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The molecular underpinnings of synaptic vesicle fusion for fast neurotransmitter release are still unclear. Here, we used a single vesicle–vesicle system with reconstituted SNARE and synaptotagmin-1 proteoliposomes to decipher the temporal sequence of membrane states upon Ca 2+ -injection at 250–500 μM on a 100-ms timescale. Furthermore, detailed membrane morphologies were imaged with cryo-electron microscopy before and after Ca 2+ -injection. We discovered a heterogeneous network of immediate and delayed fusion pathways. Remarkably, all instances of Ca 2+ -triggered immediate fusion started from a membrane–membrane point-contact and proceeded to complete fusion without discernible hemifusion intermediates. In contrast, pathways that involved a stable hemifusion diaphragm only resulted in fusion after many seconds, if at all. When complexin was included, the Ca 2+ -triggered fusion network shifted towards the immediate pathway, effectively synchronizing fusion, especially at lower Ca 2+ -concentration. Synaptic proteins may have evolved to select this immediate pathway out of a heterogeneous network of possible membrane fusion pathways.

Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion