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First published online August 17, 2006
Journal of Experimental Biology 209, 3413-3419 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02382
Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for `light-enhanced calcification'
Centre Scientifique de Monaco, Avenue Saint-Martin, MC-98000 Principality of Monaco
* Author for correspondence (e-mail: stambutte{at}centrescientifique.mc)
Accepted 13 June 2006
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Key words: light-enhanced calcification, calcification, photosynthesis, kinetic approach, light/dark, radioisotope, Stylophora pistillata
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Introduction |
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). The presence of these symbionts in corals has a
crucial effect on the metabolism of the host (for reviews, see
Muscatine, 1990;
Furla et al., 2005).
As early as 1948, it has been shown that scleractinian corals calcify
faster in the light than in the dark
(Kawaguti and Sakumoto, 1948);
a phenomenon largely confirmed by Goreau
(Goreau, 1959) and
subsequently called light-enhanced calcification (LEC). However, after more
than a half century of research, the mechanism underlying this process remains
largely unknown, although a number of hypotheses have been proposed
(Barnes and Chalker, 1990;
Cohen and McConnaughey, 2003;
Allemand et al., 2004).
), and thus
favours calcium carbonate precipitation. According to McConnaughey and Whelan,
the production of H+ by calcification favours CO2
formation to the detriment of the other dissolved inorganic carbon forms
(McConnaughey and Whelan,
1997). Dinoflagellates absorb this CO2 and thus favour
calcium carbonate precipitation. According to Furla et al., the OH-
resulting from the carbon-concentrating mechanism (CCM) present in oral layers
of cells may neutralize the H+ produced by calcification
(Furla et al., 1998), thus
allowing calcification to proceed. ). ) or
release of O2 (Rinkevich and
Loya, 1984). ). It has been shown that the composition of the organic
matrix is different between symbiotic and non-symbiotic corals
(Cuif et al., 1999).
Zooxanthellae translocate photosynthates to the host
(Muscatine and Cernichiari,
1969). However, if zooxanthellae participate in the synthesis of
the organic matrix, they only supply organic precursors, as organic matrix
synthesis is only performed by calicoblastic cells
(Puverel et al., 2005).
Although the involvement of light in coral calcification has probably been
studied more extensively than any other environmental variable, effects of
light remain one of the most poorly understood, for several reasons
(Buddemeier and Kinzie, 1976).
One of them is the possible existence of an endogenous circadian rhythm, which
would modify any potentially monotonic relationship between light and growth
(Vandermeulen and Muscatine,
1974; Chalker,
1977; Roth et al.,
1982). A circadian rhythm is a biological rhythm in which the
period is about 24 h. It is qualified as `endogenous' if it is internal to the
organism rather than due to a variation of an environmental factor
(Hirota and Fukada, 2004).
The aim of this study was to provide new information on the light-enhanced
calcification phenomenon, using the zooxanthellate scleractinian coral
Stylophora pistillata as a model, by investigating, under controlled
conditions, the time course of calcification at different hours of the day,
and after light to dark and dark to light transitions. We used 45Ca
as a tracer, which can provide an extremely sensitive and precise measure of
short-term calcification rates (Buddemeier
and Kinzie, 1976) and has been validated for physiological studies
in S. pistillata (Tambutté
et al., 1995). In a first step, we studied variations of
calcification during the day and the night and during free-running
experiments, in order to determine if calcification rates are under the
influence of an endogenous circadian rhythm. Photosynthetic rates were also
measured during the day. In a second step, we compared for the first time the
rates of calcification during transitions between light and dark and vice
versa.
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Materials and methods |
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), were stored in a 300-l aquarium, supplied with seawater
from the Mediterranean Sea (exchange rate 2% h-1) under controlled
conditions: semi-open circuit, temperature 26.0±0.2°C, salinity
38.2
, light 175 µmol photons m-2 s-1 (using
fluorescent tubes; Custom Sea Life®, California, USA) on a 12 h:12 h
light:dark photoperiod, with the light period beginning at 9:00 h. Corals were
fed three times weekly in the evening with a mix of Artemia salina
nauplii, frozen adults of Artemia salina and frozen krill.
Experimental protocol
Measurement of calcification rates
In order to determine the light intensity necessary to obtain saturating
rates, calcification rates were measured under different light intensities.
