Faraday Discussions
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Spatio-temporal resolution of primary
processes of photosynthesis
Published on 31 March 2015. Downloaded on 15/05/2015 10:15:53.
Wolfgang Junge*
Received 24th March 2015, Accepted 25th March 2015
DOI: 10.1039/c5fd90015h
Technical progress in laser-sources and detectors has allowed the temporal and spatial
resolution of chemical reactions down to femtoseconds and Å-units. In photonexcitable systems the key to chemical kinetics, trajectories across the vibrational saddle
landscape, are experimentally accessible. Simple and thus well-defined chemical
compounds are preferred objects for calibrating new methodologies and carving out
paradigms of chemical dynamics, as shown in several contributions to this Faraday
Discussion. Aerobic life on earth is powered by solar energy, which is captured by
microorganisms and plants. Oxygenic photosynthesis relies on a three billion year old
molecular machinery which is as well defined as simpler chemical constructs. It has
been analysed to a very high precision. The transfer of excitation between pigments in
antennae proteins, of electrons between redox-cofactors in reaction centres, and the
oxidation of water by a Mn4Ca-cluster are solid state reactions. ATP, the general energy
currency of the cell, is synthesized by a most agile, rotary molecular machine. While the
efficiency of photosynthesis competes well with photovoltaics at the time scale of
nanoseconds, it is lower by an order of magnitude for crops and again lower for biofuels. The enormous energy demand of mankind calls for engineered (bio-mimetic or
bio-inspired) solar-electric and solar-fuel devices.
1 Introduction
When the founders of atomic and molecular physics convened in 1927 at the 5th
Solvay Conference on “Electrons and Photons” in Brussels (see photograph in ref.
1) they had established quantum mechanics, relativity and the interplay of
stochastic and conservative forces in the nano-world. Despite their immense
insight it was probably all but evident to them how molecular events could ever be
resolved down to molecular scales of time (femto-second) and space (1 Å-unit ¼
0.1 nanometer). Neither was it evident that such a high resolution might be
applicable not only to small molecules but also to complex systems such as
oligomers, interfaces, proteins, membranes, cells and organisms. High resolution
became feasible by dramatic innovations in physical instrumentation. In the
Dept. Biology & Chemistry, University of Osnabrück, R. 35/E42 Barbarastrasse 11, 49076 Osnabrück, Germany.
E-mail: [email protected]; Tel: +49-15112180743
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1960s pulse lasers opened up the time domain of nanoseconds, soon followed by
pico- to femtoseconds (ps–fs) in the seventies. The whole spectral range from the
infrared (IR) over the visible to the ultraviolet (UV) has been covered by pulsed
photon sources. It culminated in the free electron “laser” (rather a coherent
super-radiation source) in the seventies, which provides femtosecond X-ray or
electron pulses. Pulse sources together with greatly improved detectors and data
handling capacities have allowed the high resolution of structure and kinetics,
particularly in those physical, chemical and biological systems that can be
stimulated by light.
Recent technical progress was covered in the Faraday Discussion on “Emerging
Photon Technologies for Chemical Dynamics” (FD 171). The present Faraday
Discussion (FD 177) expands this theme into “Temporally and Spatially Resolved
Molecular Science”. It aims at a rigorous exploration of the energy landscape and
the path of extremely rapid photophysical and photochemical reactions involving
a manifold of vibronic and torsional states. Two- and more-dimensional photonecho spectroscopies have been essential to overcome the lack of spectral resolution when using photon-pulses of fs-duration. Prominent topics of FD 177 have
been quantum coherence, failure of the micro-canonical approximation, solvent
effects on vibrational spectra and relaxations, and time-resolved structure analysis by fs-pulses of X-rays or electrons. A common quest in most contributions to
FD 177 has been the perfection of data and the outmost rigor in their theoretical
interpretation. It has called for simple and well dened systems, mostly small
inorganic or organic molecules. The paradigms derived from the behaviour of
simple systems – physical chemistry at its best – have provided rm grounds for
bio-physical-chemists and biophysicists to address their more complex research
objects. Although being complex in design some of nature's essential constructs,
like the proteins that supply cells with energy, originated about three billions
years ago and have been largely conserved during evolution. They are thus standardized and oen as well dened as simple chemical compounds.
