Five members of the GH57 family of hyperthermophile archaeal glucanotransferases have thus far been described. We focus here upon PfuAmyGT (PF0272 from Pyrococcus furiosus), TonAmyGT (B6YUX8 from Thermococcus onnurenius) and TliAmyGT, also known as TLGT (O32462 from Thermococcus litoralis). All three proteins have polypeptide chains that are approximately 665 residues long, and folded into 3 domains assembled into a ‘head-to-tail’ homodimer. Domain 1 is a beta/alpha barrel, domain 2 is purely helical and domain 3 contains only beta sheets. Domain 1 has been thought to be involved in catalysis, while domains 2 and 3 have been thought to be domains of unknown function (DUFs). However, with PfuAmyGT, we have very recently elevated DUF domains 2 and 3 to the status of domains carrying out definite functions. We have shown that the glucose excised by domain 1 (from a donor malto-oligosaccharide bound inside a tunnel in the same domain) is transferred to an acceptor malto-oligosaccharide bound to a separate, second binding site (SBS) for glucans present upon the surface of domain 3 (at its interface with domain 2), using a loop that is present within domain 2. In this paper, we establish that without the presence of domain 3, there is no glucanotransferase activity in either an autonomously-folded form of domain 1, or a fusion of domains 1 and 2. However, upon creation of six different chimeras consisting of recombinant fusions of domains 1, 2 and 3, derived from either PfuAmyGT, or TonAmyGT, all six chimeras display glucanotransferase activity. Unexpectedly, the identity of domain 3 is the primary determinant of the glucan preferred to be used as a donor during glucan transfer, in these chimeras.