Mechanotransduction of hair bundles arising from multicellular complexes in anemones

Sea anemones are among the simplest animals to use hair bundles to detect vibrations. Although we previously found anemone bundles to be morphologically similar to vertebrate hair bundles, only indirect evidence implicated anemone bundles in mechanotransduction. Here, we test mechanotransduction of these bundles using loose-patch current recording from apical membranes of cells at the base of deflected bundles. Step bundle deflection results in graded membrane currents that are inward in some cells (positive) and outward in other cells (negative). Positive responses range from 5 to 30 pA, abruptly saturate with stronger stimuli, and increase in duration with prolonged deflections. Negative responses range from 10 to 150 pA, show a logarithmic relation to stimulus strength, and attenuate with prolonged deflections. Additionally, responses are reversibly inhibited by streptomycin. We present a model for anemone bundle mechanotransduction modified from the gating spring model for vertebrate mechanotransduction. Because anemone bundles comprise stereocilia arising from a multicellular complex, we propose that supporting cells on opposite sides of a bundle function as oppositely polarized hair cells. Thus, deflection induces ion channels to open in cells on one side of the complex, while allowing channels to close in cells on the opposite side of the complex.