When dealing with these fundamental biological systems the canon of questions to be asked is expanded. The key questions of physical chemistry – what,
where and how fast – are to be supplemented by what for and why. The former
three address the object, its molecular structure and evolution in time. The
question what for addresses the physiological role of a given construct and the
question why whether a particular construct is exacted by laws of physics or
merely reveals nature's fancy as a legacy of evolution. In the following the relation
between pure and biologically oriented physical chemistry is illustrated by taking
oxygenic photosynthesis as an example.
2 Oxygenic photosynthesis
Oxygenic photosynthesis by cyanobacteria and plants uses sunlight and produces
oxygen and biomass. Biomass serves man as food, fuel, bre and platform
chemical. Early attempts to understand this process go as far back as the 18th
century. Jan Ingen-Housz in his study on vegetables noticed their “Great Power of
Purifying the Common Air in the Sunshine and of Injuring it in the Shade and at
Night”.2 It was a rst appreciation of the production and re-consumption – in the
reaction cycle between photosynthesis and cell respiration – of the gases that were
later coined oxygen and carbon dioxide. A rigorous spectroscopic analysis of
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photosynthesis started half a century ago using microsecond ashes of light for
excitation. In 1961 Duysens,3 Kok,4 and Witt5 independently arrived at the
conclusion that green plant photosynthesis is powered by two photosystems in
series. They drive electrons from water to NADP+. Water is oxidized by photosystem II (PSII) to yield oxygen and protons. PSII, in turn, reduces photosystem I
(PSI) which reduces NADP+ to NADPH, as illustrated in Fig. 1.6 In that same year
Mitchell (Nobel Prize 1978) postulated that ATP is synthesized from ADP and Pi at
the expense of a proton-motive force across the respective coupling membrane.7
The energy conserved in the chemical difference of the products NADPH/O2 (by
PSII and PSI) and ATP/ADP$Pi (by ATP synthase (FOF1)) drives the reduction of CO2
to biomass.
A decade later the time resolution of the primary electron transfer was
advanced into the picosecond range.8 But it took more than another decade
until Deisenhofer, Huber and Michel (Nobel Prize 1988) published the rst
structural model of a photosynthetic reaction centre (resolution 3 Å).9 It was the
rst ever structural model of any membrane protein. Today, structural models
are available for all the proteins central to photosynthesis. PSI of a cyanobacterium is resolved at a 2.5 Å resolution,10 and even the larger PSI of green plants
with a molecular mass of 660 000 a.u. is resolved at 3.4 Å.11 The latter hosts
almost 200 chlorophyll molecules, mostly with antennae function, plus the
redox-active core with four chlorophyll- and two pheophytin molecules.12
Cyanobacterial PSII, the water–quinone oxidoreductase, has been resolved
starting at 3.8 Å13 and now at a 1.9 Å resolution.14 The structure of ATP synthase
(FOF1) has only partially been determined at the atomic resolution.15,16
However, its full structure is evident from low resolution data of the holoenzyme (see ref. 6 and 17 and references therein). PSII and PSI are solid-state
devices. FOF1 is a most agile rotary machine composed of two rotary motor
generators. FO, the ion-driven motor18,19 is mechanically coupled20 to F1, the
chemical generator.15,21
The key machinery of bioenergetics (photosynthesis and respiration) dates
about three billion years ago. Its design has not changed much since then. It
justies casting into one coherent scheme the kinetic and structural insights
which have been elaborated on enzymes from different organisms (microorganisms, plants and animals).
Fig. 1 Electron and proton transfer in the coupling membrane of oxygenic photosynthesis. (a) Electron transfer (red arrows) and proton transfer (purple arrows) involving
photosystems I and II (PSI and PSII), cytochrome b6f (cyt b6f), and FOF1. It produces O2,
NADPH and ATP. Modified with permission from the Annual Review of Biochemistry,
Volume 84. © 2015, Annual Reviews, http://www.annualreviews.org.6
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3 Excitation energy transfer
Photosynthetic reaction centres are surrounded by pigments with antenna
function, in PSII between 200 and 300 chlorophyll-molecules. Being embedded in
membrane proteins they enhance the absorption cross-section of the photoreactive core. In chlorophyll-based reaction centres from all organisms the core
hosts four plus two tetra-pyrroles, the former four being bacterio-chlorophyll and
the latter two either bacterio-pheophytin or bacterio-chlorophyll (see Fig. 2).
