Eur. J. Phycol. (August 2003), 38: 247 – 256.
Photosynthetic field capacity of cyanobacteria of a tropical
inselberg of the Guiana Highlands
U W E R A S C H E R 1 , M I C H A E L L A K A T O S 2 , B U R K H A R D B Ü D E L 2
A N D U L R I C H L Ü T T G E 1
1
2
Institute of Botany, Darmstadt University of Technology, Schnittspahnstrasse 3 – 5, 64287 Darmstadt, Germany
Department of Biology, Botany, University of Kaiserslautern, PO Box 3049, 67653 Kaiserslautern, Germany
(Received 16 December 2002; accepted 8 April 2003)
Photosynthesis of cyanobacteria is well characterized under laboratory conditions. We present a detailed study of
photosynthetic capacity of cyanobacterial communities measured under natural conditions using chlorophyll fluorescence
techniques. Cyanobacteria of extensive and diverse communities grow epi- and endolithically on the bare rock of inselbergs
in the tropics where they are exposed to extreme and rapid fluctuations in irradiance, temperature and water availability.
Extreme and rapidly changing environmental conditions impose various stresses on cyanobacteria and lead to small-scale
niches of different communities along the furrows of an inselberg in French Guiana. These different cyanobacterial
communities can easily be separated from each other by their species composition. Moreover, cyanobacteria of these zonal
areas show significantly different rates of apparent quantum yield of photosystem II (PSII), are differently adapted to utilize
early morning light energy and have different strategies to face rapid cycles of desiccation. These different physiological
strategies have led to the development of different cyanobacterial communities in distinct zones which are determined by
different resistance to dehydration, water transport and storage capacity. In spite of the extreme environmental conditions
with very high solar radiation, predawn measurements of potential quantum yield of PS II showed that they are not
photoinhibited. We describe the manifold photosynthetic strategies that have developed in cyanobacteria under these
extreme and highly fluctuating natural conditions.
Key words: biological crust, chlorophyll a fluorescence, cyanobacterial communities, French Guiana, Gloeocapsa, inselberg,
light reaction, photosynthesis, quantum yield, Scytonema, Stigonema
Introduction
Terrestrial cyanobacteria are globally distributed
and are found in habitats as various as open rock
formations, dry and wet savannas and on the leafsurfaces of higher plants. For example, the open
rock surfaces of some inselbergs are coloured by
extensive cyanobacterial films and crusts (Büdel et
al., 1994, 1997a; Büdel, 1999), which give the
inselbergs their characteristic black colour, but
were misinterpreted by Alexander von Humboldt
in 1849 as manganese oxides. Even though there
are no quantitative estimates of the total area
covered by cyanobacteria, they undoubtedly play
an important role in the net primary production
(Medina, 1993; Büdel et al., 2000) and nitrogen
input (Forman, 1975; Lüttge, 1997; Freiberg, 1998;
Dojani et al., 2001) of tropical ecosystems. Despite
Correspondence to: U. Rascher, Columbia University, Biosphere
2 Center, PO Box 689, Oracle, AZ 85623, USA.
Tel: + 1 (520) 8385082. Fax: + 1 (520) 8385034.
E-mail: [email protected]
their possible ecological relevance, however, almost
nothing is known about the photosynthetic capacity of terrestrial cyanobacteria in the field (Büdel,
1999).
The photosynthetic apparatus of cyanobacteria
in general is similar to that described for higher
plants, but it has several peculiarities. In addition
to chlorophyll in the photosystems, their phycobilisomes with the pigments phycocyanin and phycoerythrin, primarily attached to the photosystem
II (PSII) dimers, extend the spectrum of visible
light usable for photosynthesis. It is not clear,
however, whether the phycobilisomes play a role in
protection from surplus irradiance (Campbell &
Öquist, 1996). Terrestrial cyanobacteria possess
only a small amount of zeaxanthin (DemmigAdams, 1990; Demmig-Adams & Adams, 1992),
which must be considered too low to affect heat
dissipation significantly (Leisner et al., 1994;
Lakatos et al., 2001). However, other pigments,
such as canthaxanthin, b-carotene and the myxoxanthophylls, may play an important role in heat
dissipation and photoprotection (Ibelings et al.,
ISSN 0967-0262 print/ISSN 1469-4433 online # 2003 British Phycological Society
DOI: 10.1080/0967026031000121679
U. Rascher et al.
1994; Lakatos et al., 2001; Albrecht et al., 2001).
