Molecular to global photosynthesis m archer (worldsci, 2004)

MOLECULAR TO GLOBAL
PHOTOSYNTHESIS


SERIES ON PHOTOCONVERSION

OF SOLAR ENERGY

Series Editor: Mary D. Archer (Cambridge, UK)

Vol. 1: Clean Electricity from Photovoltaics
eds. Mary D. Archer & Robert Hill
Vol. 2: Molecular to Global Photosynthesis
eds. Mary D. Archer & Jim Barber

Forthcoming
Photochemical and Photoelectrochemical Approaches to Solar Energy Conversion
eds. Mary D. Archer &Arthur J. Nozik
From Solar Photons to Electrons and Molecules
by Mary D. Archer


Series on Photoconversion of Solar Energy

-Vol. 2

MOLECULAR TO GLOBAL
PHOTOSYNTHESIS
Editors

Mary D. Archer
Imperial College, UK

James Barber
Imperial College, UK

Imperial College Press


Published by
Imperial College Press
57 Shelton Street
Covent Garden
London WC2H 9HE

Distributed by
World Scientific Publishng Co. Pte. Ltd.

5 Toh Tuck Link, Singapore 596224
USA office: Suite 202, 1060 Main Street, River Edge, NJ 07661

UKoffice: 57 Shelton Street, Covent Garden, London WC2H 9HE

Library of Congress Cataloging-in-PublicationData
Archer, Mary D.
Molecular to global photosynthesisI editors, Mary D. Archer, James Barber.
p. cm. - (Series on photoconversion of solar energy; v.2)
Includes bibliographical references and index.
ISBN 1-86094-256-3
1. Photosynthesis. 2. Energy crops. 1. Archer, Mary D. 11. Barber, J. (James), 1940111. Title. IV. Series.

QK882 .M84 2004
662’.8--dc22

200404401 1

British Library Cataloguing-in-Publication Data
A catalogue record for this book is available from the British Library

Copyright 0 2004 by Imperial College Press

All rights reserved. This book, or parts thereoj may not be reproduced in any form or by any means,
electronic or mechanical, including photocopying, recording or any information storage and retrieval
system now known or to be invented, without written permissionfrom the Publisher.

For photocopying of material in this volume, please pay a copying fee through the Copyright
Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, USA. In this case permission to
photocopy is not required from the publisher.
Desk Editor: Tan Rok Ting
Artist: Lionel Seow
This book is printed on acid-free paper.
Printed in Singapore by Mainland Press


This volume is dedicated

to

George Porter
The Rt Hon The Lord Porter of Luddenham OM FRS
Nobel Laureate

1920- 2002

a fine man and a great scientist


This page intentionally left blank


CONTENTS
xi

About the authors

xix

Preface
1 Photosynthesis and photoconversion
J . Barber and M. D. Archer

1.1
1.2
1.3
1.4
1.5
2

Introduction
Evolution and progress of ideas
The 'blue print' of the photosynthetic apparatus
Energy-storage efficiency of photosynthesis

Energy and chemicals from biomass

1
12
18
28
34

Light absorption and harvesting
A. Holzwarth

43

2.1 Introduction
2.2 Theoretical aspects of energy transfer in photosynthetic
antennae
2.3 General principles of organisation of light-harvesting antennae
2.4 Structural and functional basis for light absorption and
harvesting
2.5 Concluding remarks
3 Electron transfer in photosynthesis
W. Leibl and P. Mathis

3.1
3.2
3.3
3.4
4

1

43
47
51
53
81

117

Biological electron transfer
Electron transfer in anoxygenic photosynthesis
Electron transfer in oxygenic photosynthesis
Photosynthetic electron transfer: importance of kinetics

119
123
141
163

Photosynthetic carbon assimilation
G. E. Edwards and D. A. Walker

189

4.1 Environmental and metabolic role
4.2 Chloroplast and cell
4.3 C3 photosynthesis in its relation to the photochemistry
vii

189

191
192


...