These pigments are very closely spaced and thus strongly coupled. The core was
rst isolated in the pure form from bacteria. Starting in the eighties femtosecond
spectroscopy revealed that the rst electron transfer step from bacterio-chlorophyll to bacterio-pheophytin relaxes in picoseconds.22,23 Soon thereaer vibrational coherence between these pigments became evident.24 As in several
contributions to this Faraday Discussion femtosecond excitation and multidimensional photon-echo spectroscopy became the clue to investigate processes
where the micro-canonical approximation fails. An impressive series of studies on
photosynthesis has revealed quantum beats in antennae proteins (for reviews and
references see ref. 25–27, for a recent survey of quantum biology see ref. 28).
Taking up the above biophysical question of physical necessity versus legacy of
evolution one wonders whether coherent excitation transfer is a necessary
prerequisite for the high quantum yield of photosynthesis. In a theoretical study
on a structurally well characterized bacterial antenna complex it is argued that it
is rather unecessary.29 If the reorganisation time of the environment is not much
faster than the one of the system coherence is prolonged. However, it does not
increase the efficiency of energy transfer, except when excitation decay competes
with trapping.29 An experimental study on the same antenna protein was presented at this meeting in a poster by Battacharyya and Sebastian. Mechanisms for
the dephasing of coherence by the environment were discussed in posters by
Kayal et al. and Roy et al., and the mechanism of photon-induced intra-molecular
excimer formation and charge transfer was treated by Mishra et al.30
In photosynthetic antennae the excitation decay does not to compete with
trapping. This is has been corroborated by the following recent experiments. Van
Grondelle's group analysed the excitation transfer between six pigments (4 chlorophyll a, 2 pheophytin a) in the puried core of PSII.31 Quantum beats persisted
for several 100 femtoseconds even at ambient temperature. Several coherent
excimer-/charge-transfer states coexisted before the creation of a metastable
radical pair. The authors suggested that quantum design of the core is pivotal for
the high quantum yield.31 In these experiments the core of PSII is isolated from its
antennae complement and it is excited by femtosecond pulses. In vivo the core is
surrounded by antennae. Quanta trickle in at a rate of much less than 1000 per
second. Holzwarth and his colleagues studied this situation in oxygen evolving
PSII particles containing a complement of about 80 chlorophyll molecules.32,33 To
avoid singlet–singlet annihilation they kept the photon density of the exciting
pulse low. The total time for exciton trapping and charge separation was about
100 ps.32 The calculated intrinsic time of charge separation in the core, on the
other hand, was much shorter, 2.7 ps.33 This situation is paralleled in purple
photosynthetic bacteria. Excitation transfer in the B850-ring of the antenna LH2
as well as in the B875-ring of LH1 is very fast (about 100 fs) and it involves
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Fig. 2 Structural model of the redox cofactors in the core of cyanobacterial PSII (modified
with permission of Science).114 The electron transfer uses the D1-branch of the heterodimer. Chorophyll a molecules are given in green and blue, pheophytin a in blue and the
primary (QA) and secondary (QB) quinones in purple. The catalytic CaMn4-cluster is linked
via a tyrosine (TyrZ) to the chlorophyll (PD1). Centre-to-centre distances in Å-units.
coherence. The transfer from LH2 to LH1 takes 3 ps, and further on from LH1 into
the trap 35 ps.25 The long and trap-limited lifetime of excitation greatly exceeds
the decay time of coherence. Independent of whether coherent transfer is
involved or not, the only condition for high quantum yield is that the transfer
beats the dissipative loss of excitation in the whole system. This physical
constraint is rather mild, and it provides a leeway for various transfer mechanisms and structural designs. In fact, photosynthetic organisms use a wide
palette of mechanisms for excitation transfer, ranging from hopping by Försterresonance over Frenkel-excitons to more delocalized modes involving the
coherent states of many pigment molecules. Accordingly, the antennae structure
varies considerably between organisms. Chlorophyll molecules are either
enwrapped in proteins as in the LHC2 of plants,34 and in the LH1 and LH2 of
purple bacteria,35,36 or self-organized as in the chlorosomes of green bacteria.37
The energy transfer may be directed towards a deep trap (low energy trap), as in
PSI, or undirected if the trap is shallow, as in PSII.33 In all cases the quantum yield
of trapping is close to one.
