Plant Physiol. (1977) 59, 936-940
Photosynthesis and Photorespiration in Algae'
Received for publication December 2, 1976 and
NIGEL D. H. LLOYD,2 DAVID T. CANVIN,
AND
DAVID A. CULVER3
Department of Biology, Queen's University, Kingston,
ABSTRACT
The CO2 exchange of several species of fresh water and marine algae
was measured in the laboratory to determine whether photorespiration
occurs in these organisms. The algae were positioned as thin layers on
filter paper and the CO2 exchange determined in an open gas exchange
system. In either 21 or 1% 02 there was little difference between 14CO2
and 12CO2 uptake. Apparent photosynthesis was the same in 2, 21, or
50% 02. The compensation points of all algae were less than 10 id 1-1.
CO2 or 14CO2 evolution into C02-free air in the light was always less than
the corresponding evolution in darkness. These observadons are inconsistent with the proposal that photorespiration exists in these algae.
Algae are C3 plants but there is still controversy regarding the
existence or nature of photorespiration (7, 8, 33). Many algae
have been shown to produce glycolate (28, 33) and to possess
the enzymes of the glycolate pathway (28, 33). The inhibition of
photosynthesis by 02 or the Warburg effect was first shown in
algae, and has since been extensively studied (2, 34). Some
workers, however, have found no effect of 02 on CO2 fixation in
algae (1, 16, 18) and many algae show low compensation points
(4, 25, 35) and release less CO2 in the light compared to the dark
(7, 17).
In higher plants, CO2 evolution and CO2 exchange are the
most extensively studied aspects of photorespiration (36). In
algae, although CO2 evolution during photosynthesis has been
implied (33), few studies have been performed on CO2 exchange
because of the difficulties imposed by the aqueous medium. In
view of the paucity of information and the diversity of observations and opinions on CO2 exchange in algae, we decided to
investigate the CO2 exchange of several species of algae using an
open gas analysis system such as that used for measurement of
CO2 exchange in higher plants (15, 26).
MATERIALS AND METHODS
The following algae were obtained from the Indiana University Culture Collection, and were grown on Gorham's culture
medium No. 11 (21): Chlorella pyrenoidosa Chick (strain 252),
Scenedesmus quadricauda (Turp.) Breb. (strain 76), Chlamydomonas reinhardtii (-) (strain 90), and Anabaena flos-aquae
(Lyngbye) Breb. (strain 1444). Navicula pelliculosa (Breb.)
Hilse was supplied by T. Murphy at Canada Centre for Inland
Waters, Burlington, Ontario, and was grown on Chu No. 10
medium (9). All of the above species were grown with continuous aeration and light. Chlorella and Anabaena were also grown
I
Supported in part by the National Research Council of Canada and
Environment Canada, Fisheries and Marine Service.
2 Present address: Department of Biology, Carleton University, Ottawa, Ontario Canada.
3 Present address: Department of Zoology, Ohio State University,
Columbus, Ohio.
in revised form January 14, 1977
Ontario K7L 3N6
in cultures bubbled with 0.5 and 5% CO2 in air. Mougeotia sp.
was grown as a unialgal culture and supplied by B. Colman,
Department of Biology, York University, Downsview, Ontario.
Anacystis nidulans (Richt.) Drouet was grown on Gorham's
medium (21) bubbled with 1.5% CO2 and supplied by K. Budd,
Queen's University. Dunaliella tertiolecta, Thalassiosira fluviatilis, and Porphyridum sp. (Levin strain) were supplied by J.
Craigie at the Atlantic Regional Laboratory, Halifax, Nova
Scotia. These marine species were grown on a shaker without
aeration with a 16-hr photoperiod.
All species were grown at 25 C and a quantum flux density of
80 to 100 ,ueinsteins m-2 sec-'. All cultures were axenic with the
exception of Mougeotia.
Cells were harvested during linear growth phase, and concentrated, where necessary, by settling and decanting the medium.
Algae were suspended as an "artificial leaf" (12) to facilitate gas
exchange and rapid changes in gas composition. The cells were
filtered on Whatman No. 3 filter paper, producing an even
double layer of cells (4 x 4 cm). This square was cut out and
enclosed in the leaf chamber for the gas analysis measurements.