Moreover, it is not only the visible, photosynthetically active radiation which stresses the cyanobacteria on open rocks. They are often exposed to
large fluxes of ultraviolet (UV) radiation (Büdel et
al., 2000) and produce highly effective UV-absorbing compounds, such as mycosporin-like amino
acids (MAA) and the indol alkaloid scytonemin,
which is deposited extracellularly (Garcia-Pichel &
Castenholz, 1991; Karsten & Garcia-Pichel, 1996;
Büdel et al., 1997b).
High insolation often causes high temperatures
on open rock surfaces and favours rapid desiccation of the cyanobacterial mats. However, they are
dependent on liquid water for metabolic activity, in
contrast to eukaryotic green algae which can utilize
water vapour at high relative humidity (Büdel &
Lange, 1991; Lange et al., 1989). In addition to
high irradiance and temperature, frequent cycles of
desiccation and rewetting require stable changes
between a physiologically dormant dry and an
active wet state (Scherer & Zhong, 1991). This
transition can be reliably monitored by chlorophyll
fluorescence data (Bilger et al., 1989; Lange et al.,
1989, 1999). During desiccation, DF/Fm’ and
absolute values for fluorescence yield drop dramatically within a few minutes. Thus, inactivation of
photosynthesis induced by desiccation can be
clearly distinguished from other types of photoinhibition. Interestingly the frequency and the total
quantity of rain differ between the inselbergs of wet
and dry savannas. The latter are dominated by
cyanolichens as well as green algal lichens and are,
thus, often brown-coloured (Büdel et al., 2000).
Most photosynthetic studies have been performed
under laboratory conditions with isolated and
lichenized cyanobacteria (Lange et al., 1989; Demmig-Adams et al., 1990a,b; Campbell et al., 1998;
Lange et al., 1998), and we are aware of only two
studies characterizing photosynthesis of free-living
tropical cyanobacteria under natural conditions in
the field (Lüttge et al., 1995; Büdel, 1999). Nowadays
portable chlorophyll fluorescence measurement systems allow ecophysiological studies even in extreme
habitats such as the open rock formations of tropical
inselbergs. For this work we chose an inselberg in the
tropical rain forest of French Guiana. The extended
open surface of the granite rock outcrops is densely
covered by cyanobacteria of high species diversity
(Sarthou, 1992; Sarthou et al., 1995). Over the years,
flowing water has carved furrows in the granite.
Across those furrows, which are typically 1 – 3 m
wide and 0.5 m deep, three different zones of
cyanobacterial communities can be observed: the
central zone of the furrows, an intermediate zone on
the lateral slopes of the furrows and the horizontal
rock areas above the furrows. These zones are
related to different light and water regimes across the
248
furrows and, thus, provide an excellent system to
study the ecophysiological strategies of different
cyanobacterial communities. In this survey, we give
a detailed description of the photosynthetic capacity
of cyanobacterial communities of inselbergs under
natural conditions in relation to the abiotic factors.
The aim of this work is to compare the photosynthetic response of free-living terrestrial cyanobacteria, which are subjected to rapidly changing
environmental conditions, with those of cultures,
and to investigate the varying ecophysiological
strategies which have evolved in cyanobacteria of
different microhabitats.
Materials and methods
Study site and cyanobacterial communities
All measurements were conducted on Nouragues inselberg (altitude 411 m; Fig. 1), a 400 ha outcrop of solid
granite, located in Les Nouragues national park in the
centre of French Guiana close to Les Nouragues field
station (48 05’ N, 528 40’ W). The south face (slope 20 –
40%), the so-called terrasse (Fig. 2), is covered by layers
of cyanobacterial communities, separated by small
vegetation islands (1 – 20 m diameter) mainly dominated
by Pitcairnia geysksii and Clusia sp. Mean annual
rainfall is 2920 mm, with a dry season from September
to October and decreased rainfall in February and
March. Detailed descriptions of the study site, the
abiotic conditions and the plant species occurring are
given by Sarthou (1992), Larpin (1993) and Meer (1995).
