Low potential manganese ions as efficient electron donors in native anoxygenic bacteria

Area of Science:

• Biochemistry
• Photosynthesis research
• Bioinorganic chemistry

Background:

• Controlling molecular driving forces is key for understanding natural electron transfer and improving artificial energy conversion mimics.
• Oxygenic photosynthesis uses manganese ions as rapid electron donors, a feature potentially useful for studying anoxygenic photosynthesis evolution and water oxidation energetics.

Purpose of the Study:

• To develop environmental methods for tuning the redox potentials of manganese ions and photosynthetic enzyme cofactors without genetic modification.
• To investigate the potential of manganese coordination with bis-tris propane (BTP) as a model for evolutionary intermediates in biological water oxidation.

Main Methods:

• Utilized bis-tris propane (BTP) for spontaneous coordination with manganese ions.
• Investigated the binding of BTP-coordinated manganese to the bacterial reaction center of anoxygenic bacteria.
• Measured redox potentials of manganese and primary electron donors at pH 9.4.

Main Results:

• BTP coordination significantly lowered the manganese (II) to manganese (III) redox potential to ~400 mV at pH 9.4.
• Binding to a novel site in the reaction center elevated the primary electron donor's (bacteriochlorophyll dimer) redox potential by up to 92 mV.
• Facilitated electron transfer that outcompeted charge recombination, impairing the natural electron donor's function.

Conclusions:

• Bis-tris propane coordination offers an effective method to tune manganese redox potentials and facilitate electron transfer in anoxygenic photosynthesis.
• BTP-coordinated manganese serves as a viable model for evolutionary alternatives in biological water oxidation.
• This approach provides insights into the energetics of biological water oxidation and the evolution of photosynthetic systems.