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Photosynthetic carbon utilization by Enteromorpha
intestinalis (Chlorophyta) from a Swedish rockpool
a b a c d
Christer Larsson , Lennart Axelsson , Hans Ryberg & Sven Beer
a
Kristineberg Marine Research Station, S-450 34 Fiskebäckskil, Sweden
b
Department of Marine Botany, University of Göteborg, Carl Skottsbergs Gata 22, S-413 19
Göteborg, Sweden
c
Department of Plant Physiology, University of Göteborg, Carl Skottsbergs Gata 22, S-413 19
Göteborg, Sweden
d
Department of Botany, Tel Aviv University, Tel Aviv 69978, Israel
Published online: 03 Jun 2010.
To cite this article: Christer Larsson , Lennart Axelsson , Hans Ryberg & Sven Beer (1997) Photosynthetic carbon utilization
by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool, European Journal of Phycology, 32:1, 49-54, DOI:
10.1080/09541449710001719365
To link to this article: http://dx.doi.org/10.1080/09541449710001719365
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www.tandfonline.com/page/terms-and-conditionsEur. J. Phycol. (1997), 32 : 49–54. Printed in Great Britain 49
Photosynthetic carbon utilization by Enteromorpha intestinalis
(Chlorophyta) from a Swedish rockpool
C H R I S T E R L A R S S O N1, 2, L E N N A R T A X E L S S O N1, H A N S R Y B E R G3 A N D S V E N B E E R4
" Kristineberg Marine Research Station, S-450 34 FiskebaX ckskil, Sweden
# Department of Marine Botany, University of GoX teborg, Carl Skottsbergs Gata 22, S-413 19 GoX teborg, Sweden
$ Department of Plant Physiology, University of GoX teborg, Carl Skottsbergs Gata 22, S-413 19 GoX teborg, Sweden
% Department of Botany, Tel Aviv University, Tel Aviv 69978, Israel
(Received 9 May 1996 ; accepted 22 August 1996)
Enteromorpha intestinalis grows along the Swedish west coast in rockpools which are isolated from the open seawater for long time periods
and where, therefore, the inorganic carbon content is low and the pH is high during the day. In order to investigate how E. intestinalis
could grow under such apparently CO -constraining conditions, we measured its photosynthetic responses to inorganic carbon in the
#
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presence of an inhibitor of external}surface-bound carbonic anhydrase (acetazolamide) as well as an inhibitor of HCO− transport via anion
$
exchange (4,4«-diisothiocyanatostilbene-2,2«-disulfonate). The results show that both HCO− dehydration via surface-bound carbonic
$
anhydrase and HCO− transport via a 4,4«-diisothiocyanatostilbene-2,2«-disulfonate-sensitive mechanism were present in E. intestinalis, but
$
only HCO− uptake via the putative transporter was operative in rockpool water during most of the photic period (pH " 9±4, inorganic
$
carbon ! 0±45 mol m−$ and CO ! 0±05 mmol m−$). The advantage of such a mechanism, rather than extracellular HCO− dehydration, is
# $
discussed with regard to photosynthesis of marine macroalgae under in situ conditions conducive to high pH values adjacent to the thalli.
Key words : anion transport(er), AZ, carbonic anhydrase, Chlorophyta, DIDS, Enteromorpha, inorganic carbon, macroalga(e),
photosynthesis, rockpool
Introduction blood cells (AE1), such as being sensitive to the AE1-
inhibitor 4,4«-diisothiocyanatostilbene-2,2«-disulfonate
In light of the much (c. 200 times) higher HCO−
$ (DIDS : Drechsler et al., 1993, 1994).
