Synaptotagmin-1 functions as a Ca²⁺ sensor in neurotransmitter release through its two C₂ domains (the C₂A and C₂B domain). The ability of synaptotagmin-1 to bridge two membranes is likely crucial for its function, enabling cooperation with the soluble N-ethylmaleimide sensitive factor adaptor protein receptors (SNAREs) in membrane fusion, but two bridging mechanisms have been proposed. A highly soluble synaptotagmin-1 fragment containing both domains (C₂AB) was shown to bind simultaneously to two membranes via the Ca²⁺-binding loops at the top of both domains and basic residues at the bottom of the C₂B domain (direct bridging mechanism). In contrast, a longer fragment including a linker sequence (lnC₂AB) was found to aggregate in solution and was proposed to bridge membranes through trans interactions between lnC₂AB oligomers bound to each membrane via the Ca²⁺-binding loops, with no contact of the bottom of the C₂B domain with the membranes. We now show that lnC₂AB containing impurities indeed aggregates in solution, but properly purified lnC₂AB is highly soluble. Moreover, cryo-EM images reveal that a majority of lnC₂AB molecules bridge membranes directly. Fluorescence spectroscopy indicates that the bottom of the C₂B domain contacts the membrane in a sizeable population of molecules of both membrane-bound C₂AB and membrane-bound lnC₂AB. NMR data on nanodiscs show that a fraction of C₂AB molecules bind to membranes with antiparallel orientations of the C₂ domains. Together with previous studies, these results show that direct bridging constitutes the prevalent mechanism of membrane bridging by both C₂AB and lnC₂AB, suggesting that this mechanism underlies the function of synaptotagmin-1 in neurotransmitter release.