Insights into carbon acquisition and photosynthesis in Karenia brevis under a range of CO2 concentrations

Abstract

Karenia brevis is a marine dinoflagellate commonly found in the Gulf of Mexico and important both ecologically and economically due to its production of the neurotoxin brevetoxin, which can cause respiratory illness in humans and widespread death of marine animals. K. brevis strains have previously shown to be sensitive to changes in CO2, both in terms of growth as well as toxin production. Our study aimed to understand this sensitivity by measuring underlying mechanisms, such as photosynthesis, carbon acquisition, and photophysiology. K. brevis (CCFWC-126) did not show a significant response in growth, cellular composition of carbon and nitrogen, nor in photosynthetic rates between pCO2 concentrations of 150, 400, or 780 µatm. However, a strong response in its acquisition of inorganic carbon was found. Half saturation values for CO2 increased from 1.5 to 3.3 µM, inorganic carbon preference switched from HCO3− to CO2 (14–56% CO2 usage), and external carbonic anhydrase activity was downregulated by 23% when comparing low and high pCO2. We conclude that K. brevis must employ an efficient and regulated CO2 concentrating mechanism (CCM) to maintain constant carbon fixation and growth across pCO2 levels. No statistically significant correlation between CO2 and brevetoxin content was found, yet a positive trend with enhanced pCO2 was detected. This study is the first explaining how this socioeconomically important species is able to efficiently supply inorganic carbon for photosynthesis, which can potentially prolong bloom situations. This study also highlights that elevated CO2 concentrations, as projected for a future ocean, can affect underlying physiological processes of K. brevis, some of which could lead to increases in cellular brevetoxin production and therefore increased impacts on coastal ecosystems and economies.