All measurements presented here were performed in
February 1999.
To characterize the ecophysiological capacity, three
cyanobacterial zones across the furrows were selected.
These three communities cover over 90% of the inselberg
outcrop and can easily be separated by their colour (Fig. 3).
Species collection and identification
Different cyanobacterial mats were collected by scraping
the cyanobacterial samples carefully off the rock with a
knife. Five samples covering an area of approximately 2
cm2 were taken from each community. The samples were
dried rapidly over silica gel and stored in a dark
container over silica gel during transport to the
laboratory. Species identification followed Geitler
(1932), Golubic et al. (1981), Anagnostidis & Komárek
(1988, 1990), Komárek & Anagnostidis (1989, 1999) and
Hoffmann (1991). Identification was performed with
crusts mounted in water under a light microscope.
Species composition was estimated as percentage cover
for each sample.
Chlorophyll fluorescence measurements
The chlorophyll a fluorescence measurements were
performed with a miniaturized pulse-amplitude modulated photosynthesis yield analyser (Mini-PAM, Walz,
Effeltrich, Germany). A special holder (Fig. 4), similar to
Photosynthesis of cyanobacteria
249
Figs. 1 –8. Study site and dominant cyanobacterial species. Fig. 1. Les Nouragues inselberg in French Guiana. Fig. 2. Aerial
view of the bare rock outcrops of the inselberg. The ‘black’ surface colour is caused by a dense layer of cyanobacteria shown here
in full sunlight. Measurements were taken at various sites along the furrows. Fig. 3. Close-up of a furrow with the three zones of
measured cyanobacterial communities. From left (centre of furrow): ‘red’ (a), ‘green’ (b) and ‘black’ (c) communities; marks
indicate measuring spots. Scale bar represents 10 cm. Fig. 4. Special holder for fibre-optics of the Mini-PAM and sensors for
light and temperature in the centre of a furrow (‘red’ community). The cyanobacteria around the holder were manually watered,
which intensified the characteristic red colour. Figs. 5 – 8. Micrographs of the dominant cyanobacteria. Scale bars represent
20 mm. Fig. 5. Gloeocapsa sanguinea. Fig. 6. Stigonema mammilosum. Fig. 7. Stigonema ocellatum. Fig. 8. Scytonema
myochrous.
the leaf-clip holder described by Bilger et al. (1995), was
gently pressed against the cyanobacterial mats on the
rocks, to fix the fibre-optics at an angle of 608 and at a
constant distance of 7 mm from the cyanobacteria. A
NiCr/Ni thermocouple was placed on the cyanobacterial
mat next to the measuring spot to record surface
temperature. Irradiance (400 – 700 nm) was measured
by the micro-quantum sensor of the Mini-PAM calibrated against a LI-COR quantum sensor (LI-190SA,
LI-COR Inc., Lincoln, USA).
Potential quantum yield of photosystem II (PSII), Fv/
Fm, was measured in the morning before sunrise, where Fv
is maximum variable fluorescence (Fv = Fm – Fo), Fm is
maximum fluorescence of the dark-adapted cyanobacteria during a saturating light flash (800 ms, 3000 mmol
m72 s71) and Fo is ground fluorescence of the darkadapted organisms. The apparent effective quantum yield
of PSII (DF/Fm’) of the light-adapted cyanobacteria was
calculated as (Fm’ – F)/Fm’, where F is fluorescence of the
light-adapted sample and Fm’ is the maximum light-
U. Rascher et al.
250
adapted fluorescence when a saturating light pulse, as
described above, is superimposed on the prevailing
environmental light levels (Genty et al., 1989; Schreiber
& Bilger, 1993; Schreiber et al., 1995). During these
measurements, care was taken not to change the ambient
conditions, e.g. by shading. Maximum apparent rates of
photosynthetic electron transport (ETR) were calculated
as 0.5 6 (DF/Fm’) 6 irradiance, where the factor 0.5
accounts for the excitation of both PSII and PSI. Light
response curves (Fig. 10B) were fitted by using a twoparameter negative exponential function, f(x) = a(1 – e(-bx))
using Sigma Plot (SPSS Inc., San Rafael, CA, USA). The
light reflection factor is not known for cyanobacterial
mats, and no correction was made for reflection. In
addition different cyanobacteria may vary in their
production of extracellular sunblocking pigments, which
reduce the photosynthetically effective intracellular radiation, so that intracellular irradiance is not known for
cyanobacteria. Consequently only relative ETR values are
presented, and data must be interpreted with care.