Contents

Vlll

4.4
4.5
4.6
4.7
4.8
5

The Calvin cycle
Autocatalysis: adding to the triose phosphate pool
Photorespiration
C02-concentrating mechanisms
Survival and efficiencies of photosynthesis

194
203
204
209
216

Regulation of photosynthesis in higher plants

D. Godde and J. F. Bornman

221

5.1 Anatomy, morphology and genetic basis of
photosynthesis in higher plants
5.2 Adaptation of photosynthetic electron transport to
excess irradiance
5.3 Regulation of photosynthetic electron transport
by COz and oxygen
5.4 Feedback regulation of photosynthesis
5.5 Factors limiting plant growth
5.6 Possible plant responses to future climate changes
5.7 Improving plant biomass
6 The role of aquatic photosynthesis in solar energy
conversion: a geoevolutionary perspective
P. G. Falkowski, R. Geider and J. A. Raven
6.1 Introduction
6.2 From the origin of life to the evolution of oxygenic
photosynthesis
6.3 Photophysiological adaptations to aquatic environments
6.4 Quantum yields of photosynthesis in the ocean
6.5 Net primary production in the contemporary ocean
6.6 Biogeochemical controls and consequences
7
7.1
7.2
7.3
7.4

222
226
238
239
242
250
25 8

287
287
288
29 8
306
307
311

Useful products from algal photosynthesis
R. Martinez and Z. Dubinsky

323

Introduction
Microalgae
Macroalgae
Concluding remarks

323
326
353
366

Contents

8 Hydrogen production by photosynthetic microorganisms
V. A. Boichenko, E. Greenbaum and M. Seibert
8.1 Photobiological hydrogen production-a useful evolutionary
oddity
8.2 Distribution and activity of H2 photoproducers
8.3 Structure and mechanism of the enzymes catalysing Hz
production
8.4 Metabolic versatility and conditions for hydrogen evolution
8.5 Quantum and energetic efficiencies of hydrogen
photoproduction
Hydrogen
production biotechnology
8.6
8.7 Future prospects

9

Photoconversion and energy crops
M. J. Bullard

Introduction
Why grow energy crops?
The nature of biomass
Physiological and agronomic basis of energy capture and the
selection of appropriate energy crop species
9.5 Conclusions

9.1
9.2
9.3
9.4

10 The production of biofuels by thermal chemical
processing of biomass
A. V. Bridgwater and K. Maniatis
Introduction
Thermal conversion processes
Gasification
Pyrolysis
Co-processing
Economics of thermal conversion systems for electricity
production
10.7 Barriers
10.8 Conclusions

10.1
10.2
10.3
10.4
10.5
10.6

1x

397

397
400
410
418
422
425
432

453

453
455
475
484
504

521
522
527
529
5 64
59 1
599
602
604


Contents

X

11 Photosynthesis and the global carbon cycle
D. Schimel
11.1
11.2
11.3
11.4
11.5
11.6

The contemporary carbon cycle
The modern carbon budget
Photosynthesis as a carbon storage process
Assimilation and respiration
C 0 2 fertilisation
Global warming and the carbon cycle

12 Management of terrestrial vegetation to mitigate climate
change
R. Tipper and R. Carr
12.1 Potential carbon management activities in the forestry and
land use sectors
12.2 Forests and land use in the Kyoto Protocol
12.3 Climate change management, carbon assets and liabilities
12.4 Experiences and issues arising from land use and forestry
projects designed to mitigate greenhouse gas emissions
12.5 Conclusions

13 Biotechnology: its impact and future prospects
D. J. Murphy

13.1
13.2
13.3
13.4
13.5
13.6
13.7
13.8

613
614
615
618
619
62 1
622

629

629
636
639
640
643

649

Introduction
Background
Agbiotech: current applications

Transgenic crops: the future
Challenges for transgenic crops
Developing new crops
Future directions for agricultural biotechnology
Conclusions

649
652
663
683
703
7 15
719
726

Appendices

741

I Conversion Factors
I1 Acronyms and Abbreviations
111 List of Symbols

Index

74 1
742
745

747

ABOUT THE AUTHORS
Mary Archer read chemistry at Oxford University and took her PhD from Imperial
College, London, in 1968. From 1968 to 1972, she did post-doctoral work in electrochemistry with Dr John Albery at Oxford, and she then spent four years at The Royal
Institution in London, working with Lord Porter (then Sir George Porter) on photoelectrochemical methods of solar energy conversion. She taught chemistry at Cambridge
University, 1976-86. From 1991 to 1999, she was a Visiting Professor in theDepartment
of Biochemistry at Imperial College, London, and from 1999 to 2002, she held a Visiting
Professorship at ICCEPT (Imperial College Centre for Energy Policy and Technology).
She is President of the UK Solar Energy Society and the National Energy Foundation, a
Companion of the Institute of Energy and a member of the Royal Society’s Energy Policy
Advisory Group. She was awarded the Melchett Medal of the Energy Institute in 2002.
Jim Barber works on the molecular processes of photosynthesis as the Ernst Chain
Professor of Biochemistry at Imperial College, London. After graduating as a chemist
from the University of Wales, he gained his PhD in biophysics from the University of
East Anglia. Following a post-doctoral year in Holland, he joined the staff at Imperial
College as a lecturer in 1968. He was Dean of the Royal College of Science, 1988-89,
and head of the Biochemistry Department of Imperial College, 1989-99. He continues as
Director of the Centre for Photomolecular Sciences at Imperial College. Much of his
research has focused on the reactions and proteins involved in the photochemically-driven
oxidation of water. He was elected to the European Academy (Academia Europaea) in
1989 and he was awarded the Flintoff Medal of the Royal Society of Chemistry in 2002.

