title: Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex.
abstract: Light-harvesting antenna complexes not only aid in the capture of solar energy for photosynthesis, but regulate the quantity of transferred energy as well. Light-harvesting regulation is important for protecting reaction center complexes from overexcitation, generation of reactive oxygen species, and metabolic overload. Usually, this regulation is controlled by the association of light-harvesting antennas with accessory quenchers such as carotenoids. One antenna complex, the Fenna-Matthews-Olson (FMO) antenna protein from green sulfur bacteria, completely lacks carotenoids and other known accessory quenchers. Nonetheless, the FMO protein is able to quench energy transfer in aerobic conditions effectively, indicating a previously unidentified type of regulatory mechanism. Through de novo sequencing MS, chemical modification, and mutagenesis, we have pinpointed the source of the quenching action to cysteine residues (Cys49 and Cys353) situated near two low-energy bacteriochlorophylls in the FMO protein from Chlorobaculum tepidum Removal of these cysteines (particularly removal of the completely conserved Cys353) through N-ethylmaleimide modification or mutagenesis to alanine abolishes the aerobic quenching effect. Electrochemical analysis and electron paramagnetic resonance spectra suggest that in aerobic conditions the cysteine thiols are converted to thiyl radicals which then are capable of quenching bacteriochlorophyll excited states through electron transfer photochemistry. This simple mechanism has implications for the design of bio-inspired light-harvesting antennas and the redesign of natural photosynthetic systems.
authors.affiliation: Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130; Department of Biology, Washington University in St. Louis, St. Louis, MO 63130; Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130.
authors.forename: Gregory S
authors.initials: GS
authors.lastname: Orf
authors.affiliation: Department of Biology, Washington University in St. Louis, St. Louis, MO 63130; Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130.
authors.forename: Rafael G
authors.initials: RG
authors.lastname: Saer
authors.affiliation: Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130.
authors.forename: Dariusz M
authors.initials: DM
authors.lastname: Niedzwiedzki
authors.affiliation: Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130; Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130.
authors.forename: Hao
authors.initials: H
authors.lastname: Zhang
authors.affiliation: Department of Biology, Washington University in St. Louis, St. Louis, MO 63130;
authors.forename: Chelsea L
authors.initials: CL
authors.lastname: McIntosh
authors.affiliation: Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130;
authors.forename: Jason W
authors.initials: JW
authors.lastname: Schultz
authors.affiliation: Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130;
authors.forename: Liviu M
authors.initials: LM
authors.lastname: Mirica
authors.affiliation: Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130; Department of Biology, Washington University in St. Louis, St. Louis, MO 63130; Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130 blankenship@wustl.edu.
authors.forename: Robert E
authors.initials: RE
authors.lastname: Blankenship
mesh_terms: D000332:Aerobiosis; D000595:Amino Acid Sequence; D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D001429:Bacteriochlorophylls / Q000378:metabolism; D002338:Carotenoids / Q000378:metabolism; D019414:Chlorobi / Q000235:genetics / Q000378:metabolism*; D018360:Crystallography, X-Ray; D003545:Cysteine / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D004579:Electron Transport / Q000235:genetics; D004735:Energy Transfer; D045342:Light-Harvesting Protein Complexes / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D008958:Models, Molecular; D016296:Mutagenesis; D010788:Photosynthesis; D011487:Protein Conformation; D017386:Sequence Homology, Amino Acid
chemical_list: D001426:Bacterial Proteins; D001429:Bacteriochlorophylls; C086320:FMO bacteriochlorophyll protein, Bacteria; D045342:Light-Harvesting Protein Complexes; D002338:Carotenoids; D003545:Cysteine
keywords: Fenna–Matthews–Olson protein; excitation quenching; light-harvesting; photosynthesis; thiyl radical