Regulation of inorganic carbon acquisition in a red tide alga (Skeletonema costatum): the importance of phosphorus availability

Skeletonema costatum is a common bloom-forming diatom and encounters eutrophication and severe carbon dioxide (CO2) limitation during red tides. However, little is known regarding the role of phosphorus (P) in modulating inorganic carbon acquisition in S. costatum, particularly under CO2 limitation conditions. We cultured S. costatum under five phosphate levels (0.05, 0.25, 1, 4, 10 mu mol L-1) and then treated it with two CO2 conditions (2.8 and 12.6 mu mol L-1) for 2 h. The lower CO2 reduced net photosynthetic rate at lower phosphate levels (< 4 mu mol L-1) but did not affect it at higher phosphate levels (4 and 10 mu mol L-1). In contrast, the lower CO2 induced a higher dark respiration rate at lower phosphate levels (0.05 and 0.25 mu mol L-1) and did not affect it at higher phosphate levels (> 1 mu mol L-1). The lower CO2 did not change relative electron transport rate (rETR) at lower phosphate levels (0.05 and 0.25 mu mol L-1) and increased it at higher phosphate levels (> 1 mu mol L-1). Photosynthetic CO2 affinity (1/K-0.5) increased with phosphate levels. The lower CO2 did not affect photosynthetic CO2 affinity at 0.05 mu mol L-1 phosphate but enhanced it at the other phosphate levels. Activity of extracellular carbonic anhydrase was dramatically induced by the lower CO2 in phosphate-replete conditions (> 0.25 mu mol L-1) and the same pattern also occurred for redox activity of the plasma membrane. Direct bicarbonate (HCO3-) use was induced when phosphate concentration was more than 1 mu mol L-1. These findings indicate P enrichment could enhance inorganic carbon acquisition and thus maintain the photosynthesis rate in S. costatum grown under CO2-limiting conditions via increasing activity of ex-tracellular carbonic anhydrase and facilitating direct HCO3- use. This study sheds light on how bloom-forming algae cope with carbon limitation during the development of red tides.