Varied light intensity was obtained with a screen placed between the light
source and the samples. Microcolonies were adapted to the light intensity for
30 min before each experiment. Calcification rates were measured using the
protocol described previously
(Tambutté et al., 1995;
Tambutté et al., 1996).
Briefly, the microcolonies were placed in plastic holders and incubated for 1
h in 10-ml beakers containing 240 kBq of 45Ca (as
45CaCl2; New England Nuclear®, Boston, MA, USA)
dissolved in seawater, filtered using 0.45 µm Millipore membranes (filtered
seawater; FSW). Samples (100 µl) of seawater were removed during each
incubation for determination of specific radioactivity. Incubations were
performed in the same conditions of temperature (26.0±0.2°C) and
light (175 µmol photons m-2 s-1) as
in the maintenance experimental aquaria. A magnetic stirring bar maintained
water movement during the experiment. At the end of the incubation, tissues
were completely dissolved in 1 mol l-1 NaOH at 90°C for 10 min.
The supernatant was collected in a separate tube. The skeleton was rinsed
first in 1 ml NaOH, then twice in FSW, and finally twice in H2O
milliQ. The first rinse solution was added to the tissue fraction, the
remaining four were discarded since they did not contain proteins. Finally the
skeleton was dried and dissolved in 6 mol l-1 HCl. Samples of this
skeletal fraction were counted with 4 ml of Ultima Gold AB (Packard, Boston,
MA, USA). Emissions were measured using a liquid scintillation counter (2100
TR Packard, Tricarb). Protein content of each tissue fraction was measured
using the BCA Protein Assay Kit (Uptima, Montluçon, France), based on
the colorimetric determination of the amount of proteins
(Lowry et al., 1951). The
standard curve was established with bovine serum albumin. Results are
expressed as nmol Ca h-1 mg-1 of protein.
To study the calcification rate during day and night, measurements of 45Ca incorporation were performed at different hours of the day (9:30, 11:30, 13:30, 15:30, 17:30, 19:30 h) and the night (23:30, 3:30, 7:30 h) under saturating light, according to the protocol described above. Six microcolonies were used for each point of the daily cycle.
Measurement of photosynthetic rates
Photosynthetic rates were measured at different hours of the day (9:30,
11:30, 13:30, 15:30, 17:30, 19:30 h). Before each experiment, the oxygen
sensor was calibrated against airsaturated seawater (100% oxygen) and a
saturated solution of sodium dithionite (zero oxygen). Each microcolony was
placed in a respirometric glass chamber containing a Strathkelvin 928
electrode (Glasgow, UK) for 15 min under saturating light (175 µmol
m-2 s-1). The temperature was maintained constant at
26.0±0.2°C using a water bath. The incubation medium was
homogenized with a magnetic stirring bar. Oxygen was monitored every 10 s on
an acquisition station (Strathkelvin 928 oxygen system, version 2.0). Surface
area of each microcolony was measured according to the wax technique
(Stimson and Kinzie, 1991).
Results are expressed as µmol O2 cm-2
h-1.
Night and day free-running experiments
Free-running experiments were carried out to identify any possible
endogenous circadian rhythm. Calcification rates were measured after 16 and 20
h of constant dark and light conditions, according to the protocol described
above.
Transition between light and dark calcification rates
To study transitions between light and dark or dark and light, a cumulative
kinetic isotopic approach was chosen. Twenty microcolonies were placed in
plastic holders and incubated, as described above, in 10-ml beakers containing
240 kBq of 45Ca dissolved in FSW. Every 10 min, one microcolony was
sampled and the incorporated 45Ca was counted according to the
protocol described above. Three experiments per each transition were
performed. Results are expressed as nmol Ca mg-1 protein.
Statistical analysis
Paired Student's t-tests and one-way ANOVA were used for
statistical analysis (software Jump 5.1, SAS Institute, Cary, USA). Results
were considered statistically significant at P<0.05. Results are
reported as mean ± standard error of the mean (s.e.m.).
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).
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Daily cycle of photosynthesis
Photosynthetic rates were measured at different hours of the day. The daily
evolution of photosynthetic rates is shown in
Fig. 3. There is no significant
variation of photosynthetic rates during the day under constant conditions of
light (one-way ANOVA, P=0.94), with a stable value of
0.51±0.02 µmol O2 cm-2 h-1. The
same result was obtained when data were standardized per mg of protein
(0.60±0.02 µmol O2 mg-1 protein
h-1) or per g dry mass of skeleton (8.26±0.27 µmol
O2 g-1 dry mass skeleton h-1).
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Night and day free-running experiments
This set of experiments was performed to investigate the possible existence
of an endogenous circadian rhythm. For this purpose, free-running experiments
in the dark or in the light were carried out during periods of 12, 16 and 20 h
(Fig. 4A,B).
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Results for light experiments are shown in Fig. 4B. After 12 h of light, the calcification rate was not significantly different from the mean value obtained during the daily cycle (t-test, P=0.65). After 16 and 20 h of light, calcification rates were not significantly different from the value obtained after 12 h (t-test, P=0.60 and P=0.67, respectively).
Transition from dark to light (and vice versa)
In order to determine the time-course of transition of the calcification
rates from dark to light and vice versa, 45Ca uptake was
measured using a cumulative kinetic isotopic approach before and after
switching the light on or off (Fig.
5A,B). In such a graphic representation, a steady slope of the
regression line means that the calcification rate is constant over the time,
whereas a slope break means that the calcification rate changes over the
time.
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Transition from dark to light
When corals are shifted from dark to light
(Fig. 5A), the calcification
rate is constant before switching on the light and at the end of the kinetics
(points are well lined up), whereas it varies during the first hour when the
light is switched on (points are scattered), thus proving the existence of a
lag-phase.
To mathematically characterize this lag-phase, we chose a regression analysis that depends upon the intersection of two regression lines, one for the dark condition and one for the light condition. We chose the first five points and the last five points of the kinetics because points were lined up (so calcification rates were stable, as demonstrated above). The regression line of the first five points in the dark condition is: y=1.03x+111.49, r2=0.88 and the regression line of the last five points in the light condition is: y=2.50x+76.32, r2=0.91. Intersection between the two regression lines corresponds to 25 min after switching on the light, indicating that 25 min are necessary to reach the constant light calcification rate after a dark period. This is confirmed by the ratio between the slope of the first regression line and the slope of the last regression line, which is about 2.4. This means that the light calcification rate is about 2.4 times higher than the dark calcification rate, which is close to the value obtained for the daily cycle.
Transition from light to dark
A similar experiment and mathematical treatment were performed for the
opposite transition (Fig. 5B).
The regression line of the first five points in the light condition is:
y=2.90x+189.24, r2=0.89 and the
regression line of the last five points in dark condition is:
y=1.28x+235.86, r2=0.83. Intersection of
the two regression lines corresponds to 25-30 min after switching off the
light. This experiment shows that 25-30 min are necessary to reach the
constant dark calcification rate after a light period. This is confirmed by
the ratio between the slope of the first regression line and the slope of the
last regression line, which is about 2.3. This means that the light
calcification rate is about 2.3 times higher than the dark calcification rate,
which is close to the value obtained for the daily cycle.
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; Allemand et al.,
2004), this phenomenon still remains enigmatic. One of the reasons
is that the existence of an endogenous circadian rhythm could modify the
relationship between light and growth
(Vandermeulen and Muscatine,
1974; Chalker,
1977; Roth et al.,
1982). Thus in most coral calcification studies, measurements of
calcification rates are made at a given time of the day in order to avoid
possible variations caused by endogenous circadian rhythms
(Buddemeier and Kinzie, 1976;
Tambutté et al., 1995;
Tambutté et al., 1996;
Houlbrèque et al.,
2004). However until now, there has never been direct evidence of
such rhythms in corals. Most studies have been performed under natural
daylight conditions. In these conditions, different results have been
obtained: the rates either vary
(Vandermeulen et al., 1972;
Clausen and Roth, 1975;
Barnes and Crossland, 1978) or
remain constant during the day (Chalker,
1977; Hidaka,
1991). However, in such experiments, the variations of light
intensity due to natural daylight conditions can hide endogenous circadian
rhythms. Moreover, to be qualified as endogenous, the rhythm must persist
under constant conditions and during free-running experiments. In the present study, we measured calcification rates during a daily cycle of a 12 h:12 h light:dark periods under constant conditions of light, and we performed free-running experiments under prolonged conditions of dark and light.
