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Molecular recognition is central to biology and a critical aspect of RNA function. Yet structured RNAs typically lack the preorganization needed for strong binding and precise positioning. A striking example is the group I ribozyme from  Tetrahymena , which binds its guanosine substrate (G) orders of magnitude slower than diffusion. Binding of G is also thermodynamically coupled to binding of the oligonucleotide substrate (S) and further work has shown that the transition from E•G to E•S•G accompanies a conformational change that allows G to make the active site interactions required for catalysis. The group I ribozyme from  Azoarcus  has a similarly slow association rate but lacks the coupled binding observed for the  Tetrahymena  ribozyme. Here we test, using G analogs and metal ion rescue experiments, whether this absence of coupling arises from a higher degree of preorganization within the  Azoarcus  active site. Our results suggest that the  Azoarcus  ribozyme forms cognate catalytic metal ion interactions with G in the E•G complex, interactions that are absent in the  Tetrahymena  E•G complex. Thus, RNAs that share highly similar active site architectures and catalyze the same reactions can differ in the assembly of transition state interactions. More generally, an ability to readily access distinct local conformational states may have facilitated the evolutionary exploration needed to attain RNA machines that carry out complex, multi-step processes.

Differential Assembly of Catalytic Interactions within the Conserved Active Sites of Two Ribozymes