(bicarbonate) than CO concentration in seawater, it is not
# It was recently shown that Ulva lactuca could be
surprising that many species of macroalgae can use the
induced to take up HCO− directly via the DIDS-sensitive
ionic carbon form as their principal bulk source of $
mechanism when grown in a flow-through system at high
inorganic carbon (Ci) for photosynthesis (e.g. Sand-Jensen
pH, while under normal growth conditions the CA-
& Gordon, 1984 ; Maberly, 1990 ; Axelsson et al., 1991,
mediated mechanism catalysed extracellular HCO− de-
summarized in Beer, 1994). Green macroalgae differ from $
hydration (Axelsson et al., 1995). Photosynthetic HCO−
red and brown algae in having an inducible mechanism $
utilization via the latter mechanism was inhibited by the
allowing photosynthesis at high pH, probably via use of
CA inhibitor acetazolamide (AZ) and was insensitive to
HCO− (Carlberg et al., 1990). This inducible mechanism
$ DIDS. HCO− uptake via the DIDS-sensitive mechanism,
may thus function as a supplement to their Ci utilization at $
on the other hand, appeared to be insensitive to AZ. It
normal pH (Axelsson et al., 1991). Two principal ways of
was also found that while the DIDS-sensitive mechanism
utilizing HCO− have been described for this plant group.
$ operated equally well at pH 8±4 and 9±4 (at normal
In one of these, HCO− is dehydrated extracellularly by
$ seawater Ci concentrations), the CA-mediated mechanism
surface-bound carbonic anhydrase (CA) to form CO
# was almost non-functional at the higher pH value.
which is then taken up into the cells. This type of HCO−
$ So far, representatives of the genus Ulva are the only
utilization has been shown to function in several Ulva
algae that have been found to feature HCO− uptake by the
species (Bjo$ rk et al., 1992, 1993). A second way in which $
DIDS-sensitive mechanism in the field (Drechsler & Beer,
Ulva spp. can use HCO− is by its direct uptake (as
$ 1991 ; Drechsler et al., 1993). The plants in these
suggested by Giordano & Maberly, 1989 ; Drechsler &
investigations were collected in an intertidal zone of the
Beer, 1991). It was subsequently found that HCO− uptake
$ eastern Mediterranean. Here summer temperatures,
in Ulva fasciata could be facilitated by a mechanism which
irradiances and nutrient levels are high, and the resultant
features properties similar to the anion exchanger of red
high photosynthetic rates cause high pH values and low
Correspondence to : L. Axelsson. Fax : 46-523-18503. e-mail : CO (but substantial ionic Ci) concentrations adjacent to
#
l.axelsson!kmf.gu.se the thalli (cf. Beer & Israel, 1990). On the other hand, U.C. Larsson et al. 50
lactuca growing naturally in Swedish waters is usually either in natural rockpool water or in synthetic seawater
exposed to lower temperature and light conditions which (SSW) of 30 ^ (PSU) composed of 450 mol m−$ NaCl,
would restrict high photosynthetic rates. These plants 30 mol m−$ MgSO , 10 mol m−$ KCl and 10 mol m−$
%
may thus not benefit from direct HCO− uptake since CaCl . The SSW medium was buffered to pH 8±4 or 9±5
$ #
external CA-mediated HCO− dehydration could under respectively with Tris or AMPSO (final concentrations
$
those circumstances supply enough CO to meet photo- 50 mol m−$) biological buffers (Sigma), and NaHCO
# $
synthetic needs (cf. Axelsson et al., 1995). In rockpools from a stock solution was injected into the closed
occupied by algae, the stagnant water is characterized by chambers to the desired final Ci concentrations. To
high temperatures and high pH values during the day check for the presence of the two HCO− utilization
$
(Ganning, 1971 ; Truchot & Duhamel-Jouve, 1980). In mechanisms, AZ and DIDS (Sigma) were injected into the
such situations, CO concentrations are below air- electrode chambers to final concentrations of 100 and
#
equilibrium levels, and HCO− and CO#− (carbonate) 300 mmol m−$, respectively, after steady-state photo-
$ $
comprise virtually the only Ci pool. Along the Swedish synthetic rates had been reached. For each mechanism, Ci
west coast, the principal alga growing in such rock- affinity curves were obtained by first inhibiting the other
pools is Enteromorpha intestinalis L., and it was the mechanism and then adding increasing amounts of HCO−
$
purpose of this work to explore which mechanism(s) to the Ci-free SSW. When calculating the Vmax and K"
#
are involved in the photosynthetic Ci acquisition of this values in the presence of DIDS, a negative intercept on the
green alga. y-axis (cf. Fig. 1) was compensated for by adding 7 µmol
O g−" h−" to all net photosynthesis rates.
