Observation of coherent oscillations in the two-dimensional electronic spectra of photosynthetic proteins has led researchers to ask whether non-trivial quantum phenomena are biologically significant. Coherent oscillations have been reported for the soluble light harvesting phycobiliprotein (PBP) antenna isolated from cryptophyte algae. To probe the link between spectral properties and protein structure, we determined crystal structures of seven PBP light harvesting complexes isolated from different species. Each PBP is a dimer of αβ subunits where the structure of the αβ monomer is conserved, however, we discovered two dramatically distinct quaternary conformations, one that is specific to the genus Hemiselmis. Owing to steric effects emerging from a single amino acid insertion, the two αβ monomers are rotated by ~73° to an “open” configuration in contrast to the “closed” configuration of other cryptophyte PBPs. This structural change is significant for the light harvesting function because it disrupts the strong excitonic coupling between two central chromophores. 2D ES show marked cross-peak oscillations assigned to electronic and vibrational coherences in the case of the closed form. However, such features appear reduced, or absent, for open structures. Therefore cryptophytes have evolved a structural switch controlled by an amino acid insertion to modulate excitonic interactions and hence light harvesting.