Rate of calcification and photosynthesis at constant light intensity throughout a daily cycle
Under a constant light intensity of 175 µmol photons m-2
s-1, corresponding to the intensity of the saturating calcification
rate, our results show that there is no variation of calcification rate in
Stylophora pistillata during the day and during the night
(Fig. 2). An experiment
performed on Pocillopora damicornis
(Clausen and Roth, 1975) showed
a tendency towards a decrease in calcification rates between 9:00 and 15:00,
but the authors specified that the difference between light and dark
calcification rates was no significant. Chalker performed an experiment on the
coral Acropora cervicornis
(Chalker, 1977) and concluded
that there was a circadian rhythm, but a statistical analysis of the data
would have been necessary to confirm this study.
As for calcification rates, in our experiments, the photosynthetic rate
remained constant throughout the day when a constant light intensity was
applied (Fig. 3). In addition
to studies on calcification, many studies have been performed on the daily
rhythm of photosynthesis in zooxanthellae. However, most of the experiments
were done under natural daylight (Chalker
and Taylor, 1978; Porter,
1980; Hoegh-Guldberg and
Jones, 1999; Jones and
Hoegh-Guldberg, 2001; Levy et
al., 2004) and thus no endogenous rhythm could be detected. Few
experiments have been performed under constant light intensity
(Chalker, 1977;
Muller-Parker, 1984). In these
conditions, a daily rhythm was detected in the freshly isolated dinoflagellate
Gymnodinium microadriaticum
(Chalker, 1977) and in the sea
anemone Aiptasia pulchella
(Muller-Parker, 1984).
However, as for calcification, Chalker's data
(Chalker, 1977) were not
analysed statistically. Moreover, it was suggested that the circadian rhythm
in photosynthesis could be species specific
(Muller-Parker, 1984). The
rates of photosynthesis of S. pistillata measured over a 24 h period
and under constant light remain constant
(Ferrier-Pagès et al.,
1998). These results and ours show that in controlled constant
conditions of culture and experimentation, there is no variation during a
daily cycle of both calcification and photosynthesis in S.
pistillata.
In natural conditions of light, i.e. with light intensity fluctuating
during the daily cycle, it has often been noticed that the photosynthetic
rates were different between the afternoon and the morning, for the same light
intensity (Vollenweider, 1965;
Schanz and Dubinsky, 1988;
Levy et al., 2004). This
phenomenon, called the `hysteresis effect', was not observed in our
experiments, suggested that it is not linked to the photosynthetic apparatus
but probably determined by an environmental parameter such as light variation
throughout the day.
Rate of calcification at constant light intensity under free-running conditions
Whereas the rate of calcification remains stable under constant light
intensity, our results confirm that there is a sharp difference between the
day and the night calcification rates with a ratio of about 2.6. Consequently,
we checked whether this difference persisted when the corals were submitted to
longer periods of light or dark, i.e. if this difference was due to an
endogenous circadian rhythm or just relied on light regime. We thus performed
free-running experiments, under prolonged periods of dark or light conditions.
After 16 and 20 h in the dark or in the light, the calcification rates were
the same as during the 12 h period of night or light. These results confirm
that the LEC phenomenon is only due to a light-tempered parameter and not to
an endogenous circadian rhythm.
In most coral calcification studies, measurements of calcification rates
are made at a given time of the day in order to avoid possible variations
caused by endogenous circadian rhythms
(Buddemeier and Kinzie, 1976;
Tambutté et al., 1995;
Tambutté et al., 1996;
Houlbrèque et al.,
2004). In this study we determined that, when S.
pistillata is maintained under constant conditions of light intensity,
calcification rates are constant throughout the day and the night. Thus in
this study we could perform experiments on the effect of light on
calcification without being hampered by endogenous circadian rhythms.
Time-course of transitions between light/dark or dark/light calcification rates
The analysis of 28 publications on LEC shows that light/dark ratios of
calcification range from negative values to 127 with a median ratio of 3
(Gattuso et al., 1999). This
wide range of variations is attributed to the wide range of environmental and
biological conditions during the experiments. For S. pistillata,
under constant conditions of culture and experimentation (175 µmol photons
m-2 s-1, 12 h:12 h light:dark photoperiod, temperature
26°C and salinity 38.2) the calcification rate that we measured in
the light is about 2.6 times higher than the calcification rate in the dark.
This value is in the range of the mean ratio values for LEC (cf. above) and
similar to that shown before in S. pistillata
(Furla et al., 2000). In the
present study we made a fine analysis of the time necessary to switch from the
light calcification rate to the dark calcification rate and vice
versa, under constant conditions of light intensity.
