Primary Processes of Photosynthesis, Parts 1-2 - Principles and Apparatus

828 Pages·2008·32.87 MB·English

by  Renger

Preface for the ESP Series in Photochemical
and Photobiological Sciences
‘‘Itsnotthesubstance,it’sthedosewhichmakessomethingpoisonous!’’When
Paracelsius, a German physician of the 14th century made this statement he
probably did not think about light as one of the most obvious environmental
factors. But his statement applies as well to light. While we need light, for
exampleforvitaminDproduction,toomuchlightmightcauseskincancer.The
dosemakesthedifference.Thesediversefindingsoflighteffectshaveattracted
theattentionofscientistsforcenturies.Thephotosciencesrepresentadynamic
multidisciplinary field that includes such diverse subjects as behavioral res-
ponses of single cells, cures for certain types of cancer and the protective
potentialoftanninglotions.Italsoincludesphotobiologyandphotochemistry,
photomedicine as well as the technology for light production, filtering and
measurement. Light is a common theme in all these areas. In recent decades a
moremolecularcenteredapproachhaschangedboththedepthandthequality
of the theoretical as well as the experimental foundation of photosciences.
An example of the relationship between global environment and the bio-
sphere is the recent discovery of ozone depletion and the resulting increase in
high-energy ultraviolet radiation. The hazardous effects of high-energy ultra-
violetradiation on all livingsystems isnow well established. Thisdiscovery of
the result of ozone depletion put photosciences at the center of public interest
withtheresultthat,inanunparalleled effort,scientistsandpoliticiansworked
closelytogethertocometointernationalagreementstostopthepollutionofthe
atmosphere.
The changed recreational behavior and the correlation with several diseases
inwhichsunlightorartificiallightsourcesplayamajorroleinthecausationof
clinicalconditions(e.g.,porphyrias,polymorphicphotodermatoses,Xeroderma
pigmentosumandskincancers)havebeenwelldocumented.Asaresult,insome
countries(e.g.,Australia)publicservicesinformpeopleaboutthepotentialrisk
of extended periods of sun exposure every day. The problems are often
aggravated by the phototoxic or photoallergic reactions produced by various
environmental pollutants, food additives or therapeutic and cosmetic drugs.
However, if properly used, light-stimulated processes can induce important
beneficialeffectsinbiologicalsystems,suchastheelucidationofseveralaspects
of cell structure and function. Novel developments are centered around
v
vi PREFACE
photodiagnostic and phototherapeutic modalities for the treatment of cancer,
arthrosclerosis,severalautoimmunediseases, neonataljaundiceand others.In
addition,classicresearch areas such asvision and photosynthesis arestill very
active. Some of these developments are unique to photobiology, since the
peculiarphysicochemicalpropertiesofelectronicallyexcitedbiomoleculesoften
lead to the promotion of reactions that are characterized by high levels of
selectivity in space and time. Besides the biologically centered areas, technical
developmentshavepavedthewayfortheharnessingofsolarenergytoproduce
warm water and electricity or the development of environmentally friendly
techniquesforaddressingproblemsoflargesocialimpact(e.g.,thedecontami-
nation of polluted waters). While also in use in Western countries, these
techniques are of great interest for developing countries.
The European Society for Photobiology (ESP) is an organization that aims
todevelopandcoordinatetheverydifferentfieldsofphotosciencesintermsof
publicknowledgeandscientificinterests.Owingtotheeverincreasingdemand
for a comprehensive overview of the photosciences the ESP decided to initiate
an encyclopedic series, the ‘‘Comprehensive Series in Photochemical and
Photobiological Sciences’’.Thisseries isintendedtogive anin-depthcoverage
over all the very different fields related to light effects. It will allow investiga-
tors,physicians,students,industryandlaypersonstoobtainanupdatedrecord
of the state-of-the-art in specific fields, including ready access to the recent
literature. Most importantly, such reviews give a critical evaluation of the
directionsthatthefieldistaking,outlinehotlydebatedorinnovativetopicsand
even suggest a redirection if appropriate. It is our intention to produce the
monographs at a sufficiently high rate to generate a timely coverage of both
well established and emerging topics. As a rule, the individual volumes are
commissioned; however, comments, suggestions or proposals for new subjects
are welcome.
