Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers.
One of the outstanding questions concerning the early Earth is how ancient phototrophs made the evolutionary transition from anoxygenic to oxygenic photosynthesis, which resulted in a substantial increase in the amount of oxygen in the atmosphere. We have previously demonstrated that reaction centers from anoxygenic photosynthetic bacteria can be modified to bind a redox-active Mn cofactor, thus gaining a key functional feature of photosystem II, which contains the site for water oxidation in cyanobacteria, algae, and plants [Thielges M, et al. (2005) Biochemistry 44:7389-7394]. In this paper, the Mn-binding reaction centers are shown to have a light-driven enzymatic function; namely, the ability to convert superoxide into molecular oxygen. This activity has a relatively high efficiency with a k(cat) of approximately 1 s(-1) that is significantly larger than typically observed for designed enzymes, and a K(m) of 35-40 μM that is comparable to the value of 50 μM for Mn-superoxide dismutase, which catalyzes a similar reaction. Unlike wild-type reaction centers, the highly oxidizing reaction centers are not stable in the light unless they have a bound Mn. The stability and enzymatic ability of this type of Mn-binding reaction centers would have provided primitive phototrophs with an environmental advantage before the evolution of organisms with a more complex Mn(4)Ca cluster needed to perform the multielectron reactions required to oxidize water.
Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287-1604, USA. JAllen@asu.edu
James P
JP
Allen
Tien L
TL
Olson
Paul
P
Oyala
Wei-Jen
WJ
Lee
Aaron A
AA
Tufts
JoAnn C
JC
Williams
D008027:Light; D008345:Manganese / Q000378:metabolism*; D008839:Microelectrodes; D010084:Oxidation-Reduction; D010100:Oxygen / Q000378:metabolism*; D045332:Photosystem II Protein Complex / Q000378:metabolism*; D013481:Superoxides / Q000378:metabolism*
D045332:Photosystem II Protein Complex; D013481:Superoxides; D008345:Manganese; D010100:Oxygen