Mechanism of Asparagine-Mediated Proton Transfer in Photosynthetic Reaction Centers

In photosynthetic reaction centers from purple bacteria (PbRCs), light-induced charge separation leads to the reduction of the terminal electron acceptor quinone, QB. The reduction of QB to QB center dot- is followed by protonation via Asp-L213 and Ser-L223 in PbRC from Rhodobacter sphaeroides. However, Asp L213 is replaced with nontitratable Asn-L222 and Asn-L213 in PbRCs from Thermochromatium tepidum and Blastochloris viridis, respectively. Here, we investigated the energetics of proton transfer along the asparagine-involved H bond network using a quantum mechanical/molecular mechanical approach. The potential energy profile for the H-bond between H3O+ and the carbonyl O site of Asn-L222 shows that the proton is predominantly localized at the Asn-L222 moiety in the T. tepidum PbRC protein environment, easily forming the enol species. The release of the proton from the amide -NH2 site toward Ser-L232 via tautomerization suffers from the energy barrier. Upon reorientation of Asn-L222, the enol -OH site forms a short low-barrier H-bond with Ser-L232, facilitating protonation of QB center dot- in a Grotthuss-like mechanism. This is a basis of how asparagine or glutamine side chains function as acceptors/donors in proton transfer pathways.

Automated summary

In photosynthetic reaction centers from purple bacteria (PbRCs), the reduction of the terminal electron acceptor QB is followed by protonation via specific amino acid residues, such as Asp-L213 and Ser-L223 in Rhodobacter sphaeroides. However, in PbRCs from Thermochromatium tepidum and Blastochloris viridis, Asp L213 is replaced with Asn-L222 and Asn-L213, respectively. This study used quantum mechanical/molecular mechanical calculations to investigate the proton transfer along the asparagine-involved hydrogen bond network. The results suggest that Asn-L222 plays a crucial role in facilitating protonation of QB center dot- in a Grotthuss-like mechanism.