The total volume of medium on the filter paper was approximately 0.3 ml. Similar results were obtained when the algae
were suspended on 10-gm Nitex nylon mesh (B and S. H.
Thompson & Co., Montreal, Quebec).
The open gas analysis system was as previously described (15,
26). Measurements were started about 30 min after the algae
were placed in the leaf chamber because the rate of apparent
photosynthesis increased about 30% during that time but thereafter remained constant. All measurements, with the exception
of studies on the effect of temperature, were done at 25 C and
light saturation (see Fig. 1). The relative humidity of the air
entering the leaf chamber was maintained above 90% to avoid
desiccation of the cells. Quantum flux densities were measured
with a Lambda quantum sensor.
Rates of true photosynthesis, apparent photosynthesis, and
photorespiration were calculated as previously described (26)
except that it was necessary to do a control measurement with
filter paper and medium alone, and to subtract the rate of "4CO2
uptake obtained from that obtained with the algae included. This
correction was only necessary during the first min of "CO2
supply and eliminated any error caused by uptake of 14CO2 by
the medium. Rates are the means of three or four determinations.
Compensation points were obtained by measuring CO2 exchange at CO2 concentrations both above and below the compensation point and interpolating to the point where there was
zero net photosynthesis.
Chlorophyll content was determined after extraction with
80% acetone by the method of Bruinsma (5) or by extraction
with acetone, methanol, H20 (80:15:5, v/v/v) with sonication
according to the method of Daley et al. (14).
RESULTS
Light response curves of photosynthesis for Anabaena, Navicula, and Chlorella are shown in Figure 1. Apparent photosyn-
936
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Copyright © 1977 American Society of Plant Biologists. All rights reserved.
Plant Physiol. Vol. 59, 1977 PHOTOSYNTHESIS AND PHOTORESPIRATION IN ALGAE
240
NAVICULA
160-
A-
E
at
80
U
l
80_
~~~~CHLORELLA
w
z
0
and Navicula at 2, 21, or 50% 02 and of Chiorella at 21% 02. Temperature was 25 C, CO2 concentration 350 11-1 in air. Data for the three02
concentrations at each light intensity fall within the symbol.
thesis of all species of algae was saturated at about 200 ,uein-
stemns m-2 sec-1 and no inhibition was observed at high light
intensities. Light compensation points were
about 20
mueinsteins
m-2 sec-' with both Anabaena and Navicula and the 02 concentration had no effect on photosynthesis of Anabaena or Navicula
at any quantum flux density.
The response of apparent photosynthesis to CO2 concentration for Navicula, Anacystis, and Chlorella is shown in Figure 2.
Although the photosynthesis of Navicula was not close to saturation until 1,000 ,ul l-l CO2, Anacystis and Chiorella appeared to
be close to saturation at 350 ,ul 1'u.The latter concentration was
used for the "eCO2 uptake measurements and there could then be
some variation in the degree of CO2 saturation for the various
algae. This should not have much effect on the attempts to
measure photorespiration, however, as photorespiration has
been shown to be independent of CO2 concentration in that
range (27).
When a minimum estimate of true photosynthesis was determined with "CO2f2C02,
and apparent photosynthesis with
most
of the algae had rates of true photosynthesis approximately
equal to apparent photosynthesis and therefore no, or very little
photorespiration in either 1% or 21% 02 (Table I). These
measurements were obtained at 42 sec after the introduction of
the 2CO2
but similar results were obtained 3 to 4 mn after
exposure "iCO2.
to
In those cases where rates of true photosynthesis were larger than apparent photosynthesis, i.e. where there
appeared to be photorespiration, there was no effect of 02 on
apparent photosynthesis; rather the effect was due to changes in
true photosynthesis. If the algal photosynthesis responded similarly to 02 as higher plants, then both true and apparent photosynthesis should be higher in 1% 02 (27). As the "CO2 fluxes
were very small (about 5% of the rates determined with sunflowers) they were subject to considerable uncertainty and this may
be the cause of the few differences noted.
In the above experiments, there was little effect of 02on the
rates of apparent photosynr tsis (Table I), but since two preparations of algae were often involved some variation could be
expected. To reduce this variation, it was desirable to study the
effect of 02 on apparent photosynthesis of the same preparation
and to vary the 02 concentration rapidly over a wider range.
