Surviving the long fast: biochemical and photosynthetic acclimation of Synechocystis sp. CCNM 2501 to chronic nitrogen and phosphorus starvation

Microalgae accumulate carotenoids and lipids under nutrient limitation, yet how this metabolic coordination unfolds during prolonged starvation and how it differs between nitrogen and phosphorus deprivation remains poorly resolved in bloom-forming cyanobacteria. We characterized the biochemical, pigment, and photophysiological responses of Synechocystis sp. CCNM 2501 across 30 days of nitrogen (N−) and phosphorus (P−) starvation at ecologically realistic pond irradiance, and provide the first peer-reviewed molecular identification of the strain. Nitrogen starvation drove progressive chlorosis: total carotenoids declined significantly by day 9 (4.69 mg g−1 DCW) before recovering to a level statistically indistinguishable from control by day 15 (6.25 mg g−1), then collapsing by 86% at day 30 (0.86 mg g−1); maximum photosystem II quantum yield (Fv/Fm) declined from 0.43 to 0.23 and protein fell from 65% to 28.96% DCW between control and N−30d, while lipids transiently peaked at 29.26% DCW at N−15d. Phosphorus starvation induced the opposite carotenogenic response. Total carotenoids rose to a significant maximum at day 15 (11.51 mg g−1 DCW), driven by an early photoprotective phase (day 9: zeaxanthin +80% to 1.40 mg g−1; echinenone +122% to 1.78 mg g−1) followed by structural membrane remodeling (day 15: myxoxanthophyll +184% to 6.16 mg g−1), before collapsing by 80% to 2.32 mg g−1 at day 30, while protein fell from 65% to 44.89% DCW by day 30. Fv/Fm declined progressively and monotonically under nitrogen starvation (0.43 to 0.23), whereas phosphorus starvation produced a more modest, non-monotonic trajectory (0.43 to 0.26, with an intervening dip to 0.28 at day 9); by day 30 the two regimes converged toward similarly depressed values, with phosphorus starvation only marginally better preserved. Both regimes showed a turning point near day 15, though their character differed: phosphorus-starved carotenoids peaked significantly above control, while nitrogen-starved carotenoids recovered only to control levels before collapsing. These nutrient-specific trajectories show that phosphorus limitation, unlike nitrogen limitation, redirects metabolism toward photoprotective and structural carotenoids, providing a physiological basis for the extended persistence of blooms observed under phosphorus depletion in eutrophic freshwater ponds a hypothesis that will require field validation.