The mechanism of photo-energy storage in the
halorhodopsin chloride pump.
Christoph
Pfisterer,
Andreea D. Gruia, Stefan Fischer*
J. Biological
Chemistry, vol. 284, p.13562-13569 (2009).
Abstract
The
light-driven pump Halorhodopsin (hR) uses the energy stored in an
initial
meta-stable state (K), in which the bound retinal chromophore has been
photo-isomerized from all-trans to 13-cis, to drive the
translocation of one chloride anion across the membrane.
The energy stored in the
K-state
amounts to only one fifth of the photon energy. A combined
quantum mechanical/molecular mechanical (QM/MM) analysis of the protein
explains why
the protein did not evolve to store more energy: Even though it would
accelerate chloride pumping, a higher energy level of the K-state leads
to
reduced energy barriers against thermal relaxation along unproductive
pathways,
in particular via the premature cis to tran
back-isomerisation.
Minimum Energy Paths (MEP) computed
by Conjugate Peak Refinement (CPR) show that the protein has evolved to finely balance storage versus
unproductive
dissipation: The back-isomerization barriers are just high enough
(≥18kcal/mol)
to keep the decay rate (1/100ms) slower than the remaining photocycle
(1/20ms).
This need to stabilize the captured photon-energy until it can be used
in
slower subsequent steps is inherent to light-driven proteins, as seen
for example in the bacteriorhodopsin
proton pump.
|
The
four stationary states of retinal isomerization :
(protonated
Schiff-base (PSB) of the retinal in yellow)
A) All-trans ground state: the positively charged PSB makes favorable
interactions with the nearby negative groups (chloride and Asp238).
B) Transition state ‡(Ser115) of
the counter-clockwise route for cis→trans isomerization.
C) Transition state ‡(Asp238) of the clockwise route for cis→trans
isomerization.
D) 13-cis planar K-state: the PSB
makes poorer interactions with the
negative groups than in A). This is the energy storage mechanism.
|
Minimum Energy
Pathway (MEP) along a 360° rotation of the PSB:
QM/MM energy profile of the
pathway through the four structures shown on the left:
trans → ‡(Ser115) → 13‑cis→ ‡(Asp238) → trans
The total energy
(continuous black line) is the sum of:
- the retinal self energy (in blue)
- the opsin self energy (everything excluding retinal, in red)
- and the
interaction between retinal and the opsin (in green).
The arrows show the two
possible decay routes of 13-cis.
Molecular movies
showing these transitions are shown below.
|
Movie 1. Decay of
K-state via ‡(Asp238),
clockwise rotation of the PSB.
The energy barrier is 18
kcal/mol relative to the 13-cis K-state. This is the preferred route
for 13-cis → trans
backisomerisation.
Download the movie
(0.4Mb)
Movie 2. Decay of K-state via ‡(Ser115),
counter-clockwise rotation of the PSB.
The energy
barrier is 23 kcal/mol relative to the 13-cis K-state.
Download the movie
(0.6Mb)
Movie 3. 360° rotation of the PSB, trans →
‡(Ser115) → 13‑cis→ ‡(Asp238) → trans.
Concatenation of movies 1 and 2. Same order of events as in the
energy profile shown above.
Download the movie
(0.9Mb)
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