Measurements at each 02 concentration were continued for 10
937
to 15 min before switching to another concentration. The order
of 02 concentration exposure had no effect and rates for each 02
concentration were constant throughout the measurement period. The results of this systematic study are presented as rates of
photosynthesis relative to the rate that occurred in 21% 02
(Table II). In all cases, there was little or no difference between
the rates of photosynthesis in 2, 21, or 50% 02 (Table II). Also,
there was no interaction between the CO2 concentration and the
02 concentration (Table II).
Carbon dioxide compensation points were determined for the
algae by interpolation to the point of zero net photosynthesis
(Fig. 3). In all cases, the compensation points were below 10 ,tl
1-' CO2 (Table III) and were not changed at 02 concentrations
of 2 or 50% nor by temperature changes between 15 and 35 C.
Rates of release of CO2 into C02-free air in light and darkness
are shown in Table III. In all cases CO2 evolution in the light was
less than in the dark with the light/dark ratios ranging from 0.04
to 0.44. 4CO2 release after 3 min in the light is also less than that
in darkness with light/dark ratios ranging from 0.20 to 0.74
(Table IV). As the relative specific radioactivity of the "4CO2
released in the light and darkness is about the same, the ratio of
CO2 released at 3 min of flushing would be similar to the ratios
of "4CO2 release. Thus, at no time during a C02-free flush does
CO2 or "4CO2 release in the light exceed that released in darkness.
Chlorella and Anabaena cultures were also grown on 0.5 and
5% CO2 to determine if the CO2 concentration during growth
affected the CO2 gas exchange characteristics of the algae. Photosynthesis of these cultures was measured in air. The rate of
photosynthesis of the 0.5 and 5% C02-grown Chlorella was 51%
and 0%, respectively, of the rate of photosynthesis of air-grown
cells. The 5% C02-grown cells were not dead, though, as over a
period of 3 hr, the photosynthetic rate increased to that observed
in the air-grown cells. In 0.5% C02-grown Anabaena, the rate of
photosynthesis was 158% of the rate of air-grown cells but an
inhibition to 48% of the rate of photosynthesis of air-grown cells
was observed with the 5% C02-grown cultures. In all cultures
where measurements could be performed, no change was found
in the compensation points. The low rates of photosynthesis and
the adaptation in photosynthetic rate that was observed in the
algae on changing from a high to low CO2 concentration are well
known in green (3) and blue-green (24) algae.
FIG. 2. Effect of CO2 concentration on net photosynthesis of Navicula, Anacystis, and Chlorella. Temperature was 25 C and quantum flux
density 270 ,±einsteins m-2 sec-'.
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Copyright © 1977 American Society of Plant Biologists. All rights reserved.
938
LLOYD, CANVIN, AND CULVER
Plant Physiol. Vol. 59, 1977
Table I.
True photosynthesis, apparent photosynthesis and photorespiration in several
species of algae.
All determinations w re made 42 sec after the introduction of 14co at 25 C, 350 A1 1-1 Co
270 ueinstein m72 sec-L quantum flux at either 21 or
°
2
002
lN
1%
21% 02
Algae
TPS1
PR1
APS1
umol
Chlorella
Scenedesmus
Chlamydomonas
Mougeotia
Anabaena
Anacystis
Navicula
Dunaliella
Porphyridium
Thalassiosira
1.
2.
61
104
73
29
312
189
237
11.4
27
14.5
± 102
±
±
±
±
±
±
±
±
±
22
5
3
16
41
17
0.6
3
2.3
± 5
± 5
Apparent Photosynthesis
2% 02
350
41 1-1 C02
1000
21% °2
5
5
3
62 ± 5
93 ± 1
52 ± 1
-5 ± 5
16 ± 3
43
243
200
212
6.2
29
14
18
9
0.6
3
1
8 ± 7
7
5
4
0.7
± 1
0.3
±
-43
0
-3
-0.2
15
0.1
±
±
±
±
Relative Rate
102
1001
96
104
1oo1
99
103
1001
100
10l
102
100
97
100
1ool
± 43
± 19
10
± 0.7
3
± 1
109
102
102
we
could find
evolution
in
the
no
consistent evidence for the
light
by
the
algae
(Table
I).
presence
In
of
addition,
when the 02 concentration was decreased to 1 %, there was little
measurements
(Table I),
a
finding in sharp
contrast to that observed with higher plant
leaves where both true and apparent photosynthesis is stimu-
lated and photorespiration is eliminated (27).
The apparent scarcity of CO2 evolution in the light was conby rates of C02 or 04C2 evolution into CO2-free air
(Tables III and IV) in the light which were lower, in all cases,
firmed
th4w
than CO2 or
160l
100
1001
101
consistent with those of several other workers (7, 17) but inconsistent with those of Zelitch (36). The lower CO2 or "CO2
evolution in the light could be ascribed to refixation but the
insensitivity of this CO2 or "4CO2 evolution in the light to
changes in 02 concentration (17) indicates that the process
producing the CO2 is quite different from that in higher plants.
100
1O
104
103
100
103
100
108
113
95
91
100
100
100
100
91
100
CO2
105
1001oo
104
thesis,
effect on the relationship between the
50 % 02
41 1-1 c02
Chlorella
Anabaena
Navicula
PR
True photosynthesis, apparent photosynthesis and photorespiration.
Mean ± standard deviation, n = 3 or 4.
Relative rates of apparent photosynthesis at 3 oxygen
concentrations in se veral species of alga.
Temperature was 25 C and quantum flux 270 peinstein m72 sec-1.
Chlorella
Scenedesmus
Chlamydomonas
Mougeotia
Anabaena
Anacystis
Navicula
Dunaliella
Porphyridium
Thalassiosira
150 4l 1-1 C02
Chlorella
Anabaena
Navicula
02
APS
mg-1 chl hr-1
6 ± 11
70 ±
-11 ± 22
88 ±
± 0.8
68 ±
18 ± 5
-3 ± 3
± 2
264 ± 4
48 ± 22 200 ±
196 ± 7
-7 ± 41
200 ±
236 ± 4
1 ± 17 209 ±
4.3 ± 0.6
7.1 ± 0.8
6 ±
27 ± 2
44 ±
0± 4
17.3 ± 1.1 -2.8 ± 2.5 14.1 ±
55
115
55
32
Table II.
Algae
TPS
CO2
evolution in darkness. These observations are
1
95
1. Apparent photosynthetic rate shown in Table I.
DISCUSSION
Higher plants, which fix carbon via the C3 pathway, exhibit the
process of photorespiration (8, 36). In terms of CO2 exchange,
which is the best studied aspect, the presence of photorespiration
is shown by a higher rate of 14CO2 uptake than 12CO2 uptake
when "4CO2 is initially supplied (27), a marked effect of 02 on
photosynthesis (1, 16, 17, 27), a CO2 compensation point exceeding 40 Al 1-1 (8, 36), and CO2 or "4CO2 evolution into C02free air in the light at a rate that exceeds the rate of evolution of
these molecules in the dark (15, 27).
These characteristics of photorespiration have not been systematically investigated in algae, primarily because of the difficulties of CO2 exchange between the gas phase and the aqueous
medium in which the algae are suspended. Over short periods of
time, if physical support and adequate moisture are provided,
most of the aqueous medium could be removed without harmful
effects. Diffusion of CO2 to the cells would be facilitated and
CO2 exchange could be investigated. That photosynthesis of the
algae was not adversely affected by removal of the medium was
shown by typical responses to light (Fig. 1) and CO2 (Fig. 2) (30,
35, 36).
Using the "4CO2/'2CO2 technique (26), which is presently the
only technique for detecting photorespiration during photosyn-
§20O
/ANABAENA
/
2
15
E
2
k
[C
H
LHLORELLA
10
co
w
u)
5/
0~~~~
0~~~
12
8
[C02]
(MI
16
1gJ)
-5
FIG.
3.
Rate of net
concentrations Of CO2.
plots. Quantum flux
photosynthesis of Anabaena and Chlorella at low
Compensation points were determined from such
270 ~ieinsteins M-2 sec-' and 02 concentration
21%.
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Plant Physiol. Vol. 59, 1977 PHOTOSYNTHESIS AND PHOTORESPIRATION IN ALGAE
Compensation points and C02 evolution into C02-free
air by several species of algae.
Temperature 25 C, 21% 02, light intensity 270 peinstein m 2 sec 1
evolution measured 15 min after transfer to C02 free air.
Table III.