Under constant conditions of culture and experiment, we have underlined the existence of a lag-phase, which is similar for both transitions. The time necessary to switch from one calcification rate to the other is about 25-30 min. Once stabilized, the rate of calcification remains stable for at least 12 h, under constant conditions.
For the transition between light and dark, the dark calcification rate of
Acropora formosa is significantly increased during the first 20 min
of dark by prior incubation in the light
(Roth et al., 1982). We
observed a lag-phase of similar duration. Roth et al. supposed that this
lag-phase corresponds to the use of cellular reserves accumulated during light
(Roth et al., 1982). However,
for the opposite transition between dark and light, this hypothesis cannot be
applied to explain the lag-phase observed.
The transition from dark to light conditions has been slightly more studied
than the opposite transition. A lag-phase of 35-40 min has been observed
before inorganic carbon deposition was stimulated in the skeleton of
Acropora acuminata (Barnes and
Crossland, 1978). These authors suggested that this lag-phase was
an artefact arising from the dilution of 14C by an unlabelled pool
of dissolved inorganic carbon in the tissues. However, we find in the present
study the same results with 45Ca, for which it has been
demonstrated that transport from sea water to the skeleton is rapid, with no
lag-phase, and does not involve an intracellular pool
(Tambutté et al.,
1996). We can thus conclude that the lag-phase that we observed
during this transition cannot be due to an artefact arising from the dilution
of calcium.
The presence of a lag-phase was also observed during the transition from
dark to light in S. pistillata using H14CO
2-3 as a marker
(Furla et al., 2000). These
authors suggest that this lag-phase, which was about 10 min, corresponds to
the time necessary, during the day, to produce OH- by
photosynthesis in order to titrate the H+ produced by calcification
(Furla et al., 2000) and thus
to allow calcification to proceed. A study on the polarity of the tentacle of
the sea anemone Anemonia viridis demonstrated that light induces a pH
increase of the coelenteron, whereas darkness induced an acidification
(Furla et al., 1998). This pH
gradient across the tentacle becomes maximal after 20-30 min of saturating
light (Furla et al., 1998),
which is consistent with the lag-phase of transition that we obtained in this
study. Such an hypothesis can also explain the lag-phase obtained during the
transition from light to dark, since it could correspond to the time necessary
to deplete the OH- accumulated during the day (by diffusion of the
OH- out of the tentacle).
Based on the results of Allemand et al., a second hypothesis can also be
proposed (Allemand et al.,
1998). These authors found that the time required to absorb,
transport, incorporate the amino acid precursor (aspartic acid) into organic
matrix, and finally to export and incorporate it into the skeleton takes about
20 min. We can thus suggest that this time, which is similar to the length of
the lag-phase found in the present study, corresponds to the time required for
photosynthates to be transported to the calicoblastic epithelium where organic
matrix synthesis take place (Puverel et
al., 2005) and then be exocytosed towards the skeleton. In this
case, organic matrix would not only differ quantitatively between light and
dark (Houlbrèque et al.,
2004) but also qualitatively. Specific organic matrix proteins
synthesized from photosynthates could thus play a role in the light-enhanced
calcification mechanisms as previously suggested
(Muscatine and Cernichiari,
1969). This hypothesis is supported by the fact that the amino
acid composition differs between zooxanthellate and nonzooxanthellate corals
(Cuif et al., 1999). This
hypothesis can also explain the lag-phase observed for the transition between
light and dark, since the time necessary to obtain a stable dark rate of
calcification could correspond to the synthesis of the last organic matrix
proteins using photosynthates as precursors after switching off the light, and
to their transport to the site of skeletogenesis.
To conclude, we have demonstrated that under controlled conditions of constant light, there is no endogenous circadian rhythm of calcification and photosynthesis and that light-enhanced calcification is dependent on the light regime only. Thus, in these conditions, we determined that a similar lag-phase exists between the transitions from light to dark or from dark to light calcification rates. At least two hypotheses from the literature can fit with our results: the role of photosynthesis on the pH in the coelenteron and the role of photosynthesis in supplying precursors of organic matrix. In a next step, our aim will be to study the biochemical composition of the organic matrix during the day and during the night. Another approach will also be to determine the differential expression of genes in light and in dark conditions.
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Acknowledgments |
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