Vladimir Boichenko is a senior researcher and project leader at the Institute of Soil
Science and Photosynthesis of the Russian Academy of Sciences. He graduated from
Voronezh State University in 1971, and received his doctor’s degree from Moscow State
University in 1980. His scientific interests centre on the functional organisation of the
photosynthetic apparatus and mechanisms of oxygen and hydrogen photoproduction. He
has published about sixty papers in this field, collaborating extensively with colleagues in
Hungary and Germany.

Janet Bornman is Research Director of the Department of Plant Biology at the Research
Centre Flakkebjerg, Slagelse, Denmark, which forms part of the Danish Institute of
Agricultural Sciences (DIAS). She is interested in the interplay of stress factors in plants
and the mechanisms behind acclimation and longer-term adaptation with regard to plant
quality and performance. Her areas of research include the potential interactive effects of
xi


xii

About the authors

several environmental factors on plant crops, such as ultraviolet radiation, high visible
irradiance, drought and temperature, as well as the measurement of internal light
microenvironments within plant material using fibre optics. She is a member of the
Environmental Effects Panel of the United Nations Environment Programme (UNEP) that
is concerned with depletion of the ozone layer and global climate changes. She is
currently President of the European Society for Photobiology, and Scientific Editor of the
journal Physiologia Plantarum.

Tony Bridgwater is a Professor of Chemical Engineering at Aston University in
Birmingham, specialising in thermal conversion of biomass for production of fuels and
chemicals. He obtained his first degree in Chemical Engineering from UMIST, followed
his PhD and DSc from Aston. Most of his professional career has been spent at Aston
University, where he leads the Bio-Energy Research Group and heads the Chemical
Engineering and Applied Chemistry Department. His current interests are focussed on the
development of both the technologies for fast pyrolysis of biomass and the fuel and
chemical products that can be derived from the liquids. He leads the biomass pyrolysis
network PyNe sponsored by the EC and IEA Bioenergy.
Mike Bullard is the Managing Director of Bio-Renewables Ltd, a company established

in 2002 in order to develop energy crops commercially in the UK. After gaining his
doctorate from the University of York, and a brief period working at the Department of
Agricultural and Environmental Science at the University of Newcastle, he spent his
career at ADAS’ Arthur Rickwood Research Station in Cambridgeshire, UK, most
recently leading the novel crops programme, until leaving to establish the new company.
His current research interests are the optimisation of yield and quality in Miscanthus spp.
and Suliw spp., the development of small-scale electricity generation units fuelled by
biomass, and the development of next-generation technologies such as bio-hydrogen.
Rebecca Carr is a forestry and land use consultant at the Edinburgh Centre for Carbon
Management (ECCM). She gained her degree in Ecological Science from the University
of Edinburgh, during which she spent a year at Queens University, Canada and took part
in a community project in the Philippines. Her thesis looked at restoration of floodplain
woodlands with the Borders Forest Trust. Since joining ECCM, she has worked on
assessment of the carbon-offset potential of planting schemes throughout the UK.
Currently she is providing technical advice on carbon sequestration to the Scottish Forest
Alliance and working on a European project looking at synergies between carbon
verification and forest certification processes.


About the authors

...

Xlll

Zvy Dubinsky graduated in 1978 from the Department of Life Sciences at Bar Ilan
University, Israel, where he is a member of the faculty. His research interests include the
energy conversion efficiencies of algal communities, the remote sensing of phytoplankton
dynamics, the biochemistry of algal pigments, photoadaptation of the photosynthetic
apparatus, combined systems for sewage treatment and algal protein production, and the