C02 Evolution
Algae
Light
imol
Scenedesmus
Chlamydomonas
Mougeotia
Anabaena
Anacystis
Navicula
Dunaliella
Porphyridium
Thalassiosira
Point
mg7l
,l 1-1
chl hr-l
35.0
22.5
16.9
9.9
60.6
96.0
69.8
0.5
15.5
7.7
0.8
Chlorella
Compensation
Ratio
Light
Dark
Dark
2.4
4.8
24.0
9.3
0.2
0.9
0.3
C02
0.4
0.34
6
8
0.04
0.25
0.08
1
5
2
6
0.25
0.13
3
1
4
4
0.40
0.34
0.15
2.7
2.2
14co evolution into C02 free air after 3 min in
the ight or darkness by several species of algae.
Conditionsas for Table III. Algae had fixed 14C02 for 30 min
prior to flushing.
Table IV.
04C02
Algae
Light
Chlorella
Scenedesmus
,mol
Anabaena
11.6
Relative
4C02
4C02
Dark
x 102
31.5
4.9
25
Navicula
1.
evolution
mg-1
42.3
20.4
63.0
57.6
specific activity
chl
hr-11
is the
Relative1
Specific
Ratio
Light
Dark
Light
Dark
0.74
0.24
0.40
0.20
30
52
51
55
56
60
74
60
Activity
specific activity
of the
evolved as a percentage of the specific activy of
supplied during the photosynthetic period.
The characteristics of the CO2 evolved indicate that it is
more
likely due to residual dark respiration, which, while apparently
suppressed (23, 32), may continue in the light.
The low compensation points (Table III) are not typical of C3
plants that show substantial CO2 evolution in the light (36).
Further, they are not sensitive to 02 concentration or temperature such as those of C3 plants (8, 36). These characteristics of
the compensation point are similar to those observed for C4
plants (36) and it has been suggested that blue-green algae may
fix CO2 by the C4 pathway (10) but other work shows that this is
not so (22).
Changes in 02 concentration had only a slight effect on the
rate of apparent photosynthesis (Tables I and II) and this was
entirely consistent with a lack of CO2 evolution. This result was
surprising in view of previous work (34) and in view of the fact
that the experimental system should allow ready access of the
new 02 concentration to the cells.
The lack of 02 effect on apparent CO2 fixation of algae has
been noted before (1, 16, 18) but these observations are greatly
overbalanced by a vast literature showing an inhibition of photosynthesis (2, 34) by increased concentrations of 02. In most of
the earlier studies, the inhibition of photosynthesis by 02 has
been determined at 02 concentrations between 21 and 100%
and by measuring photosynthesis as 02 evolution (34). An
inhibition of 02 evolution at increased 02 concentrations with
little effect on CO2 fixation has been noted by Fock et al. (16,
18). While this would, in part, reconcile our observations with
earlier results, the position is weakened by the fact that within
our present understanding of photosynthesis, an adequate explanation cannot be formulated for net CO2 fixation to exceed net
02 evolution (16, 18) for a substantial period of time. In addition, at least some of the earlier studies (2, 34) have shown
inhibition of CO2 fixation by increased 02 concentrations. While
the significance of it is not yet clear, one should also point out
that the 02 inhibition of photosynthesis observed in algae is not
affected by temperature (34) whereas there is a clear effect of
temperature
on
the
02
inhibition of photosynthesis in higher
939
plant leaves (8). It is perhaps no coincidence that all of the
studies (Table I and II; 1, 16, 18) in which no effect of 02 on
photosynthesis could be detected used algae suspended as thin
layers on a solid support but more work will be necessary before
the contradictory observations can be reconciled.
We have concentrated our efforts on trying to determine CO2
evolution in the light in algae because we have the equipment
and have used it for extensive measurements on higher plant
leaves, and because we believe that the CO2 exchange is the best
characterized aspect of photorespiratory gas exchange. Other
workers (6, 25) have studied photorespiration in algae by determining the 02 consumption that occurs in the light. This 02
uptake can be quite substantial (6, 25) but it would appear to be
due to the oxidation of some component in the photochemical
electron transport chain (6, 19, 25, 31) rather than to have
anything to do with either glycolate formation, its subsequent
oxidation, or CO2 evolution. While we do not deny that this 02consuming process has equal claim to the term "photorespiration," it is misleading to assume that CO2 photorespiration
through the glycolate pathway accompanies it. Perhaps, it is time
that our terminology in this area should be refined.
