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

Abstract

Despite the fact that ocean acidification is considered to be especially pronounced in the Southern Ocean, little is known about CO 2 -dependent physiological processes and the interactions of Antarctic phytoplankton key species. We therefore studied the effects of CO 2 partial pressure (P CO 2 ) (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 O 2 evolution and inorganic carbon (C i ) fluxes were determined as a function of CO 2 concentration. Only the growth of C. debilis was enhanced under high P CO 2 . Analysis of the carbon concentrating mechanism (CCM) revealed the operation of very efficient CCMs (i.e., high C i affinities) in all species, but there were species-specific differences in CO 2 -dependent regulation of individual CCM components (i.e., CO 2 and HCO { 3 uptake kinetics, carbonic anhydrase activities). Gross CO 2 uptake rates appear to increase with the cell surface area to volume ratios. Species competition experiments with C. debilis and P. subcurvata under different P CO 2 levels confirmed the CO 2 -stimulated growth of C. debilis observed in monospecific incubations, also in the presence of P. subcurvata. Independent of P CO 2 , 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, CO 2 -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 CO 2 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 betw...

Resistance of Arctic phytoplankton to ocean acidification and enhanced irradiance

“…Our results also agree well with previous laboratory experiments, which have shown that Antarctic Chaetoceros isolates show little to no stimulation by increasing pCO 2 levels (Boelen et al 2011;Trimborn et al 2013;Hoppe et al 2015). Nonetheless, this genus dominated OA treatments in several experiments with natural assemblages from the Southern Ocean, suggesting it to be a 'potential winner of OA' (Tortell et al 2008;Feng et al 2010;Boelen et al 2011;Trimborn et al 2013).…”

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

“…Acclimation to increased CO 2 has been reported in a number of studies, resulting in shifts in carbon and energy utilisation (Sobrino et al, 2008;Hopkinson et al, 2010;Hennon et al, 2014;Trimborn et al, 2014;Zheng et al, 2015). Numerous photophysiological investigations on individual phytoplankton species also report species-specific tolerances to increased CO 2 (Gao et al, 2012a;Gao and Campbell, 2014;Trimborn et al, 2013Trimborn et al, , 2014, and a general trend toward smaller-celled communities with increased CO 2 has been reported in ocean acidification studies globally . Changes in community structure were observed with increasing CO 2 , with taxon-specific thresholds of CO 2 tolerance (Hancock et al, 2017).…”

“…Increased CO 2 enhanced rates of primary productivity (Wu et al, 2010;Trimborn et al, 2013) and growth (Sobrino et al, 2008;Tew et al, 2014;Baragi et al, 2015;Chen et al, 2015;King et al, 2015) in some diatom species, while others were unaffected (Chen and Durbin, 1994;Sobrino et al, 2008;Berge et al, 2010;Trimborn et al, 2013;Chen et al, 2015;Hoppe et al, 2015;King et al, 2015;Bi et al, 2017). In contrast, CO 2 -related declines in primary productivity and growth rate have also been observed (Barcelos e Ramos et al, 2014;Hoppe et al, 2015;King et al, 2015;Shi et al, 2017), suggesting that responses to ocean acidification are largely species specific.…”

Southern Ocean phytoplankton physiology in a changing climate

“…However, growth and/or carbon fixation of other diatoms (C. brevis, C. debilis, Rhizosolenia cf. alata, P. subcurvata and P. alata) and P. antarctica remained unaffected by lowered pH (Riebesell et al, 1991;Boelen et al, 2007;Hoogstraten et al, 2012;Trimborn et al, 2013;Hoppe et al, 2015) suggesting that overall, the SO phytoplankton species investigated do not seem to benefit from lowered pH levels.…”

“…Natural phytoplankton communities of the SO (Weddell Sea, Drake Passage, Western Antarctic Peninsula, Amundsen and Ross Sea) were found to actively take up CO 2 and HCO 3 − (Cassar et al, 2004;Tortell et al, 2008aTortell et al, , 2008bTortell et al, , 2010Neven et al, 2011;Tortell et al, 2013;Kranz et al, 2015;Trimborn et al, 2015), thus indicating the presence of a CCM. Also, laboratory studies have demonstrated the operation of CCMs in various SO diatoms (Chaetoceros debilis, Fragilariopsis kerguelensis, F. cylindrus, Nitzschia frigida, Pseudo-nitzschia subcurvata) and a prymnesiophyte (Phaeocystis antarctica), although important differences between species were seen in the ratios of HCO 3 − and CO 2 uptake and external CA activity (Mitchell and Beardall, 1996;Trimborn et al, 2013;Kranz et al, 2015;Young et al, 2015).…”