organisms typically display a common primitive-type morphology that is present in a range of phyla. These spermatozoa are extremely polarized cells in that the site of ATP synthesis (mitochondria in midpiece) is located at large diffusion distances from the ATP sink (dynein ATPases in the flagellum). Spermatozoa of polychaetes, sipunculids, echiuroids, echinoderms, and tunicates contain the phosphagen creatine phosphate or express the corresponding phosphagen kinase creatine kinase (or both), even when other phosphagens/phosphagen kinases are present in somatic tissues and eggs. The selective expression of the creatine kinase system in these spermatozoa may be related to potential advantages in the cellular transport of energy. To evaluate this possibility, we compared the efficacy of the major phosphagen systems for cellular transport of energy. We used a facilitated diffusion model for spatial ATP buffering, taking into account relative differences in diffusivity and thermodynamic poise. At low ratios of [total phosphagen pool]/ [total adenine nucleotide pool] (CG+P/CAd ratio), creatine phosphate carried a higher fraction of total high-energy phosphate (J) than the other phosphagens. However, J values for all phosphagens were greater than 0.9, and these differences disappeared as the CG+P/CAd ratio was increased. Thus, the functional benefit of using CP, rather than other 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 advantages of this phosphagen system for buffering of ATP, but may be linked to historical events in the evolution of the cell phenotype.