The genomic basis of electrotaxis in Dictyostelium discoideum: Electric field sensitive amino acids are dynamically encoded en masse for the streaming-stage proteome

Abstract

Electrotaxis plays a critical role in developmental cell migration, axon growth cone guidance, epithelial wound healing, tissue regeneration, and the degree of invasiveness characterizing different cancer cell lines. During electrotaxis in a direct current electric field (EF), a cell migrates preferentially either towards the anode or cathode depending on the cell-type. However, the types and ranges of mechanisms coupling trans-cellular electric fields to cellular EF-sensitive signaling systems are largely unknown. To address this cell biological phenomenon, I use transcriptomic data from a developmental genetic model in which multicellular social aggregation is induced by starvation of amoeboid cells. I find that the developmental proteome expressed during the streaming aggregation stage is measurably and substantially enriched in charged and highly polar amino acids relative to the proteomes of either the unicellular amoeboid or the multicellular fruiting body. This large-scale coding augmentation of EF-sensitive amino acid residues in thousands of streaming-specific proteins is accompanied by a proportional coding decrease in the number of small, uncharged amino acid residues. I also confirm an expected coding increase of biosynthetically costly amino acids in the proteome of the satiated feeding-stage amoeboid. These findings suggest that electrotactic capability is encoded broadly in the genetically regulated deployment of a developmental proteome with augmented EF-sensitivity. These results signify that extreme, nonuniform, evolutionary constraints can be exerted on the amino acid composition of an organisms proteome.