We have investigated the adaptation of the light-harvesting system of the photosynthetic bacterium Phaeospirillum molischianum (DSM120) to very low light conditions. This strain is able to respond to changing light conditions by differentially modulating the expression of a family of puc operons that encode for peripheral light-harvesting complex (LH2) polypeptides. This modulation can result in a complete shift between the production of LH2 complexes absorbing maximally near 850 nm to those absorbing near 820 nm. In contradiction to prevailing wisdom, analysis of the LH2 rings found in the photosynthetic membranes during light adaptation are shown to have intermediate spectral and electrostatic properties. By chemical cross-linking and mass-spectrometry we show that individual LH2 rings and subunits can contain a mixture of polypeptides derived from the different operons. These observations show that polypeptide synthesis and insertion into the membrane are not strongly coupled to LH2 assembly. We show that the light-harvesting complexes resulting from this mixing could be important in maintaining photosynthetic efficiency during adaptation.