Undulating Free Energy Landscapes Buffer Redox Chains from Environmental Fluctuations.

Roller-coaster or undulating free energy landscapes, with alternating high and low potential cofactors, occur frequently in biological redox chains. Yet, there is little understanding of the possible advantages created by these landscapes. We examined the tetraheme subunit associated with reaction centers, comparing the dynamics of the native protein and of hypothetical (in silico) mutants. We computed the variation in the total number of electrons in wild type (WT) and mutant tetrahemes connected to an electron reservoir in the presence of a time-varying potential, as a model for a fluctuating redox environment. We found that roller-coaster free energy landscapes buffer the redox cofactor populations from these fluctuations. The WT roller-coaster landscape slows forward and backward electron transfer in the face of fluctuations, and may offer the advantage of sustaining the reduction of essential cofactors, such as the chlorophyll special pair in photosynthesis, even though an undulating landscape introduces thermodynamically uphill steps in multistep redox chains.