potential of microalgae as sources of fine chemicals and pharmaceuticals. He is currently
working on projects with Rockefeller University, New York (photoacoustic determination
of phytoplankton biomass and the rate of photosynthesis), Brookhaven National
Laboratory (biological oceanography) and Germany, Egypt, Jordan and the Palestinian
Authority (marine science and coral conservation in the Red Sea).
Gerry Edwards is Professor of Botany in the School of Biological Sciences, Washington
State University. His area of expertise is Cq photosynthesis, with particular emphasis on
environmental stress. He was awarded his doctorate from the University of California,
Riverside, in 1969. Subsequently, he worked at the University of Georgia as a National
Institutes of Health postdoctoral fellow, and then moved to the Horticulture Department,
University of Wisconsin, Madison, rising to the rank of Professor. In 1981, he relocated
to the Botany Department, Washington State University, serving as its chairman until
1986. Currently, besides being Professor of Botany, he is also a Fellow of the Institute of
Biological Chemistry and Adjunct Professor of Horticulture and Landscape Architecture.
Over the course of his career, Dr. Edwards has received both a Guggenheim Fellowship
and a Fulbright Fellowship. His current research projects include several collaborations,
with topics ranging from effects of UV-B radiation, to bioenergetics of C4photosynthesis,
to source-sink relationships in rice, to studies on the diversity of C4photosynthesis in the
family Chenopodiaceae.
Paul Falkowski is a Professor in the Institute of Marine and Coastal Sciences and
Department of Geology at Rutgers University, New Jersey. He obtained his BSc and MA
from the City College of New York, and a PhD in Biology from the University of British
Columbia. His research interests include biophysics, photosynthesis, photobiology,
molecular evolution, signal transduction, apoptosis, biogeochemical cycles, and
symbiosis. He is a John Simon Guggenheim Fellow, a Fellow of the American
Geophysical Union, a Cecil and Ida Green Distinguished Professor, and the recipient of
the Huntsman Medal and Hutchinson Award. He has authored or co-authored over 190
papers in peer-reviewed journals and books, and has co-invented and patented a
fluorosensing system which is capable of measuring phytoplankton photosynthetic rates
non-destructively and in real time. Falkowslu lives in Princeton, New Jersey with his wife

and two daughters.


xiv

About the authors

Richard Geider is a Professor in the Department of Biological Sciences at the University
of Essex. After gaining his doctorate in Biological Oceanography from Dalhousie
University, Canada in 1984, he held post-doctoral positions at the University of Dundee,
Scotland and at the University of Birmingham, England, before taking up a faculty
position at the University of Delaware, USA, in 1988. He became a Fellow of the Marine
Biological Association of the United Kingdom in 1995, and moved to his current post at
the University of Essex in 1999. His current research includes laboratory, field and
theoretical studies of the factors that limit primary productivity in the sea.

Doris Godde studied biology and chemistry at Ruhr University, Bochum,Germany. Her
PhD work in the Department of Plant Biochemistry with AchimTrebst was concerned
with solar energy conversion and photosynthetic hydrogen production. In 1982 she went
to Dartmouth College, USA for a year to work on a bacterial menaquinone-cytochrome c
oxidoreductase with Bernhard Trumpower. After the birth of her two sons she worked on
a joint project of the Departments of Plant Ultrastructure and Experimental Physics at
Ruhr University on element distribution in plants. In 1989 she returned to the Department
of Plant Biochemistry, where she worked on the regulation of photosynthesis under stress
conditions. In 1995 she received her Habilitation from the Faculty of Biology and is now
Privat-Dozentin.
Elias Greenbaum is an Oak Ridge National Laboratory Corporate Fellow and Adjunct
Professor of Biotechnology at The University of Tennessee. He is a fellow of the
American Physical Society and the American Association for the Advancement of
Science. His main areas of research are the physico-chemical mechanisms of photosynthesis and their application to the production of renewable fuel and chemicals. He is a

recipient of the US Department of Energy’s Biological and Chemical Technologies
Research Program Award.

Alfred Holzwarth has worked at the Max-Planck Institute for Radiation Chemistry in
Miilheim, Germany since 1977, and has also held a Visiting Professorship at Heinrich
Heine University, Dusseldorf since 1993. His research interests centre round the study of
structure/function relationships and dynamics in pigment-protein complexes and the
design of artificial photosynthetic units based on self-organised photoactive nanodevices
with energy and electron transfer competence. He obtained his Diploma in Chemistry
from the Eidgenossische Hochschule in Ziirich in 1974, his PhD in Physical Chemistry
from the ETH Ziirich in 1977 and his Habilitation from Phillips University, Marburg in
1987.


