Interprotein electron transfer from cytochrome c2 to photosynthetic reaction center: tunneling across an aqueous interface.
Interprotein electron transfer (ET) reactions play an important role in biological energy conversion processes. One of these reactions, the ET between cytochrome c(2) (cyt) and reaction center from photosynthetic bacteria, is the focus of this theoretical study. The changes in the ET rate constant at fixed distances during the association process were calculated as the cyt moved from the electrostatically stabilized encounter complex to the bound state having short range van der Waals contacts in the tunneling region. Multiple conformations of the protein were generated by molecular dynamics simulations including explicit water molecules. For each of these conformations, the ET rate was calculated by using the Pathways model. The ET rate increased smoothly as the cyt approached from the encounter complex to the bound state, with a tunneling decay factor beta = 1.1 A(-1). This relatively efficient coupling between redox centers is due to the ability of interfacial water molecules to form multiple strong hydrogen bonding pathways connecting tunneling pathways on the surfaces of the two proteins. The ET rate determined for the encounter complex ensemble of states is only about a factor of 100 slower than that of the bound state (tau = 100 micros, compared with 1 micros), because of fluctuations of the cyt within the encounter complex ensemble through configurations having strong tunneling pathways. The ET rate for the encounter complex is in agreement with rates observed in mutant reaction centers modified to remove shortrange hydrophobic interactions, suggesting that in this case, ET occurs within the solvent-separated, electrostatically stabilized encounter complex.
Miyashita
Osamu
O
Department of Physics and Center for Theoretical Biological Physics, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA.
Okamura
Melvin Y
MY
Onuchic
José N
JN
D045362:Cytochromes c2 / Q000737:chemistry*; D004579:Electron Transport; D006860:Hydrogen Bonding; D008958:Models, Molecular; D045322:Photosynthetic Reaction Center Complex Proteins / Q000737:chemistry*
D045322:Photosynthetic Reaction Center Complex Proteins; D045362:Cytochromes c2
Proc Natl Acad Sci U S A. 2004 Nov 16;101(46):16174-9
15520377
J Mol Biol. 2002 May 31;319(2):501-15
12051924
Annu Rev Biochem. 1996;65:537-61
8811189
Science. 1991 May 31;252(5010):1285-8
1656523
Q Rev Biophys. 2003 Aug;36(3):341-72
15029828
J Mol Graph. 1994 Jun;12(2):84-9
7918256
Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3703-8
9108041
J Am Chem Soc. 2002 Jun 19;124(24):6849-59
12059205
Biochemistry. 1993 Oct 12;32(40):10885-93
8399238
Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5002-6
11296248
Biochemistry. 2001 Jul 24;40(29):8452-62
11456482
Curr Opin Chem Biol. 2003 Oct;7(5):551-6
14580557
Science. 2005 Jan 7;307(5706):99-102
15637275
FEBS Lett. 1979 Sep 1;105(1):137-42
226405
J Bioenerg Biomembr. 1995 Jun;27(3):285-93
8847342
Biochim Biophys Acta. 1974 Apr 23;347(1):1-13
4373062
Annu Rev Biophys Biomol Struct. 1992;21:349-77
1326356
Biochemistry. 2003 Dec 16;42(49):14492-500
14661961
Biochemistry. 1993 Oct 12;32(40):10894-904
8399239
Biochemistry. 1995 Sep 12;34(36):11335-43
7547861
Biochemistry. 2003 Oct 14;42(40):11651-60
14529275
Biochemistry. 1988 Apr 5;27(7):2450-61
2838074
Proc Natl Acad Sci U S A. 1974 Sep;71(9):3640-4
16592178
Biochemistry. 1999 Dec 21;38(51):16866-75
10606520
Nature. 1999 Nov 4;402(6757):47-52
10573417
Science. 2000 Oct 6;290(5489):114-7
11021791
Biochemistry. 1994 Nov 22;33(46):13517-23
7947761
Photosynth Res. 1989 Dec;22(3):173-86
24424807
Biochemistry. 2002 May 7;41(18):5807-15
11980484
Biophys J. 2004 Mar;86(3):1813-9
14990507
Q Rev Biophys. 2001 Nov;34(4):563-679
11852595