Planta

Planta (1982) 155:95-96

9 Springer-Verlag 1982

The effect of oxygen concentration on photosynthetic biomass production by algae Michael J. Merrett and Terence L. Armitage Postgraduate School of Studies in Biological Sciences, University of Bradford, Bradford, Yorkshire BD7 1DP, U.K.

Abstract. The effect of decreased oxygen concentration on photosynthetic biomass production was determined for Euglena gracilis Klebs strain z and Chlamydomonas reinhardtii Dangeard. At a constant carbon dioxide concentration of 0.03% (v/v), decreasing the oxygen concentration from 21% to 2% (v/v) gave a two-fold increase in dry-weight yield for E. gracilis; a result consistent with the operation of a functional glycollate pathway in this alga. A similar effect of oxygen concentration on dry-weight yield was not observed with C. reinhardtii. Key words: Biomass production - Chlamydomonas - Euglena - Oxygen (effect on photosynthesis).

Introduction The presence of a functional glycollate pathway is well established in cells of E. gracilis grown on air (Codd and Merrett 1971a, b). Labelling studies with 14COz showed carbon flow through the pathway (Codd and Merrett 1971 b) and the activity of glycollate pathway enzymes is adequate to account for observed rates of glycollate metabolism (Collins and Merrett 1975). As in higher plants glycollate formation in Euglena results from the oxidation of ribulose1,5-bisphosphate to 2-phosphoglycollate and 3phosphoglycerate catalysed by the oxygenase activity of ribulose-l,5-bisphosphate carboxylase (McFadden et al. 1975). Because the same catalytic site is involved in the reaction with O2 as with CO2, each substrate is a competitive inhibitor of reaction by the other. By decreasing the O2 concentration the rate of photosynthesis is increased in C3 plants and dry-matter production is also substantially increased under low 02 (Quebedeaux and H a r d y 1973; Parkinson etal. 1974). Although eukaryotic microalgae are C3 plants

in that primary C O 2 fixation is catalysed by ribulose1,5-bisphosphate carboxylase, when grown on air no effect of 02 on CO2 fixation and a low CO2 compensation point have been reported for some of these algae (Lloyd et al. 1977). In view of this it was of interest to determine whether 02 concentration had an effect on algal photosynthetic dry matter production.

Materials and methods Chlamydomonas reinhardtii Dangeard No. 90 was grown as described previously (Codd et al. 1969) at pH 6.8 and a light intensity of 380 lm. Euglena gracilis Klebs strain z Pringsheim was grown as described previously (Davis and Merrett 1975) at pH 6.7 and a light intensity of 250 Ira. Cultures were grown at 25~ with stirring, in 2-1 Pyrex vessels and gassed at a flow rate of 61 h-1 either with air, 21% O2, or 2% Oz, 97.97% Nz, 0.03% CO2 (by vol.) provided by a Signal Gas Blender, model 853 (Signal Instrument Co. Ltd., Camberley U.K.). Dry weights were determined by removing aliquots from cuitures into weighed centrifuge tubes, spinning down the cells, washing once, centrifuging down again, then drying to constant weight at 105~ C. Cell numbers were determined by haemocytometer or Coulter counter (Coulter Electronics Ltd., Luton, U.K.).

Results and discussion The simultaneous determination of ribulose-l,5-bisphosphate carboxylase and oxygenase activities has shown the ratio of these two activities to be a linear function of the ratio of the CO2 and 02 concentrations (Jordan and Ogren 1981) so that any variation in this ratio in the chloroplast will affect the production of 3-phosphoglycerate relative to 2-phosphoglycollate. The effects of diffusion gradients from and to the external medium and photosynthetic 02 evolution on the CO2 and O2 concentrations at the site of ribulose-l,5-bisphosphate carboxylase/oxygenase have been analysed by Raven (1980). In the present experiments cells were subjected to a decrease in O2