About the authors

xv

Winfried Leibl graduated in Physics from the University of Regensburg in his home
country, Germany. He then decided on a research career in the field of Biophysics and
completed his PhD at the University of Osnabruck in 1989. A post-doctoral fellowship
from the Deutsche Forschungsgemeinschaftbrought him to the Bioenergetics Section at
CEA Saclay, France, where he set up time-resolved photovoltage measurements in the
picosecond and nanosecond time range. He is currently a research scientist at the
institute. His main research interests are structure-functionrelationships in bioenergetics,
and the kinetics of electron and proton transfer in photosynthetic reaction centres.
Kyriakos Maniatis is a Principal Administrator with the Directorate General for Energy
and Transport of the European Commission, where he is responsible for the sector of
Energy from Biomass and Waste in the unit for New & Renewable Energy Sources. After
obtaining his PhD from Aston University, Birmingham, he worked as an Adjunct

Assistant Professor at the Vrije Universiteit, Brussels and as a consultant for various
companies, research institutes and international organisations before joining the European
Commission. His main expertise is in thermochemical conversion of biomass and waste.
In addition to the management of about 60 research contracts on biomass and waste on
behalf of DG TREN, he is also involved in policy development on waste and renewable
energy sources. During 1999-2001, he served as Vice-chairman of the International
Energy Agency’s Executive Committee for Bioenergy.
Rosa Martinez obtained her PhD at the University of Valencia, Spain in 1973, and is
currently Professor of Ecology in the Department of Water Science and Technology at
the University of Cantabria, Spain. Her research interests include plankton production
and respiration, Antarctic plankton biochemistry and ambient-driven gene expression in
phytoplankton. She has participated in several national and international oceanographic
cruises. Presently, she is working on a European Union project with partners from
Sweden, France, Norway and Germany, dealing with harmful dinoflagellate blooms, and
a Spanish project on toxic diatoms.
Paul Mathis received a degree in agricultural sciences in Paris, followed by a PhD in
physical chemistry on transient states in carotenoids and post-doctoral training in
Berkeley. In Saclay, he set up several instruments for flash absorption spectroscopy and
used them to study functional properties of photosynthetic reaction centres. His present
interest lies in electron transfer in purple photosynthetic bacteria. He is the head of the
Bioenergetics Section of the French Atomic Energy Commission in Saclay, a former
President of the French Photobiology Society and past-President of the International
Society for Photosynthesis Research.


xvi

About the authors

Denis Murphy is a well-known researcher in plant molecular and cell biology,

particularly in the area of seed development and lipid metabolism. He has published over
100 research papers, written numerous reviews and edited a book on biotechnology. He
has also been involved in a variety of public events relating to agbiotech, ranging from
media interviews to debates in schools and universities. He received his PhD in plant
biochemistry from York University, UK in 1977, and was then awarded a Fulbright
Scholarship at the University of California, where he spent three years working on lipid
biochemistry. He subsequently did post-doctoral fellowships at the Sheffield and Munster
Universities and the Australian National University, Canberra. In 1985,he was appointed
New Blood Lecturer at the University of Durham, where he founded the Oilseeds
Research Group. In 1990, he accepted the post of Head of the newly established Brassica
and Oilseeds Research Department at the John Innes Centre, UK, where he spent ten
years as a senior manager as well as continuing an active personal research programme.
In 1998, he was awarded an Honorary Professorship by the University of East Anglia in
recognition of his services to education and research, and he currently has a long-term
Visiting Fellowship at LEA. In 2001, he was appointed to his present post at the
University of Glamorgan.
John Raven is Boyd Baxter Professor of Biology at the University of Dundee. He has
broad interests in resource acquisition by photosynthetic organisms, and is especially
interested in aquatic phototrophs. After gaining his BA and PhD at the University of
Cambridge, UK, he stayed in Cambridge as a University Demonstrator and a Fellow of St
John’s College before moving to the University of Dundee in 1971, becoming a Professor
in 1980. Professor Raven has made contributions to the understanding of inorganic
carbon acquisition and assimilation by marine and freshwater phototrophs, the costs and
benefits of the diversity of light-harvesting systems in algae, and the implications of
variations in light harvesting, inorganic carbon acquisition mechanisms and the inorganic
nitrogen source for the trace metal requirements of aquatic phototrophs.
Michael Seibert is Principal Scientist at the National Renewable Energy Laboratory and
a Research Professor of Biology at the University of Denver and the Colorado School of
Mines. He is a Fellow of the American Association for the Advancement of Sciences and
a 1999 Glenn Awardee of the American Chemical Society. His research interests

encompass primary processes of photosynthesis including charge separation and water
oxidation, regulation of hydrogenase function and biotechnology of algal hydrogen
production. He has published over 150 papers in these areas and holds six patents.


