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Published on November 9, 2007; 10.1104/pp.107.110569

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Received October 9, 2007
Accepted November 6, 2007

Expression and inhibition of the carboxylating and decarboxylating enzymes in the photosynthetic C4 pathway of marine diatoms

Patrick J. McGinn * and Francois M. M. Morel

Department of Geosciences, Princeton University, Princeton, N.J., 08540, U.S.A

* Corresponding author; email: pmcginn{at}princeton.edu.

There is evidence that the CO2 concentrating mechanism (CCM) in the marine diatom Thalassiosira weissflogii operates as a type of single-cell C4 photosynthesis. In quantitative-PCR assays, we observed 2-4 fold upregulation of 2 phosphoenolpyruvate carboxylase (PEPCase) gene transcripts in Thalassiosira pseudonana cells adapted to low pCO2 but did not detect such regulation in Phaeodactylum tricornutum grown under similar conditions. Transcripts encoding phosphoenolpyruvate carboxykinase (PCKase) did not appear to be regulated by pCO2 in either diatom. In T. pseudonana and T. weissflogii net CO2 fixation was blocked by 3,3-dichloro-2-(dihydroxyphosphinoyl-methyl)-propenoate (DCDP, a specific inhibitor of PEPCase) but was restored by about 50% and 80%, respectively, by addition of mM concentrations of KHCO3. In T. pseudonana, T. weissflogii and P. tricornutum, rates of net O2 evolution were reduced by an average of 67%, 55% and 62%, respectively, in the presence of 20 µM quercetin, also an inhibitor of PEPCase. Quercetin promoted net CO2 leakage from inhibited cells to levels in excess of the equilibrium CO2 concentration, suggesting that a fraction of the HCO3- taken up is fated to leak back into the medium as CO2 when PEPCase activity is blocked. In parallel to these experiments, in vitro assays on crude extracts of T. pseudonana, demonstrated a mean inhibition of 65% of PEPCase activity by quercetin. In the presence of 5 mM 3-mercaptopicolinic acid (3-MPA), a classic inhibitor of PCKase, photosynthetic O2 evolution was reduced by 90% in T. pseudonana. In T. weissflogii and P. tricornutum, 5 mM 3-MPA totally inhibited net CO2 fixation and O2 evolution. Neither quercetin nor 3-MPA had a significant inhibitory effect on photosynthetic O2 evolution or CO2 uptake in the marine chlorophyte isolates Chlamydomonas sp. or Dunaliella tertiolecta. Our evidence supports the idea that C4-based CCMs are generally distributed in diatoms. This conclusion is discussed within the context of the evolutionary success of diatoms.




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