Donat-P. Ha¨der and Giulio Jori
Spring 2002
Part 1: Photophysical Principles, Pigments
and Light Harvesting/Adaption/Stress
I. Introduction
Chapter 1
Overview of Primary Processes of
Photosynthesis
Gernot Renger
Table of Contents
1.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
1.2 Basic Principles of Photosynthetic Solar Energy Transformation. . . . 12
1.2.1 Light Harvesting. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
1.2.2 Light-Induced Charge Separation . . . . . . . . . . . . . . . . . . . . . 15
1.3 Electron Transport Chains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
1.4 Architecture of the Photosynthetic Apparatus . . . . . . . . . . . . . . . . . 22
1.4.1 Anoxygenic Bacteria. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
1.4.2 Oxygen Evolving Organisms . . . . . . . . . . . . . . . . . . . . . . . . . 23
1.5 Biomimetic Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
1.5.1 Biomimetic Antennas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
1.5.2 Biomimetic Reaction Center . . . . . . . . . . . . . . . . . . . . . . . . . 27
1.5.3 Biomimetic Antenna–Reaction Center Systems. . . . . . . . . . . . 28
1.5.4 Biomimetic Proton Pump . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
1.5.5 Biomimetic ATP Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . 29
1.5.6 Catalysts for Oxidative Water Cleavage and Reductive CO
2
Fixation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
1.6 Concluding Remarks and Future Perspectives . . . . . . . . . . . . . . . . . 30
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
5
OVERVIEW OF PRIMARY PROCESSES OF PHOTOSYNTHESIS 7
Abstract
This introductory chapter describes the general principles of photosynthetic solar
energy exploitation as the unique Gibbs energy source of living matter. The overall
processcanbesubdividedintotwosequences: (a)light-drivenreactions,referred toas
‘‘Primary Processes of Photosynthesis’’, which lead to the formation of ‘‘energy rich’’
bound hydrogen (TH ) and ATP, and (b) fixation of primordial carbon, nitrogen and
2
sulfur compounds (where CO transformation into carbohydrates is by far the most
2
abundantprocess)withTH asreductantandATPasdrivingforcefortheendergonic
2
reactions.
This chapter focuses on the functional and structural organization of the ‘‘Primary
Processes of Photosynthesis’’. After a brief discussion of the underlying principles of
harvestingoflightanditstransformationintoelectrochemicalGibbsenergybyradical
pairformationinpigment–proteincomplexes,thetwotypesofreactioncenters(typeI
andtypeII)andthetwodifferentmodesofphotosynthesisinanoxygenic(non-oxygen
evolving)andoxygenic(oxygenevolving)organismsareoutlined.Itisemphasizedthat
anoxygenic(bacterial)photosynthesisisenergeticallydrivenbyonlyonetypeofreaction
center(RC)(eitherRCIorRCII)whileinoxygenicphotosynthesisbothtypesofRCs
actinseries,leadingtoelectrontransportfromwatertoNADP1.
Anisotropic incorporation of the functional complexes into membranes leads to
vectorial electron transfer and spatial separation of oxidant- and reductant-induced
reactionsconcomitantwiththeformationofatransmembraneelectrochemicalpotential
differenceforprotons,providingthedrivingforceforATPsynthesis.
The general architecture of the photosynthetic apparatus and its structural organi-
zation within different membrane systems of anoxygenic and oxygenic organisms are
described. Finally principles and strategies for construction of biometric systems are
brieflydiscussed.