#
The following conditions were measured in situ in the
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Materials and methods
rockpools : scalar photon flux density (400–700 nm, using
This work was carried out at Kristineberg Marine Research a QSL-100 meter, Biospherical Instruments), temperature,
Station on the Swedish west coast in August 1994. The O concentration (using a temperature-compensated
#
rockpools studied were located on Byxeska$ r, a small island model 57 Yellow Springs O electrode) and pH (using an
#
two nautical miles west of Kristineberg. Two rockpools of E 588 Metrohm Herisau pH meter calibrated according to
similar appearance and physical conditions, located c. 2 m the NBS-pH scale). Water samples were sterile-filtered
above the mean water level, were used : one for collection (0±45 µm) directly upon sampling, and brought to the
of algae and one to follow the changes in physical and laboratory for analysis. The Ci content was measured as
chemical conditions during the day. Since the tidal the amount of CO released in a stripping column
#
amplitudes in the area are small (c. 0±3 m), the water (containing 5 % phosphoric acid) connected to an infrared
exchange in these rockpools is due to rain and wave gas analyser (IRGA, ADC model MKIII). Nutrient analysis
action. The weather was sunny and calm during the period was carried out on an autoanalyser (Technicon Auto-
of this investigation and the water in the rockpools had analyser II).
not been exchanged for at least a week. E. intestinalis was
collected from one of the rockpools on 3 and 9 August
between 1100 and 1200 hours, and transported to the Results
laboratory for investigation of photosynthetic charac- Enteromorpha intestinalis from the rockpool was able to
teristics. Environmental conditions in the second rockpool photosynthesize at high rates in rockpool water (con-
were followed during the sunny day of 10 August. taining 0±45 mol m−$ Ci) buffered to pH 9±5 (which was
Rates of net photosynthesis were measured as O
# close to the pH measured in the rockpool at the time of
evolution in 3 ml magnetically stirred and thermostatted plant collection). This photosynthesis was inhibited by
(to 22 °C) O -electrode chambers (CS Larsson UW-
# more than 90 % by the AE1 inhibitor DIDS (Table 1).
technique, Lysekil, Sweden) equipped with Clark-type O
#
electrodes (YSI model 5331). The O levels were followed
#
on a strip-chart recorder. Light was provided by fibre- Table 1. Net photosynthetic O evolution rates of Enteromorpha
#
optics-equipped halogen lights. To prevent photodynamic intestinalis in rockpool water, buffered to two different pH values,
effects of DIDS (which may interfere with the O containing 0±45 mol m−$ Ci (control), and rates (as percentage of
# the controls) remaining after additions of inhibitors of the two
measurements ; Axelsson, unpublished), the light was
mechanisms for HCO− utilization (DIDS, 300 mmol m−$ ; AZ,
filtered through a yellow filter (Perspex 2200). This $
100 mmol m−$)
arrangement resulted in a photon flux density of c.
1000 µmol photons m−# s−" (400–700 nm) within the O
# Control DIDS AZ AZDIDS
chambers (as measured with a LI-COR LI-1000 sensor).
pH (µmol g−" Fw h−") (% of control) (% of control) (% of control)
The tips (5–10 mm) of E. intestinalis thalli were cut off
and discarded, while the next 60 mm sections were cut 9±5 130±8³41±8 9±0³8±0 112±3³2±5 9±8³4±0
into 10 mm segments and used for the experiments. All 8±4 82±3³14±0 52±3³3±7 116±7³6±2 24±3³3±4
algal segments were mixed and rinsed in the medium to be
used, and six pieces were placed in each O -electrode
# Data are average of three to six measurements³SD carried out on plants
chamber. Photosynthetic O production was measured collected on 3 August.