Strong cases have been made (28, 33) for the presence in
algae of photorespiration, which, except for a few modifications,
is similar to that in higher plants. In part, this position is based
on observations on glycolate excretion by algae. However, it
seems that significant glycolate excretion only occurs upon transfer of the algae from a high CO2 concentration to a low CO2
concentration (2, 11, 13, 20, 24, 29), a condition in which
photosynthesis is greatly suppressed (3, 24). Even then glycolate
excretion cannot account for the observed inhibition of photosynthesis by 02 (2) and either a direct inhibition is involved (2,
8) or a large portion of the glycolate is metabolized. Air-grown
algae do not excrete glycolate (11, 13, 24, 29) but since glycolate excretion can be forced using inhibitors (13, 29, 30), it is
implied that in air, the glycolate is metabolized via the glycolate
pathway (29, 33). Most of our algae were grown in air and we
could still not find any indication of CO2 evolution due to
metabolism of glycolate in the glycolate pathway. Inasmuch as
glycolate is not excreted under these conditions and because we
find no evidence for its metabolism, it may not be produced. We
are aware that such a suggestion raises questions concerning the
proposed origin of glycolate via the ribulose-1,5-diphosphate
oxygenase (8) in higher plant leaves as some mechanism would
now be necessary to protect the enzyme from 02 in the algae.
Nevertheless, our results, including the lack of effect of 02 on
apparent photosynthesis, are consistent with the view that under
normal conditions of growth, glycolate formation and photorespiration are absent in algae.
Acknowledgments - We acknowledge the technical assistance of A. McKendry and K. Lloyd.
LITERATURE CITED
1. BJORKMAN 0 1966 The effect of oxygen concentration on photosynthesis in higher plants.
Physiol Plan: 19: 618-633
2. BowEs G, JA BERRY 1972 The effect of oxygen on photosynthesis and glycolate excretion in
Chiamydomonas reinhardtU. Carnegie Inst Yearbook 71: 148-158
3. BiuGGs GE, CP WID-TINGHAM 1952 Factors affecting the rate of photosynthesis of
Chlordla at low concentrations of carbon dioxide and in high illumination. New Phytol 51:
236-249
4. BROWN DL, EB TREGUNNA 1967 Inhibition of respiration during photosynthesis by some
algae. Can J Bot 45: 1135-1143.
5. BRUINSMA J 1963 The quantitative analysis of chlorophylls a and b in plant extracts.
Photochem Photobiol 2: 241-249
6. BUNT JS, MA HEEB 1971 Consumption of 02 in the light by Chlorella pyrenoidosa and
Chlamydomonas reinhardtii. Biochim Biophys Acta 226: 354-359
7. CHENG KH, B COLMAN 1974 Measurements of photorespiration in some microscopic algae.
Planta 115: 207-212
8. CHOLLET R, WL OGREN 1975 Regulation of photorespiration in C, and C4 species. Bot Rev
41: 137-179
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Copyright © 1977 American Society of Plant Biologists. All rights reserved.
940
LLOYD, CANVIN, AND CULVER
9. CHU SP 1942 The influence of the mineral composition of the medium on the growth of
planktonic algae. J Ecol 30: 284-325
10. COLMAN B, KH CHENG, RK INGLE 1976 The relative activities of PEP carboxylase and
RuDP carboxylase in blue-green algae. Plant Sci Lett 6:123-127
11. COLMAN B, AG MILLER, B GRODZINSKI 1974 A study of the control of glycolate excretion
in Chlorella. Plant Physiol 53: 395-397
12. COOMBS J, GW BALDRY 1970 CO2 assimilation by chloroplasts illuminated on filter paper.
Nature 228: 1349-1350
13. COOMBS J, CP WHITnNGHAM 1966 The effect of high partial pressures of 02 on photosynthesis in Chlorella. I. The effect on end products of photosynthesis. Phytochemistry 5:
643-651
14. DALEY RJ, CBJ GRAY, SR BROWN 1973 A quantitative method for determining algal and
sedimentary chlorophyll derivatives. J Fish Res Board Can 30: 345-356
15. D'AousT AL, DT CANVIN 1972 The specific activity of "4CO2 evolved in COrfree air in the
light and darkness by sunflower leaves following periods of photosynthesis in "4CO2.
