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

Abstract

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 μmol L-1) and then treated it with two CO2 conditions (2.8 and 12.6 μmol L-1) for 2 h. The lower CO2 reduced net photosynthetic rate at lower phosphate levels (< 4 μmol L-1) but did not affect it at higher phosphate levels (4 and 10 μmol L-1). In contrast, the lower CO2 induced a higher dark respiration rate at lower phosphate levels (0.05 and 0.25 μmol L-1) and did not affect it at higher phosphate levels (> 1 μmol L-1). The lower CO2 did not change relative electron transport rate (rETR) at lower phosphate levels (0.05 and 0.25 μmol L-1) and increased it at higher phosphate levels (> 1 μmol L-1). Photosynthetic CO2 affinity (1/K0.5) increased with phosphate levels. The lower CO2 did not affect photosynthetic CO2 affinity at 0.05 μmol 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 μmol 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 μmol 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 extracellular 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.