Vol 437|22 September 2005
NEWS & VIEWS
483
ENVIRONMENTAL SCIENCE
The carbon cycle under stress
Dennis Baldocchi
In the summer of 2003, Europe experienced an exceptionally hot and dry spell. That ‘natural experiment’ prompted
a continental-scale analysis of how terrestrial ecosystems respond to such climatic extremes.
Plant ecosystems are major players in the car-
bon cycle — they take up carbon dioxide in
photosynthesis and release it in respiration at
rates that are nonlinear functions of tempera-
ture. How net carbon exchange by terrestrial
ecosystems will be affected by projected global
warming, and by the increased incidence of
extreme climatic events, is a question under
intense investigation. Ciais et al.1 (page 529 of
this issue) have taken advantage of an episode
of heat and drought that affected Europe
during the summer of 2003 to evaluate how
net carbon exchange of ecosystems responded.
The context to this research is well known.
Anthropogenic combustion of fossil fuels has
caused mean concentrations of CO2 in the
atmosphere to reach and exceed 380 parts per
million (p.p.m.)2, a level that is about 100
p.p.m. greater than in pre-industrial times3.
Because CO2 absorbs long-wave energy, it
warms the Earth’s atmosphere. Additional
inputs of carbon to the atmosphere will pro-
duce further warming and may contribute to
the occurrence of more-intense spells of heat4.
But how can we estimate the effects of warm-
ing trends and extreme events on ecosystem
photosynthesis and respiration?
Manipulative experiments that warm
ecosystems with infrared lamps provide some
insight into these questions5. However, such
studies are generally confined to short vegeta-
tion in small plots, so their findings do not
scale well to the dimensions of forests and con-
tinents. Natural experiments are an alternative
approach to studying how ecosystems may
respond to warming. They also provide infor-
mation on how ecosystems co-vary with ele-
vated CO2 and ozone, and with a reduction in
rainfall. But such experiments are feasible only
when environmental conditions exceed some
threshold or range of conditions. For much of
the past century, natural warming experiments
have been hindered by the fact that many
potential cases have fallen within the natural
climatic variability attributed to events such as
El Niño/La Niña, volcanic eruptions, the North
Atlantic Oscillation and the Pacific Decadal
Oscillation6. This situation is now changing as
global and regional temperature trends begin
to rise above natural climatic variability7.
The summer of 2003 in Europe is a parti-
cular case worth studying (Fig. 1). Rainfall
dropped 50% below the long-term norm. More
notably, mean air temperatures exceeded the
average of direct measurements made since
1851 by more than 6
C (see ref. 8, for exam-
ple). According to data derived from the timing
of the grape harvest in Burgundy9, this heat
spell has had no equal since 1370.
Ciais et al.1 have investigated this case by
gleaning direct and long-term carbon flux
measurements from the CarboEuroflux net-
work and crop-yield data. They also inferred
regional-scale carbon fluxes using measure-
ments from the satellite-based Moderate
Resolution Imaging Spectroradiometer, and
calculations from a regional carbon-cycle
model. They report that the 2003 heat
spell, combined with the drought, caused a
195 g C m2 yr1 decline in ecosystem photo-
synthesis and a reduction in ecosystem respira-
tion of 77 g C m2 yr1. And because the
decline in respiration was outpaced by the
reduction in photosynthesis, Europe experi-
enced a net annual loss of 0.51015 g of car-
bon when the information was integrated
across the continent.
The length of the photosynthetic growing
season is another temperature-sensitive process
that is increasing across Europe10 and contri-
butes to accumulated photosynthesis. Ciais et al.
report that climate conditions preceding the
summer of 2003 resulted in an earlier spring-
time initiation of photosynthesis compared
with 2002, the reference case. This extra carbon
assimilation offset the reduction in photosyn-
thesis in the summer of 2003. Whether contin-
ued lengthening of the photosynthetic growing
season will be correlated with summertime
drought and heat remains to be seen. But if
it is, it will mitigate the detrimental effects of
drought and extreme heat on the annual carbon
balance of European ecosystems.