to as the ‘green’ community. A third community,
covering more than 80% of the whole rock surface,
is found at some distance (normally 4 50 cm) from
the furrows in the more or less horizontal rock
areas. This community, which is dominated by
Scytonema myochrous (Fig. 8), appears deep black
regardless of its water status and is referred to as
the ‘black’ community. While Scytonema myochrous also occurs along the lateral slopes, this
species is dominant only on the horizontal rock
areas where it forms dense, bushy mats.
Abiotic factors
The abiotic conditions to which the cyanobacteria
on the open rock outcrops of the inselberg are
exposed are among the most extreme found on
earth. Irradiance may reach 2600 mmol m72 s71
and the surface temperature of the cyanobacterial
mats on the bare rock varies between 22 and 528C
during the day (Fig. 9). The decrease in irradiance
and surface temperature in the afternoon was due
to rainfall, which frequently occurred in the middle
of the afternoon. Rapid variations in irradiance
were due to fast-moving dense clouds. The surface
temperature also did not follow a simple pattern,
but fluctuated in relation to rainfall.
Results
Cyanobacterial communities
Three dominant communities composed of different species of cyanobacteria can be found across
the furrows of the inselberg (Table 1, Fig. 3). The
first community grows in the centre of the furrows.
During and after rainfall the cyanobacterial mats
are covered by flowing water up to a few
centimetres in depth, occasionally with strong
current. This community, which is dominated by
compact growth forms, like the unicellular, colonybuilding Gloeocapsa sanguinea (Fig. 5) and the
short branching species Stigonema mammilosum
(Fig. 6), appears reddish in the wet state and will be
referred to as the ‘red’ community. The second
community covers the lateral slopes of the furrows.
This community is dominated by a thick layer of
Stigonema ocellatum (Fig. 7) which forms long
branching filaments. It appears dark green in the
wet, and black in the dry state and will be referred
Light dependency of photosynthetic capacity
Apparent effective quantum yield of PSII (DF/Fm’)
was measured over several days using the chlorophyll fluorescence technique (Fig. 10). The measurements were performed while all communities
were in a wet state, but not flooded, so that CO2
diffusion was not limited by liquid water covering
the cyanobacterial mats. Special care was taken to
obtain the measurements under similar, constant
conditions (e.g. variable cloud cover was avoided).
Maximum values of DF/Fm’ at low irradiances
did not exceed 0.60. With increasing irradiance,
DF/Fm’ did not decrease strongly, but declined
Table 1. Cyanobacterial species occurring in three zones across furrows at Les Nouragues inselberg
Gloeocapsa Scytonema Scytonema
sanguinea myochrous ocellatum
Central zone of furrows
(‘red’ community)
Intermediate zone on
slopes of furrows
(‘green’ community)
Horizontal rock areas
(‘black’ community)
Stigonema
ocellatum
Stigonema
mammilosum
Stigonema
hormoides
Schizothrix
sp.
Chroococcidiopsis
sp. (endolithic)
+++
+
+
+
++
+
7
++
+
++
+
+++
7
7
+
7
+
+++
+
++
7
+
7
+
Symbols: + + + , dominant species (over 50% of cyanobacteria); + + , abundant species (20 – 50% of cyanobacteria); + , occasional species
( 5 20% of cyanobacteria); 7, not found.
