Sensitivity of Antarctic phytoplankton species to ocean acidification: Growth, carbon acquisition, and species interaction

Despite the fact that ocean acidification is considered to be especially pronounced in the Southern Ocean, little is known about CO2-dependent physiological processes and the interactions of Antarctic phytoplankton key species. We therefore studied the effects of CO2 partial pressure (PCO2) (16.2, 39.5, and 101.3 Pa) on growth and photosynthetic carbon acquisition in the bloom-forming species Chaetoceros debilis, Pseudo-nitzschia subcurvata, Fragilariopsis kerguelensis, and Phaeocystis antarctica. Using membrane-inlet mass spectrometry, photosynthetic O2 evolution and inorganic carbon (Ci) fluxes were determined as a function of CO2 concentration. Only the growth of C. debilis was enhanced under high PCO2. Analysis of the carbon concentrating mechanism (CCM) revealed the operation of very efficient CCMs (i.e., high Ci affinities) in all species, but there were species-specific differences in CO2-dependent regulation of individual CCM components (i.e., CO2 and HCO { 3 uptake kinetics, carbonic anhydrase activities). Gross CO2 uptake rates appear to increase with the cell surface area to volume ratios. Species competition experiments with C. debilis and P. subcurvata under different PCO2 levels confirmed the CO2-stimulated growth of C. debilis observed in monospecific incubations, also in the presence of P. subcurvata. Independent of PCO2, high initial cell abundances of P. subcurvata led to reduced growth rates of C. debilis. For a better understanding of future changes in phytoplankton communities, CO2-sensitive physiological processes need to be identified, but also species interactions must be taken into account because their interplay determines the success of a species. The Southern Ocean (SO) is a high-nutrient lowchlorophyll region. Compared with most other regions of the World oceans, the concentrations of nitrate and phosphate are high. The reason for this phenomenon is that the biological production is limited by the trace metal iron, which is essential for photosynthesis (Martin et al. 1990). Most of the primary production in the SO is achieved by sporadic bloom events, which mainly occur along the continental margins and only extend offshore when iron and other nutrient concentrations are high due to upwelling. These blooms are usually dominated by medium-sized diatoms and the flagellate Phaeocystis antarctica (Smetacek et al. 2004). Light is also a major factor controlling phytoplankton growth and productivity in the SO due to the occurrence of strong and frequent winds, causing pronounced deep mixing and therefore low mean and highly varying light levels (Tilzer et al. 1985). Deeply mixed layers were associated with a predominant occurrence of P. antarctica, while diatoms such Fragilariopsis cylindrus seem to favor shallow mixed layers (Kropuenske et al. 2010). Varying CO2 concentrations were found to also influence SO phytoplankton assemblages and growth (Tortell et al. 2008b; Feng et al. 2010). During winter time, the presence of sea ice prevents gas exchange between surface water and the atmosphere, causing CO2 partial pressure (PCO2) to often exceed atmospheric levels after ice-out in spring. With increasing light availability, phytoplankton growth causes CO2 to decrease. Intense photosynthetic activity can result in PCO2 values , 20 Pa toward the end of bloom periods (Arrigo et al. 1999; Cassar et al. 2004). Next to these productivity-related changes in seawater carbonate chemistry, the rise in atmospheric CO2 levels due to human-induced activities such as fossil fuel burning can have a pronounced effect on phytoplankton growth. At present-day, atmospheric CO2 concentrations are ,39 Pa, leading to a seawater pH of , 8.1. By the end of this century, the ongoing CO2 emissions are expected to cause atmospheric CO2 to rise up to 75 Pa and to lower seawater pH to , 7.9 (‘ocean acidification’; Houghton et al. 2001). As a greenhouse gas, the rise in atmospheric CO2 will also cause global temperatures to increase, an effect being particularly pronounced in polar regions (Sarmiento et al. 2004). Both the disproportional strong warming and the freshwater input from sea ice melting contribute to enhanced surface stratification in the SO, which in turn may alter the mixing and light regime experienced by phytoplankton. All these environmental changes (CO2, temperature, light) will affect SO phytoplankton in many, and most likely different, ways. In order to understand how SO phytoplankton will respond to climate change, knowledge on the physiology and ecology of Antarctic key phytoplankton species is required. The mode of carbon acquisition determines, to a large extent, how phytoplankton respond to changes in CO2. The CO2 sensitivity in photosynthesis is mainly the result of the poor affinity of the enzyme Ribulose-1,5bisphosphate carboxylase/oxygenase (RubisCO) for its substrate CO2. To overcome potential carbon limitation under present-day CO2 concentrations, marine phytoplankton operate carbon concentrating mechanisms (CCMs) that enrich CO2 at the catalytic site of RubisCO and thus enhance their photosynthetic productivity (Giordano et al. 2005). Antarctic natural phytoplankton communities were found to operate constitutive CCMs over a range of various * Corresponding author: [email protected] Limnol. Oceanogr., 58(3), 2013, 997–1007 E 2013, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2013.58.3.0997