1.1 Introduction
Hencethegeneralstruggleoflifeisnotforresourcesofmaterialandnot
forenergy,whichinformofheat,unfortunatelynontransducible,plentifully
exists in every organism, but it is the fight for entropy which becomes
disposiblethroughthetransitionfromthehotsuntothecoldearth.Inorder
to make use of this transition, plants unfold unmeasurable areas of their
leaves and forces the energy of the sun, in still unresolved ways, before it
sinks to the temperature of the earth’s surface, to carry out chemical
synthesis which no one in our laboratories can even imagine. [1]
(L. Boltzmann, 1886, see Ref. [1])
Biological organisms are open systems that are far from thermodynamic
equilibrium (about 20–25kJmol(cid:1)1) [2]. Therefore, Gibbs (free) energyw fluxes
are indispensable for their development and sustenance [2,3]. Electromagnetic
radiation in the near-UV, visible and near-infrared red region emitted from a
huge extraterrestrial nuclear power station, the sun, is the unique source that
wTheterm‘‘Gibbsenergy’’willbeusedthroughoutthischapterinsteadof‘‘freeenergy’’.
8 GERNOT RENGER
satisfies the Gibbs energy demand of life on earth. The relevance of solar
radiationastheenergetic prerequisite ofthe biosphere was alreadyrecognized
in 1845 by R. J. Maier, and the underlying thermodynamic principle correctly
formulatedbyL.Boltzmannin1886(videsupra,[1]).Theannualenergyinput
from the sun on our planet is estimated to be about 5(cid:2) (cid:3)1021kJmol(cid:1)1 [4].
Nearlyhalfofthisamountiseitherreflectedbytheatmosphereorabsorbedby
it (giving rise to storms and water movement in the oceans), the other half
irradiates the earth surfaces, i.e., oceans and land (at a ratio of 2–2.5). Only a
very small fraction, o0.1% of this 2.5(cid:2) (cid:3)1021kJmol(cid:1)1 year(cid:1)1, is eventually
transformed via photosynthesis into chemical Gibbs energy. In the overall
balance, the earth releases energy as black body radiation in the far-infrared
region (the maximum of the wavelength distribution is at about 10mm), thus
keeping the average temperature virtually constant.
Among living matter two types of organisms exist that differ entirely with
respecttotheirmodeofexploitationofsolarradiationasGibbsenergysource:
(i) photoautotrophs, which can use the light energy directly as driving force,
and (ii) heterotrophs, which can not perform direct solar energy exploitation
and therefore need the uptake of ‘‘energy rich’’ substances (food) eventually
synthesized by photoautotrophs, to extract Gibbs energy through metabolic
digestions.
In a general way these basic fundamental processes of bioenergetics can be
described by a very simple scheme depicted in Figure 1. In photoautotrophic
organisms the solar radiation increases the Gibbs energy content of a suitable
storage system in state A by its light-induced transition into a state B. This
processisreferredtoasphotosynthesisandthespecificamountofstoredGibbs
energy will be symbolized by DG (hn). In the reverse direction, food mole-
store
cules with a Gibbs energy content B0 are catabolized by the heterotrophic
organisms into a state A0 under the release of Gibbs energy that is made
available in form of the ‘‘energy currency’’ ATP of biological systems. This
Figure 1. General scheme of the fundamental bioenergetic transformations of solar
radiationasuniqueGibbsenergy:directuseinphotoautotrophicorganisms(left-hand
side)andindirectexploitationviatheuptakeoffoodoriginatingfromphotoautotrophic
systems(right-handside).
