Hair bundle motility induced by chemoreceptors in anemones

Most hair bundles are essentially fixed with respect to frequency specificity. However, hair bundles in sea anemones are dynamically tuned by actin-dependent changes in length. Tuning to low frequencies is accomplished by activation of chemoreceptors to N-acetylated sugars resulting in hair bundle elongation. We report here that following sugar-induced tuning of hair bundles, membrane currents reverse polarity in hair cells during unidirectional mechanical stimulation. Reversal in polarity of currents with sugar stimulation is inhibited if hair bundle elongation is blocked by pretreatment with cytochalasin D. A re-examination of morphological changes to hair bundles reveals a sugar-induced reorientation of stereocilia in addition to elongation with chemosensitization. In controls, hair bundles are noticeably twisted. With sugar stimulation stereocilia become oriented more parallel to the long axis of the hair bundle. This sugar-induced change in orientation is similarly inhibited by cytochalasin D pretreatment. Based on these results, we present a model wherein anemone hair bundle twisting serves as a built-in safety mechanism to preserve linkages likely to be subjected to potentially damaging tension during tuning. The twisted hair bundles can untwist while elongating to relieve excessive tension on extracellular linkages between stereocilia critical to mechanosensitivity.