Calvin Cycle in a Non-photosynthetic Alga

Oxygenic photosynthesis produces organic matter on land and in the sunlit ocean. It accomplishes this by fixing atmospheric carbon dioxide through the Calvin cycle using ATP and reducing power derived from the light-dependent electron transport and proton motive force. The resulting organic compounds serve as sustenance for non-photosynthetic organisms. The key Calvin cycle enzyme is Ribulose 1,5-bisphosphate Carboxylase/Oxygenase (RuBisCO). Curiously, some secondarily non-photosynthetic protists retain RuBisCO genes; however, the significance of this remains unclear. Here we show that a secondarily non-photosynthetic protist, Cryptomonas paramecium CCAP977/2A, is capable of autotrophic growth and carbon fixation and retains a complete set of genes for the Calvin cycle. We demonstrate that C. paramecium CCAP977/2A is cable of autotrophic growth even in the absence of organic matter. Stable carbon isotope labelling experiments using 13C- labelled inorganic carbon as a substrate showed 13C enrichment in the cell. Metabolomic analyses revealed that Ribulose 1,5-bisphosphate, the substrate of RuBisCO, and many other metabolites/products of the Calvin cycle were substantially labelled. Our results demonstrate the existence of inorganic carbon fixation ability in the non-photosynthetic protists that has thus far been ignored. The potential impact of eukaryotic non-photosynthetic primary production on global carbon flux deserves further attention.