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Evidence for the functioning of photosynthetic CO2-concentrating mechanisms in lichens containing green algal and cyanobacterial photobionts

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Abstract

The photosynthetic properties of a range of lichens containing both green algal (11 species) and cyanobacterial (6 species) photobionts were examined with the aim of determining if there was clear evidence for the operation of a CO2-concentrating mechanism (CCM) within the photobionts. Using a CO2-gas-exchange system, which allowed resolution of fast transients, evidence was obtained for the existence of an inorganic carbon pool which accumulated in the light and was released in the dark. The pool was large (500–1000 nmol · mg Chl) in cyanobacterial lichens and about tenfold smaller in green algal lichens. In Hypogymnia physodes (L.) Nyl., which contains the green alga Trebouxia jamesii, a small inorganic carbon pool was rapidly formed in the light. Carbon dioxide was released from this pool into the gas phase upon darkening within about 20 s when photosynthesis was inhibited by the carbon-reduction-cycle inhibitor glycolaldehyde. In the absence of this inhibitor, release appeared to be obscured by carboxylation of ribulose bisphosphate. The kinetics of CO2 uptake and release were monophasic. The operation of an active CCM could be distinguished from passive accumulation and release accompanying the reversible light-dependent alkalization of the stroma by the presence of saturation characteristics with respect to external CO2. In Peltigera canina (L.) Willd., which contains the cyanobacterium Nostoc sp., a larger CO2 pool was taken up over a longer period in the light and the release of this pool in the dark was slow, lasting 3–5 min. This pool also accumulated in the presence of glycolaldehyde, and under these conditions the CO2 release was biphasic. In both species, photosynthesis at low CO2 was inhibited by the carbonic-anhydrase inhibitor ethoxyzolamide (EZ). Inhibition could be reversed fully or to a considerable extent by high CO2. In Peltigera, EZ decreased both the accumulation of the CO2 pool by the CCM and the rate of photosynthesis. Free-living cultures of Nostoc sp. showed a similar effect of EZ on photosynthesis, although it was more dramatic than that seen with the lichen thalli. In contrast, in Hypogymnia, EZ actually increased the size of the CO2 pool, although it inhibited photosynthesis. This effect was also seen when glycolaldehyde was present together with EZ. Surprisingly, EZ did not alter the kinetics of either CO2 uptake or release. Taken together, the evidence indicates the operation in cyanobacterial lichens of a CCM which is capable of considerable elevation of internal CO2 and is similar to that reported for free-living cyanobacteria. The CCM of green algal lichens accumulates much less CO2 and is probably less effective than that which operates in cyanobacterial lichens.

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Abbreviations

AZ:

acetazolamide or N-[5-sulfamoyl-1,3,4-thiadiazole-2-yl]acetamide

CA:

carbonic anhydrase

DIC:

dissolved inorganic carbon (CO2 + HCO sup−inf3 + CO sup2−inf3 )

CCM:

CO2-concentrating mechanism

Hepps:

N-[2-hydroxyethyl]piperazine-N′;-[3-propanesulfonic acid]

EZ:

ethoxyzolamide or 6-ethoxy-2-benzothiazole-sulfonamide

Rubisco:

ribulose bisphosphate carboxylase-oxygenase

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Author notes

  1. Murray R. Badger

    Present address: Plant Environmental Biology Group, Research School of Biological Sciences, Australian National University, GPO Box 475, 2601, Canberra, ACT, Australia

Authors and Affiliations

  1. Julius-von-Sachs-Institut für Biowissenschaften der Universität Würzburg, Mittlerer Dallenbergweg 64, D-97082, Würzburg, Germany

    Murray R. Badger, Hardy Pfanz, Burkhard Büdel, Ulrich Heber & Otto L. Lange

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  1. Murray R. Badger
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  2. Hardy Pfanz
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  3. Burkhard Büdel
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  4. Ulrich Heber
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  5. Otto L. Lange
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Additional information

This research was supported by the Deutsche Forschungsgemeinschaft (DFG) as a project of the “Sonderforschungsbereich 251 der Universität Würzburg”. M.R.B. gratefully acknowledges the support of a Fellowship from the DFG-Graduiertenkolleg der Universität Würzburg and a travel grant from the Australian National University under its Overseas Study Program. We would like to acknowledge the excellent technical assistance of Ms. B. Bruch and Ms. D. Faltenbacher-Werner, the help of Ms. S. Neimanis in setting up the gas-exchange system and Dr. T.G.A. Green (Department of Biological Sciences, the University of Waikato, Hamilton, New Zealand) for supplying the New Zealand lichens and helpful comments on the manuscript. We would also like to thank Dr. Kristin Palmqvist who made her manuscript available to us prior to submission.

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Badger, M.R., Pfanz, H., Büdel, B. et al. Evidence for the functioning of photosynthetic CO2-concentrating mechanisms in lichens containing green algal and cyanobacterial photobionts. Planta 191, 57–70 (1993). https://doi.org/10.1007/BF00240896

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