About the authors

xvii

Richard Tipper is the Director of Carbon Asset Management for Greenergy Carbon
Partners and the Edinburgh Centre for Carbon Management. Over the past seven years,
he has worked on the development of systems to facilitate the generation and
management of climate change mitigation projects in the land use sector, particularly in
developing countries. From 1996 to 2001, he was the leader of a project funded by the
UK government’s Department for International Development to develop a model for
carbon sequestration by forestry that could deliver benefits to rural communities in Latin
America. He was lead author on the IPCC Special Report on Land Use Change and
Forestry and has also worked as a consultant to the IEA, OECD and DETR and to a
number of private companies on issues relating to the quantification and economics of
carbon assets.
David Alan Walker is Emeritus Professor of Photosynthesis at the University of
Sheffield, and was formerly Director of the Robert Hill Institute at that university. He is
probably best known for isolating chloroplasts with intact limiting envelopes that would
support carbon dioxide-dependent oxygen evolution as rapidly as the parent leaf. Work
with these organelles led him to propose the existence of specific permeases able to
support direct obligatory exchange between external (cytosolic) orthophosphate and
internal (stromal) sugar phosphates.


This page intentionally left blank

PREFACE
In the midst of all this dwells the Sun ... Sitting upon the royal throne, he rules all the family of
planets which turn about him ... we find in this arrangement an admirable world harmony.

Nicholas Copemicus, On the Revolutions of the Heavenly Spheres, Book I, Ch. 10.

The Sun has been shining for some four and a half billion years, and is expected to do
so for as long again. It is the Earth’s only truly sustainable source of energy.
Photosynthesis, the process by which the energy of sunlight absorbed in the
chlorophyll pigments of green plants fixes atmospheric carbon dioxide (C02) to
carbohydrates, supplies us directly or indirectly with all our food. The oxygen
discarded by plants as part of this process replenishes the atmosphere with the oxygen
humans and animals need for survival.
Photosynthesis in past eras laid down the fossil fuels-oil, coal and gas-which
today supply the major portion of the world’s energy. These are being rapidly and
irreversibly consumed, and we currently contemplate global resource depletion of oil
and gas within a few decades. Only renewable sources of energy can fill this looming
gap sustainably. Present-day photosynthesis already supplies about 14% of the
world’s energy, mainly in the form of fuelwood, and photosynthesis could in future
be harnessed to provide a greater fraction of our energy needs. The end product of
photosynthesis, the organic matter called biomass, is a rich store of energy, which can
be burned to liberate heat or converted by a number of chemical and biological means
to biofuels such as methane and ethanol. In the course of this, the C 0 2 fixed in the
biomass by photosynthesis is liberated to the atmosphere once again. Thus the use of
sustainably grown biomass and energy crops as energy sources is C02-neutral and
avoids increasing the burden of atmospheric C02.
One does not need to subscribe to Jim Lovelock’s image of the Earth as the living
organism Gaia to recognise that life has adapted to the way things naturally are, and

the way things naturally are has adapted to life. What is new and unnatural about life
today is the global influence that we exert on the atmosphere and biosphere. The
burning of fossil fuels is causing atmospheric levels of C02 to rise steadily, and
damaging consequences will be avoided only if the world moves to low-carbon or
carbon-neutral sources of energy.

xix


Preface

xx

As the Prince of Wales remarked in a lecture in Cambridge some years ago,
“The strategic threats posed by global environment and development problems
are the most complex, interwoven and potentially devastating of all the
challenges to our security ... Scientists ... do not fully understand the
consequences of our many-faceted assault on the interwoven fabric of
atmosphere, water, land and life in all its biological diversity. Things could
turn out to be worse than the current scientific best guess. In military matters,
policy has long been based on the dictum that we should be prepared for the
worst case. Why should it be so different when the security is that of the planet
and our long-term future?’
This book is about photosynthesis in all its biological diversity-how it works at a
molecular level, how plants store its products, and how we may increase the amount
of carbon fixed in the biosphere and the use of biomass as an energy source to
improve the security of our planet.
We thank first our authors, who have provided such readable accounts of their
various fields and who have remained (mostly) patient through the elephantine
gestation of this book. We are also grateful to those who have worked on various

parts of this book, in particular Alexandra Anghel, Jeffrey Archer, Lynn Barber,
Barrie Clark and Stuart Honan, and to Gabriella Frescura, Laurent Chaminade, Joy
Quek and Yugarani Thanabalasingam of Imperial College Press. Before he retired,
Professor Jim Bolton wrote the earliest version of some parts of Chapter I .
Finally, we remember with gratitude and respect George Porter, our friend and
mentor at the Royal Institution and Imperial College. His early recognition that better
understanding of the mechanisms of photosynthesis would lead to improved design of
in vitro methods of solar energy conversion was the wellspring of much of his later
research. It was he who, as Chairman of the Scientific Advisory Board of Imperial
College Press, inspired this book, and the book series on the photoconversion of solar
energy of which this book constitutes the second volume.

