The crystal structure of the Sup35 prion segment, GNNQQNY, revealed precise side chain packing and an extensive H-bond network. However, the conformers and stabilizing interactions involved at nascent amyloid formation are still unclear. Here, long molecular dynamics simulations and quantum mechanical calculations have been utilized to study the conformation and energetics of the initial structure that acts to nucleate further growth. Considering all the plausible intermediates that may act as stepping stones, we find that the initial nucleus is a twisted single-layer, three-stranded parallel beta-sheet. H-bonds between beta-strands in this twisted sheet, some of which differ from those of the crystal structure's nontwisted beta-strands, are key for the nucleus' formation and stability. High level theoretical calculations of these H-bonds' energetics can account for this amyloid-like trimer's remarkable stability. The intermeshing of facing sheets to form the dry interface provides less stability and would occur between two three-stranded beta-sheets without metastable water nanowires.