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First published online July 30, 2004; 10.1104/pp.104.041319 Plant Physiology 135:2106-2111 (2004) © 2004 American Society of Plant Biologists The Role of the C4 Pathway in Carbon Accumulation and Fixation in a Marine Diatom1Department of Environmental Sciences, Rutgers University, New Brunswick, New Jersey 08901 (J.R.R.); and Department of Geosciences, Princeton University, Princeton, New Jersey 08544 (A.J.M., F.M.M.M.)
The role of a C4 pathway in photosynthetic carbon fixation by marine diatoms is presently debated. Previous labeling studies have shown the transfer of photosynthetically fixed carbon through a C4 pathway and recent genomic data provide evidence for the existence of key enzymes involved in C4 metabolism. Nonetheless, the importance of the C4 pathway in photosynthesis has been questioned and this pathway is seen as redundant to the known CO2 concentrating mechanism of diatoms. Here we show that the inhibition of phosphoenolpyruvate carboxylase (PEPCase) by 3,3-dichloro-2-dihydroxyphosphinoylmethyl-2-propenoate resulted in a more than 90% decrease in whole cell photosynthesis in Thalassiosira weissflogii cells acclimated to low CO2 (10 µM), but had little effect on photosynthesis in the C3 marine Chlorophyte, Chlamydomonas sp. In 3,3-dichloro-2-dihydroxyphosphinoylmethyl-2-propenoate-treated T. weissflogii cells, elevated CO2 (150 µM) or low O2 (80–180 µM) restored photosynthesis to the control rate linking PEPCase inhibition with CO2 supply in this diatom. In C4 organic carbon-inorganic carbon competition experiments, the 12C-labeled C4 products of PEPCase, oxaloacetic acid and its reduced form malic acid suppressed the fixation of 14C-labeled inorganic carbon by 40% to 50%, but had no effect on O2 evolution in photosynthesizing diatoms. Oxaloacetic acid-dependent O2 evolution in T. weissflogii was twice as high in cells acclimated to 10 µM rather than 22 µM CO2, indicating that the use of C4 compounds for photosynthesis is regulated over the range of CO2 concentrations observed in marine surface waters. Short-term 14C uptake (silicone oil centrifugation) and CO2 release (membrane inlet mass spectrometry) experiments that employed a protein denaturing cell extraction solution containing the PEPCKase inhibitor mercaptopicolinic acid revealed that much of the carbon taken up by diatoms during photosynthesis is stored as organic carbon before being fixed in the Calvin cycle, as expected if the C4 pathway functions as a CO2 concentrating mechanism. Together these results demonstrate that the C4 pathway is important in carbon accumulation and photosynthetic carbon fixation in diatoms at low (atmospheric) CO2.
1 This work was supported by the NSF-EMSI program through the Center for Environmental Bioinorganic Chemistry (CEBIC) and by a Hatch/McIntyre-Stennis grant through the New Jersey Agricultural Experiment Station. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.041319. * Corresponding author; e-mail reinfelder{at}envsci.rutgers.edu; fax 732–932–8644. Received February 19, 2004; returned for revision April 27, 2004; accepted April 29, 2004. This article has been cited by other articles:
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