Mary Archer
Jim Barber
Imperial College, bizdoti
October

2003


CHAPTER 1

PHOTOSYNTHESIS AND PHOTOCONVERSION
MARYD. ARCHER
Centre for Energy Policy and Technology,
Imperial College London SW7 2AZ, UK
mda 12 @cam.ac. uk
and
JAMES BARBER
Wolfson Laboratories, Department of Biological Sciences, South Kensington Campus,

Imperial College London SW7 2AZ, UK
j . barber @ imperial.ac. uk
Nature set herself the task of capturing the lightjlooding toward the earth and of storing this,
the most elusive of all forces, by converting it into an immobile force ... the plant world constitutes a reservoir in which the jleeting sun rays are fixed and ingeniously stored for future use,
a providential measure to which the very existence of the human race si inescapably bound.
Julius Robert Mayer, The Organic Motion in its Relation to Metabolism, 1845.

1.1 Introduction
The word photosynthesis means ‘building up by light’, and the process is the building
up, by plants, algae and certain bacteria under the action of sunlight, of organic
compounds (mainly carbohydrates) from two very simple inorganic molecules, water
(HzO) and carbon dioxide ( ( 2 0 2 ) . Put another way, photosynthesis is the light-driven
reduction of atmospheric carbon dioxide by water to energy-rich organic compounds.
But this reductionist, chemist’s view gives little hint of the central role of photosynthesis in sustaining life on Earth. Photosynthesis is the primary engine of the
biosphere, essential to life since it is almost the sole process by which the chemical
energy to maintain living organisms is made. It provides all our food, either directly
in the form of green plants or indirectly in the form of animals that eat green plants or
other animals that have eaten green plants. The only living organisms not sustained
directly or indirectly by photosynthesis are the chemoautotrophs, primitive bacteria
that harness the energy of inorganic compounds such as H2S to obtain the metabolic
energy they need to grow and replicate, and the organisms that feed off them. Humans
and other animals are heterotrophs-they ey cannot synthesise their own organic


2

J. Barber and M . D. Archer

compounds from inorganic sources, but must ingest them as food. Photosynthetic
organisms are photoautotrophs-able to harness solar energy to fix C 0 2 (that is, store

it in solid form as products of photosynthesis). Modern photosynthetic organisms
come in a wide range of shapes and sizes, ranging from the 1-1Opn-1-sized
photosynthetic bacteria and small, nonvascular mosses to giant sequoia trees that can
reach more than 100 m in height.

1.1.I Photosynthesis as the creator of fossil fuels and biomass
Photosynthesis in past geological eras has provided the dominant contribution to
today’s energy supplies: the fossil fuels (oil, coal and natural gas) on which we
currently so heavily depend were laid down by the decay of plant matter and marine
organisms in the Carboniferous Period between 345 and 280 million years ago.
Photosynthesis also provides an often-underrated contribution to world energy
resources today by creating biomass, the organic matter associated with living or
recently living organisms. Traditional plant and animal biomass-mainly fuelwood
and animal dung-are re important sources of non-commercial energy, currently
providing about 14% of the world’s total final energy consumption and nearly twice
that in the developing world, as shown in Table 1.1. Traditional plant biomass is,
however, often gathered and burned unsustainably, leading to deforestation, soil
degradation and net COz emissions. Only better land management techniques
throughout the developing world can prevent this.
Table 1.1

Supply and consumption of biomass energy in 1998

Mtoe

1

OECD

Non-OECD

World

TPES
of which biomass
% biomass

5097.0
169.1
3.3

4518.2
893.3
19.8

9615.2
1062.4
11.1

TFC
of which biomass
% biomass

3467.0
99.6
2.9

3178.8
842.9
26.5

6645.7
942.5
14.2

(I

= Total Primary Energy Consumption; TFC = Total Final Consumption; Biomass is here defined
as combustible renewables and (organic) wastes. All figures are in Mtoe (million tonnes of oil equivalent).
TPES and TFC differ mainly because of the inefficiency of electricity generation from burning fossil fuels.
Source: IEA World Energy Outlook 2000 (www.ieu.org/slutist/keywrZ~.
a TPES


Photosynthesis and photoconversion

Qure

1.1

3

The phormynthericrespiratory cycle. Adapted fmmHall and& (1993).