4 Electron transfer
Excitation transfer into the very core of any reaction centre results in a very rapid
charge separation. The rst metastable product is a radical pair which is formed
in picoseconds. In PSII this pair is pheophytinD1+–chlorophyllD1 (see Fig. 2).
Herein the subscript D1 refers to the subunit to which the respective pigment is
attached. While the positive charge is localized on this particular chlorophyll in
PSII (PD1 in Fig. 2), it is delocalized over two bacterio-chlorophylls, the “special
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38
pair”, in the reaction centre of purple bacteria. The delocalization of the
unpaired electron over this “special pair” hence is not pivotal for a high quantum
yield, in contrast with previous beliefs.39
The charge separation is directed across the membrane. The membrane is
charged by 50 mV (eld strength 107 V m1) per single turnover of each photosystem. Light induced voltage transients were rst detected in plant chloroplasts.
Electrochromic absorption changes of intrinsic pigments served as a molecular
voltmeter40,41 with a very high time-resolution.42 The vibrational Stark-effect as a
molecular voltmeter was discussed in a poster of this Faraday Discussion by S.
Bagchi et al.
Structural pseudo-C2-symmetry is a common feature of most reaction centres.
Their hetero-dimeric structure is considered an evolutionary legacy of a homodimeric and truly C2-symmetrical common ancestor.43–46 Anaerobic green bacteria
still host a homo-dimeric reaction centre.43
Independent of the type of reaction centre and organism, the positions and
orientations of the six pigments in the core are very much the same. There are
three pigments on each branch of the dimer. While only one branch is redoxactive in type II centres (of purple bacteria and in PSII of plants and cyanobacteria), both are similarly active in a type I centre (PSI). The functional asymmetry
in the former has been attributed (by Stark-effect spectroscopy) to different
dielectric screenings in the two branches.47 The asymmetric activity of type II
centres is linked to its function as a one-electron to two-electron gate, whereas
PSI, with its longer line of secondary acceptors, functions mono-electronically
(for a thorough discussion and references see ref. 48).
The mechanism of electron transfer between cofactors that are embedded in
the protein is adequately described by the Marcus theory.49,50 It models tunnelling
within the limits of the Born–Oppenheimer approximation. The rate is a function
of the (edge-to-edge) distance between donor and acceptor (r), and it depends on
three parameters: the standard free energy difference between the donor and the
acceptor (DG0), the reorganization energy of their environment (l) and the decay
constant of wave-function-overlap (b):
"
#
2
ðDG0 þ lÞ
rate exp
expðbrÞ
(1)
4lkT
This simple relation in terms of only three parameters has been experimentally
very well met. In synthetic donor–spacer–acceptor triads it holds over three orders
of magnitude.51 As for the electron transfer between cofactors in a protein, various
pathways were screened in cytochrome c. Its heme served as the electron acceptor
for a photosensitizer which was covalently attached to various positions at the
surface. The transfer rate decreased depending on whether the electron passed
mainly along single bonds, hydrogen bonds or through a void volume in the
protein.52,53 In a related study, Dutton and colleagues54 analysed the wealth of
kinetic and structural data on the electron transfer in photosynthesis and cell
respiration. They corrected the observed rates for the matching driving force
(determined!) and reorganization energy (assumed!), namely DG0 ¼ l. Over 13
orders of magnitude the normalized rates decline mono-exponentially with the
edge-to-edge distance (r) between donor and acceptor. Deviations by one order of
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magnitude can be attributed to local variations of l and b. The donor–acceptor
distance is hence the major determinant of the rate of electron transfer.55 The
reorganization energy (l) and the decay constant of the electronic wave functions
(b) in proteins do not vary too much. Nature's engineering of structures for rapid
electron transport has thus relied mainly on the distance between redox-cofactors
(r) and on the driving force (DG0).55
Once the core of the reaction centre is hit by an excitation the primary electron
transfer is very fast. In PSII the radical pair (chlorophyll+–pheophytin) appears in
picoseconds. The electron is then transferred to a rst quinone (QA) in about 400
picoseconds and from there on to a second quinone (QB) in some 100 microseconds.56,57 The electron hole, on the other hand, is rapidly transferred in some
ten nanoseconds to a tyrosine58 and further in microseconds to the Mn4Cacluster. All of these reactions outrun by orders of magnitude the respective