#Photosynthetic carbon utilization by Enteromorpha intestinalis 51
Table 2. Net photosynthetic O evolution rates of Enteromorpha
#
intestinalis in synthetic seawater, buffered to two different pH
values, containing 1±0 mol m−$ Ci (control), and rates (as
percentage of the controls) remaining after additions of inhibitors
of the two mechanisms for HCO− utilization (DIDS,
$
300 mmol m−$ ; AZ, 100 mmol m−$)
Control DIDS AZ AZDIDS
pH (µmol g−" Fw h−") (% of control) (% of control) (% of control)
9±5 50±6³18±9 17±7³0±5 100±0³0±0 12±2³3±1
8±4 93±3³19±7 82±3³11±4 56±0³1±4 23±0³5±3
Fig. 1. Rates of net photosynthetic O evolution (NPS) by
#
Enteromorpha intestinalis as a function of Ci concentration at
Data are averages of three to six measurements³SD carried out on pH 8±4 (open symbols) and pH 9±5 (filled symbols).
plants collected on 9 August. Photosynthesis was measured either in the presence of the AE1
inhibitor DIDS (300 mmol m−$), illustrating the Ci-uptake
Similar results were obtained in non-buffered rockpool characteristics of the CA-mediated mechanism (circles), or in the
water, showing that the AMPSO buffer per se did not presence of AZ, an inhibitor of external CA (100 mmol m−$),
illustrating the response of DIDS-sensitive HCO− uptake
interfere with photosynthetic rates and, thus, allowing $
(diamonds). Data are from one experiment conducted on 9
for its use in subsequent experiments to prevent pH August.
changes in longer-term measurements and after the
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addition of AZ (the stock solution of which was strongly
Table 3. Photosynthetic Vmax and K " (Ci) values for Enteromorpha
basic). Photosynthesis of E. intestinalis was not inhibited #
intestinalis, at two different pH values, in the presence of DIDS
(but in fact slightly stimulated) by AZ, an inhibitor of (300 mmol m−$) to illustrate the Ci-uptake characteristics of the
external CA, at pH 9±5. In rockpool water buffered to CA-mediated mechanism or in the presence of the CA inhibitor
pH 8±4, the inhibition by DIDS alone was some 50 % only, AZ (100 mmol m−$) to illustrate the response of the DIDS-
suggesting that more than one HCO− utilization mech- sensitive HCO−-uptake mechanism
$ $
anism was operable at that pH. A complementary addition
of AZ caused a further inhibition of photosynthesis, Lineweaver–Burk plot
verifying the presence of the CA-mediated mechanism. Hanes plot
After this addition of AZ, 25 % of the original rate still Condition Vmax (µmol O g−" h−") K" (mol m−$) Vmax (%)
# #
remained, most of which probably resulted from uptake of
pH 8±4AZ 35±1³18±3 0±17³0±12 86±1³10±9
CO supplied from the spontaneous dehydration of
# pH 8±4DIDS 197±5³55±0 1±35³0±50 75±3³20
HCO−. Such remaining photosynthesis after both pH 9±5AZ 44±6³17±7 0±31³0±06 102±3³6±5
$
inhibitors had been added was considerably lower at pH 9±5DIDS – "3 –
pH 9±5 (c. 10 % of the original rate), which is in agreement
both with the lower fraction of CO present at Ci
# Data are averages of three experiments (³SD), in each of which the net
equilibrium and the much lower rate of spontaneous photosynthetic O evolution was measured in the range of
#
HCO− dehydration at that pH (Johnson, 1982). Despite 0±1–2±2 mol m−$ Ci. Plants were collected on 9 August.