Photosynthesis of cyanobacteria
Fig. 9. Irradiances and surface temperatures measured daily
on the inselberg from 15 to 27 February 1999, at the same
times and sites where photosynthesis was measured. The
decrease in irradiance and temperature in the afternoon was
caused by rain, which regularly occurred at this time of the
day and year.
linearly with a gentle slope (Fig. 10A). This resulted
in comparatively high values for apparent effective
quantum yield at high irradiances and, therefore,
high values for apparent ETR (Fig. 10B). Maximum relative ETR values of 404 and 240 were
measured for the ‘black’ and ‘red’ communities,
respectively. The ‘red’ community in the centre of
the furrows always showed significantly lower
DF/Fm’ values than the two other communities of
cyanobacteria, which exhibited a similar light
dependency of PSII (Fig. 10). DF/Fm’ values varied
between 0.15 and 0.40 for the ‘red’ and between
0.20 and 0.55 for the other communities over a
wide range of irradiances.
Photosynthetic capacity during the morning
The activation of photosynthesis during the early
morning hours was characterized by measuring a
typical morning time course (Fig. 11). Heavy rain
had occurred in the evening of the previous day, so
that the cyanobacteria were still wet in the
morning. Optimal apparent quantum yield (Fv/
Fm) was surprisingly low before sunrise, about 0.2
for the ‘red’ community and 0.4 for the other two
communities (‘green’ and ‘black’; Fig. 11B). During
dawn apparent quantum yield (DF/Fm’) increased
251
Fig. 10. (A) Apparent effective quantum yield (DF/Fm’) and
(B) apparent rates of relative electron transport (ETR)
recorded over several days, while the cyanobacterial
communities were well wetted after natural rainfall. Symbols
indicate independent measurements and lines indicate linear
regressions (A) or fitted exponential growth to maximum
(B). Filled circles and continuous lines, cyanobacterial
community in the centre of the furrows (‘red’ community);
open squares and broken lines, cyanobacterial community at
the sides of the furrows (‘green’ community); open triangles
and dotted lines, cyanobacterial community on top of the
vertical rocks, beside the furrows (‘black’ community).
showing an activation of photosynthesis, which
differed between the communities. At 6:35 hours
(irradiance 5 1 mmol m 72 s71), the ‘red’ community displayed reduced photosynthetic efficiency,
while the other cyanobacterial mats were already
activated. When irradiance reached 10 – 20 mmol
m72 s 71 (around 7:00 hours), DF/Fm’ attained
maximum values of 0.49, 0.54 and 0.57 for the
‘red’, ‘green’ and ‘black’ communities, respectively.
With further increase in irradiance during the
morning, DF/Fm’ again decreased and showed the
same light-dependent characteristics described
above (Fig. 10).
Interestingly, PSII could also be activated by
artificial light flashes. At 6:10 hours (before dawn;
Fig. 11C) and 6:35 hours (during dawn; Fig. 11D),
short light pulses (*3000 mmol m72 s 71, duration
0.8 s) were applied once every 30 s. While photosynthesis was still in an inactivated state, DF/Fm’
increased significantly within minutes due to light
pulses (Fig. 11C and ‘red’ community only in Fig.
U. Rascher et al.
252
Fig. 12. Activation of light reactions by water, measured at
one site for each community. Symbols and lines as in Fig. 10.
DF/Fm’ was measured every minute; rain water was applied
at time 0 and subsequently every minute between the
measurements. Care was taken not to apply excess water
that might inhibit CO2 diffusion. Irradiances were 549 + 99,
479 + 93 and 488 + 158 mmol m72 s71 during the
measurements of the ‘red’, ‘green’ and ‘black’ communities,
respectively.
Fig. 11. Morning time course of activation of light reactions
during sunrise. Symbols and lines as in Fig. 10. (A), (B)
Morning time course over 4 h for irradiance and apparent
quantum yield. For each community 10 different spots were
measured. During this period surface temperature increased
from 248C to 318C. Before sunrise ( 5 1 mmol m72 s71) Fv/
Fm is plotted; these points are marked with an asterisk. After
6:45 h, irradiance reached *3 mmol m72 s71, and
measurements are noted as DF/Fm’. (C), (D) Additional
activation of photosynthesis of one spot by applying
saturating light pulses of the Mini-PAM every 30 s
simultaneously with the measurements at 6:10 and 6:35 h,
respectively. Curves were fitted using a peak equation.
11D). Activation of a similar magnitude was
observed while ambient irradiance increased during
sunrise (Fig. 11B). The ‘green’ and ‘black’ communities showed high values of DF/Fm’, which did not
increase after additional light pulses at 6:35 h
(Fig. 11D).