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c o n c e n t r a t i o n f r o m 21% to 2 % in the gas phase when g r o w i n g p h o t o t r o p h i c a l l y u n d e r n e a r - o p t i m u m conditions a n d the effect on d r y - w e i g h t yield d e t e r m i n e d before o t h e r c o n d i t i o n s , such as a decrease in light intensity resulting f r o m s h a d i n g in the cultures, c o u l d influence the results. Euglena cultures subjected to decreased 0 2 c o n c e n t r a t i o n gave a significant increase in d r y - w e i g h t yield c o m p a r e d with those in air (Fig. 1), b u t with Chlamydomonas this effect was n o t o b s e r v e d (Fig. 1). T h e o p e r a t i o n of a " C O 2 - c o n c e n t r a t i n g m e c h a n i s m " has been d e m o n s t r a t e d in lowC O 2 - g r o w n cells o f Chlamydomonas ( B a d g e r et al. 1980) a n d o t h e r m i c r o a l g a e (Raven a n d Glidewell 1978; B e a r d a l l a n d R a v e n 1981) a n d this w o u l d increase the C O 2 : O 2 ratio at the site o f r i b u l o s e - l , 5 b i s p h o s p h a t e c a r b o x y l a s e / o x y g e n a s e activity. This increase in the C O 2 : O 2 ratio represses p h o s p h o g l y c o late f o r m a t i o n so that decreased 0 2 c o n c e n t r a t i o n has no effect on p h o t o s y n t h e t i c d r y - w e i g h t yield as o b s e r v e d with Chlamydomonas (Fig. 1), whereas with Euglena a similar " C O 2 - c o n c e n t r a t i n g m e c h a n i s m " m a y n o t be operative.

References

Badger, M.R., Kaplan, A., Berry, J.A. (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: Evidence for a carbon dioxide concentrating mechanism. Plant Physiol. 66, 407~, 13

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Fig. 1. The effect of oxygen concentration on photosynthetic biomass yield of Euglena and Chlamydomonas. e - - o , cell number 2% 02 (v/v); A - - A , cell number 2I% 02 (v/v); [], dryweight yield 2% Oz (v/v); [], dryweight yield 21%/2 (v/v): Vertical bars show variation from four separate experiments

96 Time (h)

Beardall, J., Raven, J.A. (1981) Transport of inorganic carbon and the "COg concentrating mechanism" in Chloretlaemersonii (Chlorophyceae). J. Phycol. 17, 134-141 Codd, G.A., Merrett, M.J. (1971a) Photosynthetic products of division-synchronized cultures of Euglena. Plant Physiol. 47, 635-639 Codd, G.A., Merrett, M.J. (1971b) The regulation of glycolate metabolism in division-synchronized cultures of Euglena. Plant Physiol. 47, 640 643 Codd, G.A., Lord, J.M., Merrett, M.J. (1969) The glycolate oxidizing enzyme of algae. FEBS. Lett. 5, 341-342 Collins, N., Merrett, M.J. (1975) The localization of glycollatepathway enzymes in Euglena. Biochem. J. 148, 321-328 Davis, B., Merrett, M.J. (1975) The glycolate pathway and photosynthetic competence in Euglena. Plant Physiol. 55, 30 34 Jordan, D.B., Ogren, W.L. (1981) A sensitive assay procedure for simultaneous determination of ribulose-l,5-bisphosphate carboxylase and oxygenase activities. Plant Physiol. 67, 237 245 Lloyd, N.D.H., Canvin, D.T., Culver, D.A. (1977) Photosynthesis and photorespiration in algae. Plant Physiol. 59, 936-940 McFadden, B.A., Lord, J.M., Rowe, A., Dilks, S. (1975) Composition, quaternary structure and catalytic properties of D-ribulose-l,5-bisphosphate carboxylase from Euglena gracilis. Eur. J. Biochem. 54, 195 206 Parkinson, K., Penman, H.L., Tregunna, E.B. (1974) Growth of plants in different oxygen concentrations. J. Exp. Bot. 25, 132 144 Quebedeaux, B., Hardy, R.W.F. (1973) Oxygen as a new factor controlling reproductive growth. Nature (London) 243, 477479 Raven, J.A. (1980) Nutrient transport in microalgae. Adv. Microb. Physiol. 21, 47-226 Raven, J.A., Glidewell, S.M. (1978) C4 characteristics of photosynthesis in the C3 alga Hydrodictyon @icanum. Plant Cell Environ. 1, 185 197 Received 19 January; accepted 17 February 1982

The effect of oxygen concentration on photosynthetic biomass production by algae.

The effect of decreased oxygen concentration on photosynthetic biomass production was determined for Euglena gracilis Klebs strain z and Chlamydomonas...
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