$
the presence of a CA-mediated mechanism, the addition of
AZ alone did not reduce the rate of photosynthesis at occasions, however, it may be due to differences in the
pH 8±4. Thus, at the comparably low Ci concentration of physiological states of the plant material.
0±45 mol m−$, the DIDS-sensitive mechanism alone was By applying a selective inhibitor for one of the HCO−
$
capable of supplying most of the Ci uptake. utilization mechanisms at a time, it was possible to assess
The photosynthetic responses of E. intestinalis were the capacity of the other. This was done at two different
also examined at a higher Ci concentration (1 mol m−$) pH values by adding increasing concentrations of Ci after
in SSW. The results verify the presence of both HCO− the addition of the inhibitor. The results of such an
$
utilization mechanisms, of which the CA-mediated experiment are shown in Fig. 1, while Table 3 summarizes
mechanism did not function at the higher pH (i.e. AZ alone photosynthetic Vmax and K" (Ci) values of three
#
had no effect at pH 9±5 ; Table 2). At pH 8±4, on the other experiments. In the presence of DIDS, the CA-mediated
hand, AZ caused a significant reduction in photosynthesis mechanism was the only mode of HCO− utilization in
$
rates, while as much as 80 % of the rate remained after operation and CO , mainly derived from catalysed HCO−
# $
adding DIDS alone. The probable reason for the difference dehydration, was the only Ci form crossing the plasma-
between these results and those above (i.e. in natural lemma. Under such conditions E. intestinalis exhibited
rockpool water buffered to pH 8±4) is that the function of high photosynthetic rates over most of the Ci range at
the CA-mediated mechanism is favoured at higher Ci pH 8±4 (open circles in Fig. 1) and showed a high Vmax. In
concentrations. There is no apparent reason for the addition, Ci saturation was nearly reached at the normal
difference in photosynthetic rates at pH 9±5 between seawater concentration (2 mol m−$). At pH 9±5, corre-
Tables 1 and 2 ; since the algae were collected on different sponding net photosynthetic rates were low and reachedC. Larsson et al. 52
response to Ci. At pH 9±5, the almost identical Vmax values
may be based on HCO− uptake only, since the con-
$
tribution of CO at such a high pH must be minimal.
#
Examination of the physical and chemical conditions of
a rockpool during a sunny day confirmed high pH values,
high O concentrations, low Ci levels and high levels of
#
nutrients other than Ci (Fig. 2). Comparing these findings
with the photosynthetic responses of E. intestinalis (Fig. 1)
reveals that, during most of the day, the pH of the water
is so high and the Ci concentration so low as not to allow
any Ci utilization via the CA-mediated mechanism, but
only via the DIDS-sensitive one. There is also a decrease
in the Ci concentration of the rockpool throughout the
day, confirming that photosynthetic Ci uptake by E.
intestinalis exceeds the CO supply from animals or from
#
the atmosphere. In the early morning, before photo-
synthesis starts, the Ci concentration is highest and the pH
reaches its lowest value.
Fig. 2. Diurnal variations in some physical and chemical
parameters of a rockpool similar to the one from which
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experimental plants were taken. (A) Scalar photon flux density
Discussion
(PFD), temperature and salinity ; (B) dissolved inorganic carbon The two known mechanisms for HCO− use in marine
(Ci), oxygen concentration (O ) and pH ; (C) total inorganic $
# macroalgae, i.e. extracellular CA-catalysed HCO− de-
nitrogen (N-tot), nitrate (NO−), ammonium (NH+) and phosphate $
$ % hydration and direct HCO− uptake, are both present in E.