Water dependency of photosynthetic capacity
Thus far, water supply was considered optimal for
the cyanobacteria (Figs. 10, 11). In the following
experiments, the influence of water status on DF/
Fm’ was investigated under constant ambient light.
Rain water was added to totally desiccated
cyanobacteria (without detectable chlorophyll a
fluorescence) at time 0 and then again every 60 s.
DF/Fm’ was measured before water was added and
between each successive addition of water (Fig. 12).
All the communities showed a rapid activation of
PSII. Before watering, initial values of F and Fm’
were identical. Furthermore, after the initial wetting, both parameters increased threefold yet
remained equal (DF/Fm’ = 0). In the following
minutes DF/Fm’ increased gradually until maximum values were achieved after 20 – 30 min. The
‘green’ and ‘black’ communities revealed the same
kinetics, while the ‘red’ community reached saturation at a lower DF/Fm’.
To show the long-term reaction to water supply,
10 different spots for each community were
measured every 10 min. Water was applied at time
zero and in between the measurements (Fig. 13A).
The ‘red’ community saturated at the lowest levels,
while there was no significant difference between
the ‘green’ and ‘black’ communities under wellwatered conditions (45 – 65 min in Fig. 13B and 0 –
60 min in Fig. 13C). The last water was supplied to
the cyanobacteria at 47 min, and decreases in DF/
Fm’ were observed during desiccation (Fig. 13B).
Even though water status was not measured
directly, it can be deduced from chlorophyll
fluorescence data. Despite the fact that the same
amount of water was provided to all three
communities, photosynthesis of the ‘red’ and
‘black’ communities became inactive almost half
an hour earlier than that of the ‘green’ community.
A sudden (within minutes) decline in DF/Fm’ to
zero (in combination with a similar decline in
Photosynthesis of cyanobacteria
253
Fig. 13. Activation and desiccation processes of the three communities after watering. (A) Totally dry cyanobacteria were wetted
manually using rain water at time 0 and subsequently every 10 min. DF/Fm’ was measured every 10 min in between two
successive watering events. (B) At 47 min (dotted vertical line), the last water was applied to the then totally activated
cyanobacteria, and DF/Fm’ was measured every 5 – 10 min. (C) Desiccation was monitored for several hours after heavy rainfall
(8 mm), which ended at time 0. After this rain, the furrows were filled with flowing water. Ten different spots were measured in
each community. Symbols and lines as in Fig. 10. Significance of differences between pairs of communities indicated by symbols
in the upper-left corner of (A) are shown by asterisks (*p 5 0.05; **p 5 0.01; ***p 5 0.001). Irradiance was 1776 + 328 mmol
m72 s71 for (A) and (B), and 337 + 199 mmol m72 s71 for (C).
absolute fluorescence values) was observed after
about 20 min of desiccation, and is thought to
indicate inactivation of photosynthesis. This inactivation process was patchy, leaving photosynthetically active spots next to inactive spots,
which is reflected in the high standard deviations
during the drying process (Fig. 13B; 65 – 90 min).
This experimental treatment represented moderate
rainfall, which did not provide enough water to fill
the furrows.
The desiccation process after heavy rainfall
followed a different pattern (Fig. 13C). In this
case, running water was present in the furrows for
up to 1 h after rainfall stopped. The ‘red’ community was continuously flooded and the ‘green’
community could transport liquid water by capillary forces to extend its active period. The
boundary of the ‘black’ community is defined by
the distance water can be transported. As a
consequence, the water supply of the ‘black’
community was limited by its own storage capacity
and photosynthesis was inactivated earlier (Fig.
13C).
Discussion
We present here one of the first detailed studies of
the photosynthetic capacity of different cyanobacterial communities in situ on the bare granite rock
of an inselberg. We focus on the effects of the most
important abiotic factors, namely light and water.
In general, cyanobacteria exhibit low apparent
effective quantum yield of PSII (DF/Fm’) under low
light conditions, as revealed in detail under
laboratory conditions by Campbell et al. (1998).