wasteful back-reactions of excited states and radical pairs. Rapid forward reactions and slow back-reactions guarantee the high quantum yield of photosynthesis. On the other hand they require losses of free energy. In other words,
photosynthesis sacrices energy efficiency for directionality.48
5 Water oxidation
PSII is a water–quinone oxidoreductase. The structure of cyanobacterial PSII is
resolved at 3.8 Å,13 3.5 Å,59 and 1.9 Å.14 Water (-derivatives) are oxidized by the
catalytic Mn4Ca-cluster and oxygen plus protons are liberated. When dark adapted PSII is excited by a series of short light ashes the Mn4Ca-cluster is clocked
through sequentially higher and metastable oxidation states, until reaching the
highest state (see ref. 60 and references therein). Only then the reaction with
bound water proceeds (in one millisecond) to yield dioxygen (see ref. 61). The
stepwise accumulation and pooling of four oxidizing equivalents, before initiating what still appears as the reaction of four-electrons-at-once, serves two
purposes. It homogenizes the energy demand of successive electron transfer
steps, and controls hazardous intermediates (e.g. hydroxyl radical and superoxide) on the way from water to dioxygen. There is a wealth of detailed kinetic
studies on water oxidase, addressing the chlorophyll-moiety, an intermediate
tyrosine, the Mn4Ca-cluster, electrons, protons and oxygen. A wide range of
optical (X-ray, UV, VIS and IR), magnetic and mass spectroscopic techniques have
been utilized to resolve electron transfer, proton transfer, conformational
changes of the protein, substrate binding and product release in the time-domain
from nano- to milliseconds (for reviews and references see ref. 62–65).
The precise structure of the manganese cluster is still under contention.
During standard X-ray exposure of PSII-crystals Mn4 is the prime target of radiation damage66,67 (for radiation damage of metal markers for protein structural
studies see Helliwell et al.).68 The reduction of Mn may inuence its ligation state.
The lack of unequivocal structural models of the Mn4Ca-cluster in its sequential
oxidation states is a major obstacle for a thorough understanding of the nal
reaction cascade. For the time being, two non-invasive approaches, namely by
magnetic resonance spectroscopy (Endor69) and by theoretical chemistry (density
functional theory71), have converged towards one particular structural model of
the CaMn4-cluster and its ligands including water (derivatives). X-ray crystal
structural analysis will eventually take up, either challenging or corroborating the
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present structural concept by a probe-before-destroy-approach (for principles and
perspectives of this technique see Miller et al.).70 PSII-crystals have been exposed
to an ultra-short and intense X-ray pulse (100 fs) of a free-electron-laser.72,73 The
feasibility of analysing the cluster-structure in its sequential oxidation states has
been clearly demonstrated, although at a limited resolution so far (5–5.5 Å).73
Structural details on the Mn4Ca-moiety, bound water (derivatives), and amino
acid ligands is the essential complement of kinetic data when aiming to understand the detailed reaction mechanism of this “holy grail” of photosynthesis.
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6 ATP synthesis
Mitchell's daring hypothesis on proton-driven ATP synthesis7 roused the unprepared bioenergetics community. Soon thereaer essential elements of his
hypothesis were detected in plant chloroplasts. Illumination generates transmembrane voltage40 and a pH-difference,74 and the pH-difference75 and/or the
voltage76 can drive the synthesis of ATP. The molecular structure of ATP synthase
was then still unknown. Only its bipartite construction with a membrane portion,
FO, which conducts protons, and a peripheral portion, F1, which interacts with
nucleotides, was apparent. Boyer (Nobel Prize 1996) and his colleagues found that
F1 hosts two, if not three identical catalytic sites, that operate alternately,77 if not
in a rotary mode.78 Conformational energy stored in the enzyme might drive the
formation of ATP from ADP and P1.79 In 1994 Walker (Nobel Prize 1996) and his
colleagues presented the rst structural model of its chemical generator at a 2.3 Å
resolution,15 now at 1.9 Å,80 which strongly favoured a rotary function of F1. F1 is a
pseudo-hexagon of two types of subunits arranged as (ab)3 with a cranked sha
(subunit g) in its centre. It suggests that the rotation of the central sha drives
ATP synthesis when progressing from one catalytic site on b to the next. Soon
thereaer the rotation of the central sha was experimentally established, starting without time resolution by the biochemical crosslink technique,81 and then
time resolved either by polarized photobleaching and recovery82,63 or uorescence
microscopy.83 The latter technique became the gold standard in the eld
(for original video recordings see ref. 119). Its principle is illustrated in Fig. 3a.
