An organelle K+ channel is required for osmoregulation in Chlamydomonas reinhardtii

Abstract

Fresh water protozoa and algae face hypotonic challenges in their living environment. Many of them employ a contractile vacuole (CV) system to uptake excessive water from the cytoplasm and expel it to the environment to achieve cellular homeostasis. Potassium, a major osmolyte in CV, is predicted to create higher osmolarity for water influx. Molecular mechanisms for K+ permeation through plasma membrane have been well studied. How K+ permeates organelles such as CV is not clear. Here, we show that a six-transmembrane K+ channel KCN11 in Chlamydomonas is exclusively localized to CV. Ectopic expression of KCN11 in HEK293T cells results in voltage-gated K+ channel activity. Disruption of the gene or mutation of key residues for K+ permeability of the channel leads to dysfunction of cell osmoregulation in very hypotonic conditions. The contractile cycle is inhibited in the mutant cells with slower rate of CV swelling, leading to cell death. These data demonstrate a new role for six transmembrane potassium channels in the CV functioning and provide further insights into osmoregulation mediated by contractile vacuole.