Are these results applicable to similar situa-
tions on other continents, and can the conse-
quences be projected into the future? Here we
must consider how heat and drought conspire
to affect short-term physiological and long-
term ecological processes. The discovery that
heat and drought stresses reduced both photo-
synthesis and respiration provides new infor-
mation for constraining models that couple
climate with the carbon cycle. Such models
have previously assumed that drought and
warming stif le photosynthesis but increase
respiration11. In the former situation, per-
turbations in ecosystem photosynthesis and
respiration will increase atmospheric CO2
and amplify the carbon-cycle feedback on
climate warming.
The strength of the observed reduction in the
photosynthesis of European forests may not be
Figure 1 | Consequences
of heat and drought. A
parched field in Lavaur,
southern France, in July 2003.
P.
P
A
V
A
N
I/
A
FP
/G
ET
TY
IM
A
G
ES
22.9 N&V 483 MH 16/9/05 5:34 PM Page 483
Nature Publishing Group© 2005

NEWS & VIEWS NATURE|Vol 437|22 September 2005
484
felt by forests in North America under similar
conditions of temperature and rainfall. This is
because, in North America, temperate forests
generally experience higher summertime tem-
peratures than do forests in Europe. Over time,
their photosynthetic machinery has accli-
mated, causing their photosynthetic rates to
peak at higher temperatures than for forests in
Europe12. And because the temperature sensi-
tivity of photosynthesis is very plastic, it is rea-
sonable to expect that forests will acclimate if
mean temperatures continue to rise gradually
across Europe, thereby modulating the negative
response to temperature reported by Ciais and
colleagues. A repeat of extreme temperatures in
the near term, on the other hand, could have
detrimental, even lethal, consequences.
One indirect but long-term effect would be a
replacement of current forest vegetation with
other species. But here again caution is neces-
sary. Many forests in Europe and North Amer-
ica have been regrowing since major harvesting
ceased around the end of the nineteenth and
beginning of the twentieth centuries. So even if
Europe’s climate were to remain steady, one
may expect certain levels of species transition.
Another long-term effect of reduced photo-
synthesis and growth involves the link between
the fall of leaf litter, and its decomposition and
provision of nutrients for photosynthesis and
plant growth the following year. Ciais and col-
leagues’ study did not last long enough to pro-
vide insight into this process, but a reduction in
subsequent photosynthesis can be expected.
Finally, the report1 shows how episodes of
heat and drought will affect the ability of Euro-
pean countries to comply with the require-
ments of the Kyoto Protocol to reduce carbon
emissions by limiting fossil-fuel combustion
or increasing terrestrial carbon sinks. One
potential outcome would be the production of
real-time information on carbon cycling, so
that fossil-fuel combustion could be adjusted
as the weather changes. Achieving such a
goal, however, would require an integrated
modelling system that predicts weather and
carbon cycling in tandem, and the expansion
of satellite- and field-measurement systems
that would feed such a model. ■
Dennis Baldocchi is in the Department of
Environmental Science, Policy and Management,
137 Mulford Hall, University of California, Berkeley,
Berkeley, California 94720, USA.
e-mail: baldocchi@nature.berkeley.edu
1. Ciais, Ph. et al. Nature 437, 529–533 (2005).
2. Keeling, C. D. & Whorf, T. P. in Trends: A Compendium of
Data on Global Change (Carbon Dioxide Information
Analysis Center, Oak Ridge Natl Lab., Oak Ridge, TN, 2005).
3. Petit, J. et al. Nature 399, 429–436 (1999).
4. Meehl, G. A. & Tebaldi, C. Science 305, 994–997 (2004).
5. Harte, J. et al. Ecol. Appl. 5, 132–150 (1995).
6. Jones, P. D. & Mann, M. E. Rev. Geophys. 42,
doi:10.1029/2003RG000143 (2004).
7. Jones, P. D. & Moberg, A. J. Clim. 16, 206–223 (2004).
8. Stott, P. A., Stone, D. A. & Allen, M. R. Nature 432, 610–613
(2004).