Under both natural and laboratory conditions,
maximum apparent effective quantum yield was
achieved at low irradiances and DF/Fm’ never
exceeded 0.60. This agrees with data presented by
Lüttge et al. (1995). In addition, there was little
apparent down-regulation of light reactions (i.e.
only a small decrease in DF/Fm’) with increasing
irradiance. Moreover, apparent effective quantum
yield never decreased to low levels, so that electron
transport rates (ETR) at high irradiances were
remarkably high. Consequently, non-photochemical quenching mechanisms, which would further
decrease DF/Fm’, were minimal. This supports the
suggestion of Stransky & Hager (1970) that
cyanobacteria lack the xanthophyll cycle, which
constitutes the main component of dynamic
adaptation to excessive light in higher plants (see
Demmig-Adams & Adams, 1996). However,
chronic photoinhibition was not observed during
predawn measurements, although the cyanobacteria were exposed to extreme irradiance (Fig. 11). In
contrast, cyanobacteria grown under artificial
laboratory conditions sustained damage to the
photosynthetic apparatus and did not recover for
several days after sudden transfer to high light
(Demmig-Adams et al., 1990b). Survival in the
extremely high-light habitat of the inselbergs,
therefore, requires other mechanisms to protect
U. Rascher et al.
against surplus irradiance. Effective sunblocking
pigments, which are produced by all cyanobacteria
in light-exposed environments, can provide the
main basis for reducing intracellular light (Büdel,
1999; Büdel et al., 1997b) and help reduce ETR.
Mechanisms of protection against damage by high
irradiance can be observed in the formation of
effective extracellular sun-blocking pigments, such
as the indol-alkaloid scytonemin (Garcia-Pichel &
Castenholz, 1991). In exposed epilithic cyanobacteria of Venezuela and French Guiana, scytonemin,
with its absorption maximum at 380 nm, is found
in such high concentrations that PAR up to
500 nm is reduced. Moreover, intracellular carotenoids such as zeaxanthin (Demmig-Adams et al.,
1990a) and canthaxanthin (Albrecht et al., 2001;
Lakatos et al., 2001) may prevent photodamage, as
indicated by two other studies: (i) photoinhibition
took place in cyanobacterial mutants that were
unable to form canthaxanthin (Albrecht et al.,
2001); (ii) increased canthaxanthin content was
closely correlated with irradiance in cyanobacterial
mats of different habitats in Venezuela (Lakatos et
al., 2001). However, formation of these pigments is
rather slow and takes place over days (EhlingSchulz et al., 1997; Lakatos et al., 2001). Thus, the
effective irradiance inside the cells of free-living
cyanobacteria is much lower than at their surface,
which allows colonization of the bare rocks of
inselbergs with their highly fluctuating light environment.
Another feature was observed during the morning
hours, which are ecologically important for carbon
gain of the cyanobacteria. Water supply can be
considered good in the early morning, because of
frequent night-time rainfall and high relative humidity during the night. Irradiance and temperature are
moderate and, therefore, optimal conditions for
photosynthesis occur during this time of the day. We
have demonstrated that the photosynthetic apparatus of cyanobacteria can be activated after a period of
darkness either by weak light, which occurs naturally
during dawn, or artificially by intermittent light
pulses. Under natural conditions, this activation is
completed gradually (Fig. 11B). When stimulated by
light pulses, however, activation occurs within a few
minutes (Fig. 11C, D), resulting in a strong increase
in Fv/Fm (0.20 – 0.48; Fig. 11B). In purple nonsulphur bacteria and cyanobacteria, respiratory and
photosynthetic electron flow share the same electron
transport intermediates (Scherer, 1990). Respiratory
electron flow in the dark generally shifts the electron
transport chain towards a reduced state (for a review
of this so-called state transition, see Campbell et al.,
1998). In the dark or under very low light, therefore,
cyanobacteria are in the so-called state II, which
results in low variable fluorescence. As light is
applied to the dark-adapted cyanobacteria, PSI
254
activity partially oxidizes the electron transport
chain and the cells shift towards state I, with higher
PSII efficiency (Campbell et al., 1998). This phenomenon is well known from laboratory studies and was
recently shown for marine algal assemblages (Behrenfeld & Kolber, 1999). Here we show for the first
time that this state transition also occurs in terrestrial
cyanobacteria and is ecologically important. This
transition between state II and state I, with its
concomitant activation of photosynthesis, takes
place every morning under natural wet conditions.