OVERVIEW OF PRIMARY PROCESSES OF PHOTOSYNTHESIS 9
processisdenotedrespiration(forthesakeofsimplicitynodistinctionismade
between aerobic respiration and anaerobic fermentation; see biochemistry
textbooks for details) and the specific amount of available Gibbs energy will
be symbolized by DG(ATP).z
The description of the fundamental principles of solar energy exploitation
summarized in Figure 1 raises questions about the nature of molecules that
substantiate states A/B and B0/A0. Biological organisms use very few sub-
stances. Based on considerations of van Niel [5] the photosynthetic transition
A - B can be described by the overall reaction:
hv
H X þ T(cid:1)!TH þ X ð1Þ
2 2
where H X is a suitable hydrogen donor and T a hydrogen acceptor with
2
G1(TH )4G1(XH ). In fact, this reaction is coupled with ATP formation. In
2 2
subsequent reaction sequences both species TH and ATP give rise to assimi-
2
lation of the primordial elements carbon, nitrogen and sulfur. The most
important among these reactions is the well-known CO fixation into carbo-
2
hydrates via a sequence of dark reactions referred to as the Calvin–Benson
cycle [6–8] which by far is quantitatively the largest chemical process on the
earthsurface.Theestimatedannualturnoverisoftheorderof200–300billion
tons of fixed CO [4].
2
Correspondingly, state B0 of the Gibbs energy converter in photoheterotro-
phic organisms is symbolized by hydrogen donor T0H that becomes oxidized
2
under the release of DG(ATP), as the analogous reversal of reaction [1].
If one takes into account the evolutionary principle of the ‘‘survival of the
fittest’’,understandably,anyimprovementintheefficiencyofthesefundamen-
talbioenergeticprocesseswasofadvantageinthecompetitionoflivingsystems
for Gibbs energy sources. Basically, two parameters are of physiological rele-
vance:(i)thespecificstoragecapacityDG (hn)thatdescribesthemolarGibbs
store
energy increase of the transition A - B and DG(ATP) the corresponding
decreaseofthereactionB0 -A0 (Figure1),and(ii)thenatureofthechemicals
thatenabletheselarge-scalestatetransitionsthroughsufficientavailabilityand
controlofthereactivityofthemolecularspeciesparticipatingintheseprocesses.
Thedevelopmenttowardsmoreefficientsystemsofbothphotosynthesisand
respiration was inevitably restricted by atheoretical thermodynamic limit that
emerges from the dependence of life on water. As a consequence, DG (hn)
Store
can reach its possible maximum level at the stage of water cleavage into the
elements H and O . This valueDGmaxðhnÞis 237.17kJmol(cid:1)1 [9]. In reality,
2 2 store
1
however, the hydrogen is bound to T¼NADP so that DG (hn) is about
store
20kJmol(cid:1)1lower.Thebioenergeticlimitofphotosyntheticwatercleavageinto
molecular oxygen and metabolically bound hydrogen was reached 2–3 billion
years ago at the evolutionary level of prokaryotic cyanobacteria ([10–12]; for
furtherreading,seeChapters19and22].Thisprocessisthethermodynamically
zThesymbolDG(ATP)isasimplificationbecauseitsuggeststhatATPistheonly‘‘Gibbsenergy
currency’’inbiologicalsystems.
10 GERNOT RENGER
highest possible form of solar energy transformation into chemical Gibbs
energy that could be achieved in the biosphere.
The‘‘invention’’ofabiomoleculardevicethatenablesthisreactionhadtwo
consequences of paramount importance: (a) it allowed the water pool on the
earthsurfacetobecomeavailableashydrogensourceforthebiosphereand(b)
theresultingformationofdioxygenasaphotosynthetic‘‘waste’’productledto
the present day aerobic atmosphere [13,14], thus opening the road for a much
moreefficient(aboutoneorderofmagnitude)exploitationoftheGibbsenergy
contentoffoodthroughtheaerobicrespirationofheterotrophicorganisms(for
thermodynamic considerations, see [15,16]). Accordingly, the ‘‘discovery’’ of
oxygenic photosynthesis and the concomitant formation of an aerobic atmo-
spherewasthebioenergeticprerequisiteforthedevelopmentofallhigherforms
of life on earth. Furthermore, the release of molecular oxygen led to the
generation of the stratospheric ozone layer as the indispensable protective
‘‘umbrella’’ against deleterious UV-B irradiation.