(PO$−) concentrations. The first three values (to the left of the
%
$
dotted line) are the same as those measured at the end of the intestinalis. This is evidenced by the effects of the inhibitors
period (so as to show the periodicity more clearly). of each mechanism (AZ and DIDS ; cf. Beer, 1994 ;
Axelsson et al., 1995) when added subsequently to
photosynthesizing thalli. However, when studied at
zero at c. 0±5 mol m−$ Ci (filled circles in Fig. 1). The shape pH 9±5 and 0±45 mol m−$ Ci, the thalli showed no
of the Ci response curve at pH 9±5 during DIDS inhibition evidence of a functional CA-mediated mechanism, and
did not allow for the determination of any Vmax or K" only the DIDS-sensitive mechanism was utilized. Since the
#
values, but a comparison of the initial slopes at the two pH pH was even higher, and the Ci concentration lower, in
values suggests that the K" at the higher pH was about 10 the rockpool during most of the day (cf. Fig. 2), it follows
#
times that at the lower pH and that Ci saturation occurred that E. intestinalis living therein utilized only HCO− uptake
$
at a concentration far above that of natural seawater via the DIDS-sensitive mechanism during that time. It has
(assuming that the Vmax was about the same at the two been suggested earlier that direct HCO− transport is
$
pH values). In the presence of AZ, photosynthetic HCO− favoured under such conditions since the equilibrium CO
$ #
utilization should be based on HCO− uptake via the concentration at high pH values would be extremely low
$
DIDS-sensitive mechanism. In this case, maximal Ci-based (e.g. Axelsson et al., 1995). At pH 9±5, and 0±45 mol m−$
O evolution was similar at pH 8±4 and pH 9±5 (diamonds Ci, the CO concentration is c. 0±05 mmol m−$, and it
# #
in Fig. 1), and Ci saturation occurred well below the would be even lower at pH 10 (c. 0±006 mmol m−$).
natural seawater Ci concentration (but close to the Ci level Therefore, it is unlikely that E. intestinalis could make use
found in the rockpool, i.e. c. 0±5 mol m−$). The results of of this Ci form even if its rate of resupply were secured by
these measurements thus verify the presence of two extracellular}surface-bound CA. Indeed, as evidenced
HCO−-utilizing mechanisms in the E. intestinalis collected here, the extracellularly acting CA inhibitor AZ had no
$
from a rockpool : a DIDS-sensitive mechanism with effect on photosynthetic rates in rockpool water (nor in
comparatively low maximal capacity (Vmax) but a high SSW of high pH).
affinity for Ci (i.e. a low K" value) at both pH 8±4 and 9±5 At high pH value, the CO#− concentration is high and,
# $
(Table 3), and a surface-bound CA-mediated mechanism since HCO− utilization via dehydration is not operating,
$
with high maximal capacity (Vmax) but a low affinity (i.e. the question arises whether CO#− (in addition to HCO−)
$ $
high K" value) for Ci which was very pH-dependent. For could be used directly by E. intestinalis. Uptake of CO#−
# $
the CA-mediated mechanism at pH 8±4, the Lineweaver– has been viewed as both non-existent and feasible :
Burk plot (which emphasizes photosynthetic rates at low Maberly (1992) found that the presence of CO#− did not
$
Ci concentrations) gives a significantly higher Vmax than affect photosynthesis rates of U. lactuca collected from
the Hanes plot (which emphasizes rates at high Ci levels). British tidal pools while Drechsler et al (1994) found that
While this difference may have several explanations, the the affinity for Ci at high pH values was in accordance
more similar Vmax values calculated from the two plots for with the uptake of both HCO− and CO#−. In the latter
$ $
the DIDS-sensitive mechanism suggest a simpler kinetic case, it was shown that residues of the high-pK aminoPhotosynthetic carbon utilization by Enteromorpha intestinalis 53
acids arginine and lysine probably comprised the binding} the thalli (up to pH 10 within the unstirred boundary layer
transport site for HCO−, and that divalent anions might of Ulva ; Beer & Israel, 1990). In the Swedish rockpool, the
$
also be utilized by the same transporter. In this study, the pH and non-Ci nutrient levels were high and, due to the
DIDS-sensitive mechanism features a significant difference photosynthetic activity and the stagnant water, it is likely
in Ci affinity at different pH values (Fig. 1, Table 3). Since that the pH adjacent to the E. intestinalis thalli was even
