Sandercyanin is a mildly fluorescent biliprotein with a large Stokes shift, a tetrameric quaternary structure, and a biliverdin (BV) chromophore that does not covalently bond to the protein. To adapt this promising protein for use in bioimaging, it is necessary to produce monomeric mutants that retain the spectroscopic properties while increasing the fluorescence quantum yield. Modulating these properties through the protonation state of BV's propionic tails is a possible avenue, if detailed mechanistic information on the role of such chains becomes available. In this study, we use a microstate model for the titration process of BV and couple it with constant pH molecular dynamics to study protonation states in the apo protein, the artificial monomer, and the tetramer and identify shifts. Our results indicate that several residues might have a central role in oligomerization as a response to the presence of BV and especially to the protonation state of the propionic tails. While the absorption properties are not strongly impacted by the tails, their protonation state has an impact on the chromophore geometry, which likely influences the fluorescence.