Photosynthetica 6: 150-157
16. FOCK H, DT CANVIN, BR GRANT 1971 Effects of oxygen and carbon dioxide on photosynthetic 02 evolution and CO2 uptake in sunflower and Chlorella. Photosynthetica 5: 389394
17. FOCK H, K EGLE 1966 Uber die "Lichtatmung" bei grunen Pflanzen. I. Die Wirkung von
Sauerstoff und Kohlendioxyd auf den CO2-gaswechsel wahrend der licht-und dunkel
phase. Beitr Biol Pflanzen 42: 213-239
18. FOCK H, H SCHAUB, W HILGENBERG 1968 Uber den Sauerstoff und Kohlendioxidgaswechsel von Chlorella und Conocephalum wahrend der Lichtphase. Z Pflanzenphysiol 60: 56-
63
19. GLIDEWELL SM, JA RAVEN 1975 Measurement of simultaneous oxygen evolution and
uptake in Hydrodictyon africanum. J Exp Bot 26: 479-489
20. HAN TW, JH ELEY 1973 Glycolate excretion by Anacystis nidulans: effect of HCO3concentration, oxygen concentration and light intensity. Plant Cell Physiol 14: 285-291
21. HUGHES EO, PR GORHAM, A ZEHNDER 1958 Toxicity of uni-algal culture of Microcystis
aeruginosa. Can J Microbiol 4: 225-236
22. IHLENFELDT MJA, J GlBSON 1975 CO2 fixation and its regulation in Anacystis nidulans
Plant Physiol. Vol. 59, 1977
(Synechococcus). Arch Microbiol 102: 13-21
23. IMAFUKu H, T KATOH 1976 Intracellular ATP level and light induced inhibition of respiration in a blue-green alga Anabaena variabilis. Plant Cell Physiol 17: 515-524
24. INGLE RK, B COLMAN 1976 The relationship between carbonic anhydrase activity and
glycolate excretion in the blue-green alga Coccochlorispeniocystis. Planta 128: 217-223
25. LEX M, SILVESTER WB, WDP STEWART 1972 Photorespiration and nitrogenase activity in
the blue-green alga, Anabaena cylindrica. Proc R Soc Lond B 180: 87-102
26. LUDWIG LJ, DT CANVIN 1971 An open gas-exchange system for the simultaneous measurement of the CO2 and 14CO2 fluxes from leaves. Can J Bot, 49: 1299-1319
27. LUDWIG LJ, DT CANVIN 1971 The rate of photorespiration during photosynthesis and the
relationship of the substrate of light respiration to the products of photosynthesis in
sunflower leaves. Plant Physiol 48: 712-719
28. MERRETT MJ, JM LORD 1973 Glycolate formation and metabolism by algae. New Phytol 72:
75 1-768
29. NELSON EB, NE TOLBERT 1969 The regulation of glycolate metabolism in Chlamydomonas
reinhardtii. Biochim Biophys Acta 184: 263-271
30. PRITCHARD GG, WJ GRIFFIN, CP WHITnINGHAM 1962 The effect of CO2 concentration,
light intensity and isonicotinyl hydrazide on the photosynthetic production of glycolic acid
by Chlorella. J Exp Bot 13: 176-184
31. RADMER RJ, B KOK 1976 Photoreduction of 02 primes and replaces CO2 assimilation. Plant
Physiol 58: 336-340
32. RIED A 1970 Energetic aspects of the interaction between photosynthesis and respiration. In
Prediction and Measurement of Photosynthetic Productivity. PUDOC, Wageningen pp
231-246
33. TOLBERT NE 1974 Photorespiration. In WDP Stewart, ed, Algal Physiology and Biochemistry. Blackwell, Oxford England pp 475-504
34. TURNER JS, EG BRITTAN 1962 Oxygen as a factor in photosynthesis. Biol Rev 37: 130-170
35. WHiTnINGHAM CP 1952 Rate of photosynthesis and concentration of carbon dioxide in
Chlorella. Nature 170: 1017-1018
36. ZELITCH I 1971 Photosynthesis and Photorespiration and Plant Productivity. Academic
Press, New York
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