YnaI exemplifies the diversity of structural gating mechanisms in mechanosensitive channels of small conductance

Osmotically varying environments are challenging for bacterial cells. Sudden drops in osmolytes cause an increased membrane tension and rupture the cells in the absence of protective mechanisms. One family of protective proteins are mechanosensitive channels of small conductance that open in response to membrane tension. Although these channels have a common architecture, they vary widely in the number of transmembrane helices, conductivity, and gating characteristics. Despite of several structures of channels in the open and closed state, the underlying common principles of the gating mechanism are not well understood. Here we show that YnaI opens by radial relocation of the transmembrane sensor paddles together with a shortening of the pore. This contrasts the prototypic smaller MscS which tilts the sensor paddles and retains the pore length. A chimera of both channels with the YnaI sensor paddles and the pore containing C-terminal part of MscS has the conductivity of the pore donor and the tension response of the paddle donor together with the conformational changes of the respective donor. Our research shows that elements with different types of structural rearrangements can be mixed and matched within one channel as long as they support the common area expansion on the periplasmic side.