‘New’ biomass in the form of energy crops (crops grown specifically for energy
production) have only a small commercial presence today, but could make an
important contribution to future, more sustainable energy supplies. Indeed. many
experts see biomass as providing the dominant renewable energy resource in the postfossil fuel era. Production of biomass and energy crops represents one of the few
ways of turning solar energy-a fluctuating, intermittent and dilute source of
energy-into a compact, storable chemical form that can provide energy on demand.

Energy crops can simply be dried and burned to provide heat or generate electricity.
More value is added, though at a cost that is likely to be uneconomic at times of low
fossil fuel prices, by converting biomass or energy crops into biofuels by biological,
thermal or chemical means such as fermentation, pyrolysis and gasification.

1.1.2 Phorosynrhesis and the modern atmosphere

Photosynthesis in algae and higher plants provides a further vital service to man in
that it is the sole replenisher of oxygen in the atmosphere. Indeed, it was the advent of
oxygenic photosynthesis (this is oxygen-evolving photosynthesis as carried out by
green plants, discussed in Section 1.2.1) that changed the atmosphere of the Earth
from its primitive, reducing state containing virtually no frm oxygen to today’s
breathabk air. During oxygenic photosynthesis, photosynthetic organisms absorb
carbon dioxide (COz), fix it as carbohydrates (of empirical formula [CH,O]) and
discard oxygen (OL)to the atmosphere, as shown in Fig. 1.1. During respiration,
animals and plants (as well as algae) do the opposite-take in oxygen, ‘burn’ s t o r 4
carbohydrates by the process of metabolism, hence obtaining the energy needed to
sustain life. and discard carbon dioxide to the atmosphere. Animals and plants thus
live in symbiosis, but not symmetrically so. If animal rife were suddenly to ce-,
forests would reclaim agricultural land and weeds the cities, but photosynthesis would


4

J. Barber and M.D. Archer

continue to cycle oxygen and carbon dioxide through the atmosphere, missing little
more from the kingdom of Animalia than pollinating insects.
If photosynthesis were suddenly to cease, it would be altogether another matter,
because animal life could not survive for long without fresh supplies of oxygen. Some

105 net GtC' is fixed by photosynthesis on land and in the oceans each year, and this
releases about 260 Gt of oxygen into the atmosphere. The atmosphere contains
1.2 x lo6Gt oxygen, so the cycling time of oxygen through the biosphere is -4600
years. If photosynthesis were to down tools, the atmosphere would return to its
primordial reducing state on this timescale as plants and animals respired and expired.
Humans would start to suffer from hypoxia as the partial pressure of oxygen in the
atmosphere fell from its current level of 21 kPa to anything much below 15 P a . This
would hardly be our most urgent problem since we would run short of food in a
matter of months. Even if we did not (say we made food from fossil fuels or biomass),
the oxidative decay of dead trees and plants and organic carbon in soils would release
the -2500 Gt of organic carbon currently sequestered in the biosphere into the
atmosphere as C02 on a timescale of decades. Much of this would eventually dissolve
in the oceans but the atmospheric concentration of C02 would be temporarily
quadrupled and the global warming experiment would be fast-forwarded.

I . 1.3 Fluxes and sinks of photosynthetic carbon
The carbon cycle, described by David Schimel in Chapter 11, is the flow of carbon in
various chemical forms through the Earth's atmosphere, oceans, biosphere and
lithosphere. It involves chemical (geological) processes such as the formation of
carbonate rock, physical processes such as the dissolution of atmospheric carbon
dioxide in surface waters, mechanical processes such as the transport of dissolved
carbon dioxide to the deep ocean-and the biological processes of photosynthesis and
respiration. Compared with the other processes, the biological cycle is fast: although
the amounts of carbon stored in rocks and the deep ocean are much greater than those
in biomass or the atmosphere (see Fig. 1 1. l), the amount of carbon taken up annually
by photosynthesis and released back to the atmosphere by respiration is 1,000 times
greater than the annual flow of carbon through the geological cycle.

' 1 GtC = I gigatonne of carbon = lo' tonnes of carbon, a convenient unit in which to express carbon
masses in different carbon compounds on a common basis. Another unit that is often used is the

numerically equivalent PgC: 1 PgC = 1 petagramme of carbon = I O l 5 grammes of carbon = 1 GtC.