9. Chuine, I. et al. Nature 432, 289 (2004).
10. Menzel, A. & Fabian, P. Nature 397, 659 (1999).
11. Cox, P. M. et al. Nature 408, 184–187 (2000).
12. Falge, E. et al. Agric. For. Meteorol. 113, 53–74 (2002).
nevertheless, their evolutionary origin is pre-
served in their three-dimensional structure.
Second, the structure shows how domains
with specialized functions have been added
to the core through a series of gene insertion
events. For example, the warhead is contained
within the thioester domain (TED), a helical
domain that has been crystallized previously
as an isolated fragment3. This previous work
demonstrates that TED can fold autonomously,
and the implication is that it once existed as a
separate protein, although there is nothing like
it today. TED lies in a loop within a third type
of domain, CUB (ref. 4), which in turn fits
between the MG7 and MG8 domains of the
core. And another domain, called anaphyla-
toxin (ANA), is inserted in a loop within the
MG6 domain.
Why insert the thioester domain in a larger
protein? In short: regulation. To be an effective
but selective killing machine, C3 must patrol
the bloodstream in an inactive form until it
encounters ‘non-self ’ (for example, bacteria
and viruses). Activation occurs by cleavage of
C3 at specific sites (in inserted domains), result-
ing in the generation of the active fragments,
C3b and C3a. By comparing the conformation
of full-length C3 with that of the inactivated
fragment (C3c) and with the structure of the
isolated TED3, Gros and colleagues propose
how the molecular warhead of C3 is armed
(Fig. 1)2. Two steps are involved: first C3 is phys-
ically uncovered, then it is chemically primed.
STRUCTURAL BIOLOGY
Origins of chemical biodefence
Robert Liddington and Laurie Bankston
The idea that complex biological systems can evolve through a series of
simple, random events is not universally accepted. The structure of a vital
immune protein shows how such evolution can occur at a molecular level.
Before antibodies evolved, primitive multi-
cellular organisms devised a general defence
system against bacterial and viral invaders
called ‘innate immunity’. The system has sur-
vived in vertebrates with its core components
little changed during the intervening 700 mil-
lion years1. A central element of this defence
strategy is an activated thioester — a molecu-
lar warhead — that is today used only in this
setting, perhaps because it is potentially so
destructive. The protein C3, a member of a
small family of related proteins carrying this
warhead, is a large molecule of the ‘comple-
ment’ system, which identifies foreign agents
and targets them for destruction. On page 505
of this issue, Gros and colleagues2 present the
atomic-resolution crystal structure of C3, as
well as that of an inactivated fragment, C3c.
From the structure of C3, it is immediately
apparent how this large multi-domain protein
evolved from a series of simpler building-
blocks into a tightly regulated killing machine
(Fig. 1). First, the core of C3 is composed of
eight copies of a simple three-dimensional
motif, which Gros et al. term ‘macroglobulin’
(MG1–MG8), arranged in tandem. The pres-
ence of these repeated domains suggests that
the core arose through duplications of a pri-
mordial gene that originally encoded a single
domain. Random mutations occurring over
hundreds of millions of years mean that the
component amino-acid sequences of individ-
ual domains no longer share any similarity;
Figure 1 | Arming the warhead. Model of the conformational changes that occur on cleavage and
activation of complement component C3 to yield the active fragments C3a/ANA and C3b, based on
the structure reported by Gros and colleagues2. Proteolytic cleavage of C3 on the pathogen surface
releases C3a/ANA from C3b, allowing macroglobulin domain 8 (MG8) to swing away from the
thioester domain (TED). This exposes the thioester (white triangle) and enables a switch to an active
conformation in which a histidine (red pentagon) reacts covalently with the thioester to form the
armed warhead. Further cleavage (not shown) leads to loss of the TED and CUB (‘complement
C1r/C1s, Uegf, Bmp1’) domain, yielding the inactivated fragment, C3c.
22.9 N&V 483 MH 16/9/05 5:34 PM Page 484
Nature Publishing Group© 2005