Uptake and metabolism of glucose in the Nostoc–Gunnera symbiosis

Abstract

Summary The transition of Nostoc colonies from free‐living to symbiotic conditions, in the Nostoc–Gunnera association, involves increased heterocyst frequency and a reliance on carbon imported from the host for metabolic processes, including N2 fixation. Here the uptake of a glucose analogue, 3‐[14C]‐O‐methyl‐glucose (14C‐OMG), in freshly isolated symbiotic and free‐living Nostoc cells was characterized. In situ isotope enrichment coupled with GC–MS was used to elucidate the primary pathway(s) of 1‐[13C]‐glucose metabolism in the Nostoc–Gunnera symbiosis. The characteristics of 14C‐OMG uptake by symbiotic clusters suggested a respiratory driven process mediated by a hexose transporter. However, uptake by various Nostoc isolates decreased with increasing heterocyst frequency and was specifically associated with vegetative cells. In isolated and symbiotically intact Nostoc cells, 1‐[13C]‐glucose was imported and converted to various intermediates of the incomplete citric acid cycle, glycolysis and N2‐assimilating pathways. Labelling profiles indicated that C metabolism was altered in infected, but not in uninfected, rhizome tissue. Although it has been proposed that cyanobacteria such as Nostoc metabolise glucose using enzymes of the oxidative pentose phosphate cycle, our results suggest that glucose is also metabolised via glycolysis as well as the incomplete citric acid cycle in symbiotic cells.