The hexagonal body of the enzyme is xed on a solid support so that the hydrolysis of ATP drives the sha around. In a pioneering experiment, a uorescent
actin lament was attached to the foot of the central stalk of F1 and the rotation of
the lament was video-recorded in a uorescence microscope.83 In the author's
lab the uorescent probe was attached to the holo-enzyme, FOF1, as shown in
Fig. 3a. Notably the procession of this enzyme over its reaction coordinate can be
recorded in real-time. By certain tricks it has been feasible to correlate the
dynamic jumps and transient dwells of the live enzyme with the still pictures of
the inhibited enzyme as a crystal structure.84–86 Moreover, the rotor position has
been externally manipulated by an attached hyper-paramagnetic bead.87,88
Ongoing studies in this line will likely provide more precise data on the energy
landscape of F1, a prerequisite for thorough theoretical descriptions (see ref.
89–91 and references therein). The wealth of structural and kinetic data qualies
ATP synthase as a hydrogen atom of nano-motoring. The sophisticated, yet simple
electro-mechano-chemical operation of ATP synthase has been described in
several reviews.6,17–20,92,93 For animations of the enzyme and its two motors, FO and
F1, see ref. 121. A few salient features shall be emphasized in the following.
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The micro-videographic assay for the rotary activity of FOF1.115,116 (a) The holoenzyme is solubilized in detergent and the crown of F1 is attached by His-tags to a solid
support. A fluorescent actin filament is attached to the rotor ring of FO (modified with
permission from FEBS Lett.116). (b) When ATP hydrolysis drives the rotor ring round, the
actin filament, subject to viscous drag on the filament, is curved. The elastic parameters of
the filament are determined by fluctuation analysis (modified figures from ref. 115 with
permission). For the original video-recordings see ref. 120.
Fig. 3
Both FO and F1 are stepping motors. When driven by ATP hydrolysis F1 rotates
with a period of 120 , with substeps of 40 and 80 .94–96 This stepping reects the
presence of three equivalent reaction sites on F1 and torque production during
substrate binding, catalysis and product release. On the other hand FO steps by
36 ,97,98 reecting the C10 symmetry of the particular bacterial FO. The mechanism
and the structure of the rotary ion-motor, FO, is not discussed here. For the
principle of operation see ref. 18, for the kinetic properties ref. 99, for the
structure ref. 16 and for simulations of its reaction dynamics ref. 89,99,100. Here
we focus on the cooperation of FO and F1 in the holo-enzyme.
If the proton-motive force is larger than the thermodynamic force of ATP
hydrolysis the electrochemical motor of ATP synthase, FO, drives the chemical
generator, and F1 synthesizes ATP. If the force-relation is reversed, motor and
generator change roles. ATP hydrolysis by F1 drives FO to generate the protonmotive force. If the forces match the enzyme rests. Thermodynamic quasi-equilibrium between the two motors was used to determine the torque generated by
ATP hydrolysis.101 As illustrated in Fig. 3a a long lament (3 mm) was attached to
the rotary electromotor of the holo-enzyme. It slows the turnover rate of the
enzyme by several orders of magnitude into a state of quasi-equilibrium. The
torque was calculated from the elastic deformation of the lament (documented
in Fig. 3b), which reects the counteraction of the drive and the viscous drag. The
mean torque, 56 pN nm, conformed with the calculated driving force of
ATP-hydrolysis (70 kJ mol1),101 which implies that the two motors do not slip
against each other.