the HCO− concentration is about 3 times lower at the higher. Thus, in both of these habitats the CO con-
$ #
higher pH, such a difference is in line with the assumption centrations adjacent to the thalli of photosynthesizing
that only HCO− is taken up by this mechanism. algae must be so low that the CA-mediated mechanism
$
While only the function of the DIDS-sensitive mech- common to many algae is not sufficient to supply enough
anism was found to be of importance for E. intestinalis Ci. It is suggested that the DIDS-sensitive HCO− uptake
$
under the high-pH}low-Ci rockpool conditions, inhibition mechanism has evolved as a response to such conditions,
of the CA-mediated mechanism with AZ reduced the and that it is expressed especially under conditions of
photosynthetic rates at pH 8±4 and 1 mol m−$ Ci. The fact severe CO limitation. It is further suggested that this trait
#
that the latter mechanism was present (albeit not functional is a contributing factor allowing these opportunistic green
at high pH) points to a potential for its use under algae to occupy the CO -constraining habitats in which
#
conditions of relatively low pH and high Ci concen- they grow. The fact that U. lactuca (which possesses the
trations. Such conditions are present in the morning hours potential for a similar DIDS-sensitive HCO− uptake
$
or, alternatively, when the rockpools become flooded with mechanism ; Axelsson et al., 1995) does not thrive in
fresh seawater. Thus, the presence of both mechanisms of Swedish rockpools illustrates the truism that other traits,
HCO− utilization can be seen as an ideal adaptational not connected with Ci utilization, are also of importance
$
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feature of E. intestinalis to normal seawater as well as to the for determining the growth habitats of marine green algae.
varying conditions within the rockpool on both a diurnal
and a longer-term basis. Also, the maximal capacity (as Acknowledgements
reflected in the Vmax value) of the CA-mediated mechanism
is higher than that of the DIDS-sensitive mechanism, and Dr G. Magnusson is thanked for the help with nutrient
this feature can be favourably utilized at higher Ci analyses. The provision of working facilities at
concentrations during, for example, flooding of the Kristineberg Marine Research Station is greatly appreci-
rockpool. Under stagnant conditions of high pH and ated. This investigation was supported by the Royal
lower-than-ambient Ci concentrations, however, DIDS- Swedish Academy of Sciences, the Swedish Natural
sensitive HCO− uptake can support positive photo- Science Research Council, the Royal Society of Arts and
$ Sciences in Gothenberg, the Magnus Bergvall foundation,
synthetic rates while the CA-mediated mechanism under
such conditions could not account for any photosynthesis the Lars Hierta foundation, and the R. J. Gust Richert
at all (cf. Figs 1, 2 and Table 3). foundation.
The DIDS-sensitive mechanism has previously been
described only for two Ulva species, and only forms References
growing in the eastern Mediterranean featured HCO−
$ A, L., U, J. & R, H. (1991). Mechanisms for con-
uptake via such a mechanism in nature (Drechsler & Beer, centrating and storage of inorganic carbon in marine macroalgae. In
1991 ; Drechsler et al., 1993, 1994). Despite the fact that Seaweed Cellular Biotechnology, Physiology and Intensive Cultivation (Garcia-
inducible Ci utilization at high pH appears to be an almost Reina, G. & Pederse! n, M., editors), 185–198. COST 48 : Universidad de
Las Palmas de Gran Canaria.
universal property of green macroalgae (Carlberg et al.,
A, L., R, H. & B, S. (1995). Two modes of bicarbonate
1990), no DIDS-sensitivity has so far been reported for utilization in the marine green macroalga Ulva lactuca. Plant, Cell Environ.,
field-collected algae from other regions. It is likely that an 18 : 439–445.
induction of HCO− utilization at high pH reflects the B, S. (1994). Mechanisms of inorganic carbon acquisition in marine
$ macroalgae (with special reference to the Chlorophyta). Prog. Phycol.
induction of DIDS-sensitive HCO− uptake (as shown for
$ Res., 10 : 179–207.
laboratory-grown U. lactuca ; Axelsson et al., 1995). If B, S. & I, A. (1990). Photosynthesis of Ulva fasciata. IV. pH, carbonic
so, the degree of induction of HCO− utilization at high anhydrase and inorganic carbon conversions in the unstirred layer. Plant,
$
pH measured for field-collected green algae from the Cell Environ., 13 : 555–560.
