Aerobic preference in the marine protist Paradiplonema papillatum having anaerobic genomic potential

Background The diplonemid Paradiplonema papillatum is a marine planktonic protist with predicted complex and versatile metabolism. Investigation of carbohydrate metabolism and capacity for anaerobic life strategy revealed a disparity between its genomic and actual physiological preference. Despite possessing the genetic toolkit that should allow it to thrive in anoxic environment, P. papillatum primarily relies on aerobic metabolism, which it finely tunes in response to nutrient availability. Results Isocitrate dehydrogenase (IDH) of the tricarboxylic acid (TCA) cycle serves as a key regulatory switch. The NAD + - and NADP + -dependent IDH paralogues maintain the cycle’s plasticity, as this enzyme can support both the standard oxidative TCA cycle and its reductive branch, depending on metabolic requirements. The TCA cycle provides reduced cofactors, which branches into both canonical and non-canonical pathways when nutrients are abundant. This branched respiration is supported by ubiquinones UQ 8 and UQ 9 , whose biosynthetic pathway is a mosaic of a genes of different evolutionary origins. In addition to oxidative phosphorylation, P. papillatum can synthesize ATP in the propionate cycle and the acetate:succinate coenzyme A (CoA) transferase/succinyl-CoA synthetase cycle via substrate-level phosphorylation. Conclusions Our results highlight the complex regulation of mitochondrial metabolism in the diverse and abundant diplonemids and provide insight into the physiological strategies of marine planktonic microeukaryotes.