Antarctic phytoplankton down-regulate their carbon-concentrating mechanisms under high CO2 with no change in growth rates

Abstract

High-latitude oceans, in particular the coastal Western Antarctic Peninsula (WAP) region of the Southern Ocean, are experiencing a rapidly changing environment due to rising surface ocean temperatures and CO 2 concentrations. However, the direct effect of increasing CO 2 on polar ocean primary production is unclear, with a number of experiments showing conflicting results. It has been hypothesized that increased CO 2 may cause a reduction of the energy-intensive carbon concentrating mechanism (CCM) in phytoplankton, and these energy savings may lead to increased productivity. To test this hypothesis, we incubated natural phytoplankton communities in the WAP under high (800 ppm), current (400 ppm) and low (100 ppm) CO 2 for 2 to 3 wk during the austral spring-summer of 2012/2013. In 2 incubations with diatom-dominated phytoplankton assemblages, high CO 2 led to a clear down-regulation of CCM activity, as evidenced by an increase in half-saturation constants for CO 2 , a decrease in external carbonic anhydrase activity and a higher biological fractionation of stable carbon isotopes. In a third incubation, there was no observable regulation of the CCM, possibly because HCO 3 − served as the major inorganic carbon source in all treatments for this phytoplankton assemblage. We did not observe a significant effect of CO 2 on growth rates or community composition in the diatom-dominated communities. The lack of a measureable effect on growth despite CCM down-regulation is likely explained by a very small energetic requirement to concentrate CO 2 and saturate Rubisco at low temperatures.

Ocean acidification of a coastal Antarctic marine microbial community reveals a critical threshold for CO<sub>2</sub> tolerance in phytoplankton productivity

“…Tolerance of CO 2 levels up to ∼ 1000 µatm has often been observed in natural phytoplankton communities in regions exposed to fluctuating CO 2 levels. In these communities, increasing CO 2 often had no effect on primary productivity (Tortell et al, 2000;Tortell and Morel, 2002;Tortell et al, 2008b;Hopkinson et al, 2010;Tanaka et al, 2013;Sommer et al, 2015;Young et al, 2015;Spilling et al, 2016) or growth (Tortell et al, 2008b;Schulz et al, 2013), although an increase in primary production has been observed in some instances (Riebesell, 2004;Tortell et al, 2008b;Egge et al, 2009;Tortell et al, 2010;Hoppe et al, 2013;Holding et al, 2015). These differing responses may be due to differences in community composition, nutrient supply, or ecological adaptations of the phytoplankton community in the region studied.…”

“…This process requires additional cellular energy (Raven, 1991) and numerous studies have suggested that the energy savings from down-regulation of CCMs in phytoplankton could explain increases in rates of primary productivity at elevated CO 2 levels (e.g. Cassar et al, 2004;Tortell et al, 2008bTortell et al, , 2010Trimborn et al, 2013;Young et al, 2015). In Antarctic phytoplankton communities, Young et al (2015) showed that the energetic costs of CCMs are low and any down-regulation at increased CO 2 would provide little benefit.…”

“…Cassar et al, 2004;Tortell et al, 2008bTortell et al, , 2010Trimborn et al, 2013;Young et al, 2015). In Antarctic phytoplankton communities, Young et al (2015) showed that the energetic costs of CCMs are low and any down-regulation at increased CO 2 would provide little benefit. We found that the CCM component carbonic anhydrase (CA) was utilised by the phytoplankton community at our control CO 2 level (343 µatm) and was down-regulated at high CO 2 (1641 µatm; Fig.…”

“…Tolerance to CO 2 levels up to ∼ 800 µatm have been reported for natural coastal communities in the West Antarctic Peninsula and Prydz Bay, East Antarctica (Young et al, 2015;Davidson et al, 2016). Although in Prydz Bay, when CO 2 levels exceeded 780 µatm, primary productivity declined and community composition shifted toward smaller picoeukaryotes Thomson et al, 2016;Westwood et al, 2018).…”

The CO2 switch in diatoms

“…Cells regulate their CCM to maintain an intracellular concentration of CO 2 that saturates Rubisco by ~80% 8,9 . Correspondingly, downregulation of the CCM in response to high CO 2 should have little effect on the intracellular CO 2 to O 2 ratio, resulting in no change in the rate of photorespiration.…”