Although torque production by F1 was expected to progress in steps (under the
given conditions), the torque output to the actin lament on FO was almost
constant. This surprising observation has been explained by solving the Fokker–
Planck equation of a stepping nanomotor when elastically coupled to a heavy
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101
load. Decreasing the stiffness of the elastic buffer between the stepping drive
and the load attens the torque prole at the output. It increases the turnover rate
by orders of magnitude over the one with a stiff transmission (see Fig. 4a). In
other words, an elastic force–torque transmission is pivotal for high kinetic efficiency of the stepping nanomotor that drives a heavy load.102 This benet of a
compliant transmission applies to all of nature's intrinsically stepping nanomotors. The distribution of elastically compliant and stiff domains over FOF1 was
determined by uctuation analysis.20,103,104 The result is illustrated in Fig. 4b. The
most compliant domain (stiffness 70 pN nm) of the holo-enzyme is located on the
central rotor and between the sites where the respective power strokes are
generated (see ref. 6 and 20 for details and references). The rest of the enzyme,
and in particular the stator, are stiffer by an order of magnitude. The elastic
transmission decouples the two motors kinetically while keeping them strictly
coupled, both thermodynamically and, in the time average, also under a steady
turnover. It explains why this enzyme can run with different gears in different
organisms. The gear ratio of FO : F1, and likewise the expected H+ : ATP ratio,
ranges from 8 : 3 in mammalian mitochondria105 to 10 : 3 in yeast mitochondria105 and 14 : 3 in chloroplasts,106 and it varies between 10 : 3 and 15 : 3 in
different bacteria (see ref. 107 and references therein). Organisms (organelles)
thriving at a large and constant ion-motive force, like mammalian mitochondria,
run at low gear (speedsters), and those at a low and/or uctuating force, like
chloroplasts and in alkaliphilic bacteria, at high gear (tractors).6 Because the two
motors are kinetically decoupled the enzyme can operate with a strictly proton
specic ion motor in some organisms,99 and optionally on sodium or proton108,109
Fig. 4 On the elastic torque transmission between the ion-driven motor, FO, and the
chemical generator, F1, of rotary ATP synthase. (a) The distribution of elastically compliant
(red) and stiff domains (grey) over the enzyme. Numbers give the torsion stiffness in pN
nm.6,117,118 (b) Calculated dependence of the turnover rate of a stepping and rotary
nanomotor, which is coupled to a heavy load, on the torsion stiffness of the transmission
to the load.115 With permission from the Annual Review of Biochemistry, Volume 84. ©
2015, Annual Reviews, http://www.annualreviews.org.
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in others, depending on the ambient ion concentration. The elastically compliant
transmission accounts for considerable freedom of design for both rotor and
stator in the similarly bipartite relatives of FOF1, namely the archeal A-ATPase and
the V-ATPase of eukaryotes.6,110 They all share with other nucleotide triphosphatases the (pseudo-)hexagonal design of the catalytic headpiece, namely with helicases and bacterial DNA-translocases which rotate and/or translocate proteins,
RNA or DNA, in their central cavity and probably share a common ancestry.111
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7
Outlook
Oxygenic photosynthesis in its present and fossil forms provides man with food,
ber and fuel. The quantum yield of photosynthesis is almost perfect. As to
primary energy efficiency in relation to the solar spectrum (about 20%), oxygenic
photosynthesis compares well with single-band-gap photovoltaic cells.112 For the
yearly average of crops in the eld however the efficiency drops down to 2%, and
for bio-ethanol production to 0.2%, if not being energy negative (as were biofuels
of the rst generation). The total useful energy of biomass which is globally
produced in one year (on land) is only about 5-times greater than man's yearly
energy consumption. It is obvious that present day biomass, and even more so
biofuels, cannot satisfy man's ever growing energy demand. Although bio-ethanol
is produced and used on a large scale in Brazil, it is no option for countries with
higher population densities and/or industrialization, namely China, the EU and
India. The products of photosynthesis should thus rather be reserved for food,
feed, bre and platform chemicals. A sustainable energy supply calls for technical
utilization of solar energy. Wind-power, photo-thermal and photo-voltaic devices
are technically established, economically competitive, and increasingly installed
worldwide. It is a major scientic challenge to develop new techniques for the
production of solar fuels, articial photosynthesis with greater efficiency, and
based on low cost catalysts.113
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Original video recordings of rotary motion of F1: http://www.k2.phys.waseda.ac.jp/
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Original video recordings of FOF1: http://www.home.uni-osnabrueck.de/
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Animations of the rotary activity of F1, FO, and FOF1: http://www.mrcmbu.cam.ac.uk/research/atp-synthase/molecular-animations-atp-synthase
http://www.home.uni-osnabrueck.de/wjunge/Media.html.
562 | Faraday Discuss., 2015, 177, 547–562 This journal is © The Royal Society of Chemistry 2015