B$ , M., H, K., R, Z., G-R, G. & P! , M.
Swedish west coast (Larsson et al., 1990) suggests that
(1992). Inorganic-carbon assimilation in the green seaweed Ulva rigida C.
only a low level of this mechanism was present in Ulva Ag. (Chlorophyta). Planta, 187 : 152–156.
and Enteromorpha spp. collected from exposed areas, while B$ , M., H, K., R, Z. & P! , M. (1993). Inducible
Enteromorpha spp. collected from sheltered regions of the mechanism for HCO− utilization and repression of photorespiration in
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protoplasts and thalli of three species of Ulva (Chlorophyta). J. Phycol. 29 :
eulittoral, and especially from rockpools, featured higher
166–173.
levels of this mechanism. With the present addition of E. C, S., A, L., L, C., R, H. & U, J. (1990).
intestinalis to Ulva fasciata (Drechsler et al., 1993), there are Inducible CO concentrating mechanisms in green seaweeds. I.
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now two genera known in which HCO− can be taken up Taxonomical and physiological aspects. In Current Research in Photo-
$ synthesis, vol. IV (Baltscheffsky, M., editor), 529–532. Kluwer, Dordrecht.
via a DIDS-sensitive mechanism. In the eastern
D, Z. & B, S. (1991). Utilization of inorganic carbon by Ulva
Mediterranean, the high ambient temperature, light and lactuca. Plant Physiol., 97 : 1439–1444.
nutrient levels are conducive to high pH values adjacent to D, Z., S, R., C, Z. I. & B, S. (1993). BicarbonateC. Larsson et al. 54
uptake in the marine macroalga Ulva sp. is inhibited by classical probes of and field observations. In Current Research in Photosynthesis, vol. IV
anion exchange by red blood cells. Planta, 191 : 34–40. (Baltscheffsky, M., editor), 533–536. Kluwer, Dordrecht.
D, Z., S, R., C, Z. I. & B, S. (1994). The M, S. C. (1990). Exogenous sources of inorganic carbon for photo-
relationship of arginine groups to photosynthetic HCO− uptake in Ulva synthesis by marine macroalgae. J. Phycol., 26 : 439–449.
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sp. mediated by a putative anion exchanger. Planta, 194 : 250–255. M, S. C. (1992). Carbonate ions appear to neither inhibit nor stimulate
G, B. (1971). Studies on chemical, physical and biological conditions use of bicarbonate ions in photosynthesis by Ulva lactuca. Plant, Cell
in Swedish rockpool ecosystems. Ophelia, 9 : 51–105. Environ., 15 : 255–260.
G, M. & M, S. C. (1989). Distribution of carbonic anhydrase S-J, K. & G, D. M. (1984). Differential ability of marine and
in British marine macroalgae. Oecologia, 81 : 534–539. freshwater macrophytes to utilize HCO− and CO . Mar. Biol., 80 :
$ #
J, K. S. (1982). Carbon dioxide hydration and dehydration kinetics in 247–253.
seawater. Limnol. Oceanogr., 27 : 849–855. T, J. P. & D-J, A. I. (1980). Oxygen and carbon dioxide
L, C., A, L., C, S., R, H. & U, J. (1990). in the marine intertidal environment ; diurnal and tidal changes in
Inducible CO concentrating mechanisms in green seaweeds. II. Ecology rockpools. Respir. Physiol., 39 : 241–254.
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