Predawn measurements of chlorophyll fluorescence have to be interpreted with care. Measurements of dark-adapted organisms do not reveal
maximum fluorescence and, therefore, the optimal
quantum yield (Fv/Fm) and non-photochemical
quenching (qN and NPQ) cannot be calculated in
the standard way. Phycobilisomes also influence F0
values, and respiration operates even in high
irradiances, keeping a relatively large proportion
of QA oxidized. These mechanisms also influence
fluorescence values. Thus, maximum fluorescence
values, either for Fm or for Fm’, cannot be obtained
without application of DCMU to block electron
transport.
The spatial distribution of cyanobacterial mats
on the bare rocks of the inselberg is governed by
different ecophysiological capacities and microhabitat niches. ‘Black’ communities dominated by
Scytonema can be regarded as generalists, covering
more than 80% of the open rock formations. High
photosynthetic quantum efficiency over a wide
range of irradiances (Fig. 10) and the ability to
reduce atmospheric N2 enable these cyanobacteria
to become the dominant species in this habitat. The
fast activation kinetics during dawn and after
watering facilitate their widespread colonization
of the rocks. Cyanobacteria are resistant to
desiccation and can survive in the dry state for
long periods. This resistance to dehydration may be
due to three factors – water storage, water holding
capacity and water distribution – and is a prerequisite for occupying the bare granite outcrops of
inselbergs. Nevertheless, growth of the cyanobacteria is limited by the availability of liquid water,
but photosynthetic electron transport of the ‘black’
community is reduced fastest after natural rain
events (Fig. 13C).
The other communities (‘red’ and ‘green’) cover
microhabitats along the furrows and make use of
the different water regimes. Although the ‘green’
and ‘black’ communities differ only in the relative
abundance of different species, their photosynthesis
clearly shows different kinetics during desiccation
(Fig. 13). The separation between the ‘green’ and
‘black’ community is determined by the distance
water can be transported from water-filled furrows
by capillary forces of the Stigonema species. With
Photosynthesis of cyanobacteria
their long branched filaments, they become dominant in the ‘green’ community (Table 1). The
filaments have a large surface area, and transport
water by capillary forces, as well as having a high
water storage capacity within the thick mats (Fig.
13B). While photosynthetic capacity of the ‘green’
community is similar to that of the ‘black’
community, water transport and water storage
capacity differ (Fig. 13B). The extended time period
of optimal water status favours higher productivity
of Stigonema species.
Gloeocapsa sanguinea, which dominates the ‘red’
community, can be found in low abundance all
over the inselberg. In the centre of the furrows,
however, Gloeocapsa sanguinea is the dominant
species. Although the ‘red’ community has lowest
values of apparent effective quantum yield, it is not
overgrown in the furrow-centre. The limit of
growth in the ‘green’ community is sharply defined
by the level of potential water flow. Rapidly
flowing water mechanically strains the long filaments of Stigonema ocellatum and favours the
survival of compact growth forms, such as Gleocapsa sanguinea, which dominate the furrow centre.
Their comparatively low photosynthetic capacities,
however, may be offset by long periods of water
flow after rain.
The photosynthetic responses of free-living
cyanobacteria to extreme and fluctuating irradiance and water availability have been described in
this study. In addition, species-specific strategies,
leading to a distinct zoning of terrestrial cyanobacterial communities, have been revealed which
explain their coexistence on a small scale across the
furrows.
Acknowledgements
U. Rascher thanks the DFG for supporting the
opportunity of making the measurements in
French Guiana in the framework of the ‘Graduierten-Kolleg 340 – Communication in biological systems’. M. Lakatos and U. Rascher thank the
DAAD and the EU (European tropical forest large
scale facility program) for covering the travel
expenses. We thank Prof. Dr Pierre CharlesDominique (University Paris Sud, CNRS) for
making possible the stay at the well-equipped Les
Nouragues field station (UPS 656, CNRS) in
French Guiana.
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