Astheresultoftheinterplaybetweenoxygenicphotosynthesisandrespiration
a global steady state emerges that can be summarized by the overall equation:
oxygenicphotosynthesis
CO2þH2O (cid:1) !(cid:1) (cid:1)CH2O(cid:1)þO2 ð2Þ
respiration
where –CH O– represents a unit of carbohydrate.
2
However, the great bioenergetic advantages of life under aerobic conditions
are only one side of the ‘‘oxygen coin’’ – the other is the toxicity of molecular
oxygen[17].Becauseofthelatter,theglobalaccumulationofmolecularoxygen
in the atmosphere and, in particular, the dissolved gas in the oceans was
disastrousforalmostallexistingorganisms.Thevastmajoritywereeventually
killed, a small fraction survived in anoxygenic ecological niches (for broader
discussionsofthedualroleofmolecularoxygenandtheimplicationsforthelife
on earth, see [17]).
InadditiontoitsparamountroleastheindispensableGibbsenergysourcefor
the biosphere, solar radiation is also most important for information transfer.
Signalingbylightiswellknownfortheprocessofvisionbutitalsogivesriseto
a multitude of other processes such as the ticking of ‘‘biological clocks’’,
morphogenesis via light-regulated gene expression, triggering of enzyme acti-
vitiesandphototacticmovementsofmicroorganisms.Theseprocessescompris-
ingdifferenttypesofphotoreceptors(see[18–21]andreferencestherein).Figure
2 gives a simplifiedschematicsummary of theessential light-inducedprocesses
in biological organisms.
This book focuses on a description of the bioenergetic function of light
through its photosynthetic transformation into chemical Gibbs energy. The
overall process of photosynthesis consistsof, essentially, two types of reaction
sequences: (a) an electron transport chain with light energy as driving force,
leading to the formation of suitable metabolically bound hydrogen (mostly
NADPH) and ATP. This sequence is often summarized by the term ‘‘primary
processes of photosynthesis’’, and (b) a chain of enzyme-catalyzed steps that
OVERVIEW OF PRIMARY PROCESSES OF PHOTOSYNTHESIS 11
Figure 2. Overall scheme of generation and transformation of electronically excited
states(symbolizedbyP*)inbiologicalsystems.
i
give rise to CO fixation with the products of the ‘‘primary processes’’, with
2
NADPH and ATP acting as powerful hydrogen donor and Gibbs energy
source, respectively. The overall reaction sequence of the Calvin–Benson cycle
leading to CO fixation can be summarized by the equation:
2
2NADPH þ 3ATP4(cid:1) þ CO þ 2H O!
2 2
ð3Þ
(cid:1)CH O(cid:1) þ2NADP þ þ 3ADP3(cid:1) þ 3P2(cid:1) þ Hþ
2 i
where –CH O– symbolizes a carbohydrate unit and P2(cid:1) is HPO2(cid:1); the proto-
2 i 4
nation states of the species are those attained at physiological pH values.
The Calvin–Benson cycle reactions [6–8] are sometimes referred to as ‘‘sec-
ondary processes of photosynthesis’’. They do not contribute to solar energy
transformation into Gibbs energy but rather provide a transduction of the
productsofthe‘‘primaryprocesses’’intosubstancesthataremoreappropriate
for long-term storage. An extreme example of most important relevance for
mankind’s technological way of life are the fossil Gibbs-energy resources oil
and coal. The total fossil fuel reserve is estimated to be about 4(cid:3)1019 kJ (see
[4]), corresponding to about 100 times the current annual photosynthetic
carbon dioxide fixation.
Thischapterprovidesnotonlyabriefsummaryonthegeneralfeaturesofthe
‘‘primary processes of photosynthesis’’ but its more ambitious goal is to
stimulate the readers’ interest on detailed information about apparatus and
mechanismsofthiskeypartofphotosynthesisSubsequentchapters,writtenby
leading experts, provide excellent descriptions of different facets of this fasci-
nating field.