An ancestral glutamate receptor mediates cell volume regulation during high K⁺ stress in cyanobacteria

Cyanobacteria, able to survive photoautotrophically in harsh environments, possess various ancestral homologs of ion transport systems found in eukaryotic cells. The model cyanobacterium, Synechocystis sp. PCC 6803, contains five K⁺ channels; however, their function and role have not been fully explained. This study determined the structure, function, and physiological role of an ancestral glutamate receptor, GluR0, in Synechocystis. Growth of a gluR0 mutant (ΔgluR0) increased under high KCl conditions. Subcellular fractionation showed that GluR0 was localized in the plasma membrane of Synechocystis, and expression of GluR0 enabled a K⁺ uptake-deficient Escherichia coli mutant to grow under low K⁺ conditions. The membrane topology of GluR0 was opposite to that of the canonical K⁺ channel but similar to that of the animal glutamate receptor. Microfluidic device-aided single-cell analysis that enabled instantaneous extracellular solution exchange revealed that after KCl upshock, the cell volume of ΔgluR0 decreased more rapidly than the wildtype. These data provide the first direct evidence that a prokaryotic glutamate receptor homolog with K⁺ channel activity plays a role in responding to rapid changes in the ionic environment. This function likely reflects a property of glutamate receptors that was acquired early on during evolution.