Cryptophytes are photosynthetic microalga that flourish in a remarkable diversity of natural environments by using pigment-containing proteins with absorption maxima tuned to each ecological niche. While this diversity in the absorption has been well established, the subsequent photophysics is highly sensitive to the local protein environment and so may exhibit similar variation. Thermal fluctuations of the protein conformation are expected to introduce photophysical heterogeneity of the pigments that may have evolved important functional properties in a manner similar to that of the absorption. However, such heterogeneity is averaged out in ensemble measurements and, therefore, has not yet been probed. Here, we report single-molecule measurements of phycoerythrin 545 (PE545), the prototypical cryptophyte antenna protein, in its native dimeric form. A conformational ensemble was resolved consisting of distinct photophysical states with different light-harvesting properties. Proteins that did not quench, partially quenched, or fully quenched absorbed light were observed. Light intensity increased the quenched-state population of the dimer, potentially as a mechanism to deal with the extreme light intensities found in aqueous environments. Cross-linking, which mimics local interactions, introduces this light-dependent functionality while also suppressing other conformational dynamics. The cellular organization can, therefore, actively modulate the protein conformation and dynamics, selecting for distinct levels of light harvesting. Thus, the complex conformational equilibrium provides an additional mechanism for cryptophytes and likely other photosynthetic organisms to optimize solar energy capture and conversion.