Tracking the Flow of Water through Photosystem II Using Molecular Dynamics and Streamline Tracing

Abstract

The CaMn(4) cluster of the oxygen-evolving complex (OEC) of photosynthesis catalyzes the light-driven splitting of water into molecular oxygen, protons, and electrons. The OEC is buried within photosystem II (PSII), a multisubunit integral membrane protein complex, and water must find its way to the CaMn(4) cluster by moving through protein. Channels for water entrance, and proton and oxygen exit, have previously been proposed following the analysis of cavities found within X-ray structures of PSII. However, these analyses do not account for the dynamic motion of proteins and cannot track the movement of water within PSII. To study water dynamics in PSII, we performed molecular dynamics simulations and developed a novel approach for the visualization of water diffusion within protein based on a streamline tracing algorithm used in fluid dynamics and diffusion tensor imaging. We identified a system of branching pathways of water diffusion in PSII leading to the OEC that connect to a number of distinct entrance points on the lumenal surface. We observed transient changes in the connections between channels and entrance points that served to moderate both the flow of water near the OEC and the exchange of water inside and outside of the protein. Water flow was significantly altered in simulations lacking the OEC which were characterized by a simpler and wider channel with only two openings, consistent with the creation of an ion channel that allows entry of Mn(2+), Ca(2+), and Cl(-) as required for construction of the CaMn(4) cluster.

Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks

“…This channel has been shown via molecular dynamics to be impermeable to water [11], with a barrier of $22 kcal/mol at the bottleneck composed of D1-L91, CP43-F292, and CP43-F358 [12 ]. This leaves the 'narrow,' 'broad,' and 'large' channel systems as options for water entry from the lumen to the OEC ( Figure 2, with nomenclature from [9,13,14]).…”

Radiolytic Mapping of Solvent-Contact Surfaces in Photosystem II of Higher Plants

“…Gabdulkhakov et al (24) additionally performed Xe gas co-crystallization x-ray crystallography. Recently, molecular dynamic simulations coupled with water streamline tracing have been used to map the path of water movement to the oxygen-evolving site (25,26). These authors identified five putative water channels which, in large measure, are similar to the channels identified in previous studies (see Table 1,Ref.…”

“…Briefly, since most of the computational studies examine static crystal structures (22,24,41), they fail to take into account molecular motion on the nsec time scales which could substantially alter the overall shape and dimensions of the identified water channels within PS II. Vassiliev et al (25,26) have at least partially addressed this problem using molecular dynamic simulations of water movement within the photosystem. It has also been implicitly assumed that no conformational changes occur in the PS II structure during normal S-state cycling which affect either water transport to the active site (i.e.…”

“…Gabdulkhakov et al (24) used nobel gas and dimethyl sulfoxide co-crystallization studies in combination with CAVER to examine the 2.9 Å structure of T. elongatus (14), and Ho and Styring calculated solvent-accessible surfaces for the 3.0 Å T. elongatus structure of Loll et al (13). Molecular dynamic simulations have also been used to probe for water channels within the photosystem (25,26), the latter study being performed on the recent high resolution PS II structure (15).…”

Mutations in the CP43 Protein of Photosystem II Affect PSII Function and Cytochrome C550 Binding

“…Interestingly, the current crystal structure identified a third chloride ion bound near the C-terminal amino acid of PsbU, which is located between PsbU and cytochrome c 550 Kawakami et al, 2011). This chloride is ligated by water molecules and lies close to the exit of a proposed hydrogen-bonding network leading from the Mn 4 CaO 5 cluster to the lumen that could possibly serve to transport anions, water or protons (Gabdulkhakov et al, 2009;Vassiliev et al, 2010;Kawakami et al, 2011 …”