We report a hybrid, coarse-grained and atomistic, molecular dynamics simulation study of the size, motion, and function of the SecY protein-conducting channel. Growing and pushing virtual soft ball constructs through the pore of SecY, we mimic the push-through of polypeptides, performed cotranslationally by the ribosome and posttranslationally by the SecA ATPase. Forced lateral opening of a "front gate" between transmembrane helices is also induced by the passage of the virtual probes, with implications for the membrane insertion of peptides. We conclude that the SecY channel can stretch to allow passage of peptides with transversal sizes of approximately 16 A. The observed motion of a transmembrane helical "plug" controlling the closed and open states of the channel is consistent with experimental results and confirms previous hypotheses. Additionally, the "hinge" region for front gate opening is observed to be highly mobile as postulated. Both the forced dilation of a "ring" of residues at the middle of the pore and the lateral opening of the front gate are shown to induce plug displacement, but neither accomplish a full-extent motion of the plug to the back of the channel. For probes whose passage does not destroy the resilience of the SecY, both lateral exit and full translocation are observed, despite the fact that applied forces were always in the direction along the pore axis. Lateral exit is accompanied by front gate opening and slight plug displacement, whereas full translocation is accompanied by large plug displacement but no apparent lateral opening. Simulations also reveal that dilating the pore ring is a more effective way to destabilize the plug than intercalation of a cylinder-like probe at the front gate. Based on the simulations, the existence of a family of diverse open states is proposed.