A Brownian Dynamics Study of the Effects of Cytochrome f Structure and Deletion of Its Small Domain in Interactions with Cytochrome c6 and Plastocyanin in Chlamydomonas reinhardtii

Abstract

The availability of seven different structures of cytochrome f (cyt f) from Chlamydomonas reinhardtii allowed us, using Brownian dynamics simulations, to model interactions between these molecules and their redox partners, plastocyanin (PC) and cytochrome c6 (cyt c6) in the same species to study the effect of cyt f structure on its function. Our results showed that different cyt f structures, which are very similar, produced different reaction rates in interactions with PC and cyt c6. We were able to attribute this to structural differences among these molecules, particularly to a small flexible loop between A-184 and G-191 (which has some of the highest crystallographic temperature factors in all of the cyt f structures) on the cyt f small domain. We also showed that deletion of the cyt f small domain affected cyt c6 more than PC, due to their different binding positions on cyt f. One function of the small domain in cyt f may be to guide PC or cyt c6 to a uniform dock with cyt f, especially due to electrostatic interactions with K-188 and K-189 on this domain. Our results could serve as a good guide for future experimental work on these proteins to understand better the electron transfer process between them. Also, these results demonstrated the sensitivity and the power of the Brownian dynamics simulations in the study of molecular interactions.

Electrostatic strain and concerted motions in the transient complex between plastocyanin and cytochrome f from the cyanobacterium Phormidium laminosum

“…The resulting kinetic data have been very useful to analyse the interaction between Pc and Cf by means of theoretical methods, including Molecular Dynamics (MD) at sub-nanosecond time scale [17], rigid-body MD [18], Molecular Modelling [19] supported by NMR data and Brownian Dynamics (BD) simulations [20][21][22][23][24][25][26][27][28]. Last computations, in particular, are in good agreement with experimentally calculated reaction rates [21,[24][25][26], thereby explaining many effects of ionic strength and mutations on the kinetics.…”

Cytochrome c 6 of Cyanobacteria and Algae: From the Structure to the Interaction

“…In silico data on the Chlamydomonas Cc 6 -Cf complex shows not only the relevance of hydrophobic and electrostatic interactions in bringing the two heme proteins sufficiently close as to allow efficient electron transfer (Gross and Pearson 2003;Haddadian and Gross 2005) but also the key role of the Cf small domain in guiding Cc 6 to dock with Cf, which suggests that Cc 6 explores different positions on Cf (Haddadian and Gross 2006). This finding, along with the kinetic study demonstrating that multiple conformations of Cc 6 contribute to electron transfer within the Cf -Cc 6 complex (Grove et al 2012), is in agreement with recent paramagnetic relaxation enhancement (PRE) NMR data (Díaz-Moreno et al 2014), which are not compatible with a well-defined Nostoc CfCc 6 complex (Díaz-Moreno et al 2005a).…”

Investigating the mechanisms of photosynthetic proteins using continuum electrostatics

“…Brownian dynamics simulations enable to determine relative association rate constants and thus to study for instance the influence of mutations or of ionic strength on association rates. These simulations have been also applied to a variety of photosynthetic electron transfer complexes and allowed to interpret experimental findings on the association between electron transfer partners (Pearson and Gross 1995;Pearson et al 1996;De Rienzo et al 2001;Haddadian and Gross 2006;Gross and Rosemberg 2006;Haddadian and Gross 2005).…”