LAUSR

Phaeocystis antarctica is an integral player of the phytoplankton community of the Southern Ocean (SO), the world’s largest high-nutrient low-chlorophyll region, and faces chronic iron (Fe) limitation. As the SO is responsible for 40% of anthropogenic CO2 uptake, P. antarctica must also deal with ocean acidification (OA). However, mechanistic studies investigating the effects of Fe limitation and OA on trace metal (TM) stoichiometry, transcriptomic, and photophysiological responses of this species, as well as on the Fe chemistry, are lacking. This study reveals that P. antarctica responded strongly to Fe limitation by reducing its growth rate and particulate organic carbon (POC) production. Cellular concentrations of all TMs, not just Fe, were greatly reduced, suggesting that Fe limitation may drive cells into secondary limitation by another TM. P. antarctica was able to adjust its photophysiology in response to Fe limitation, resulting in similar absolute electron transport rates across PSII. Even though OA-stimulated growth in Fe-limited and -replete treatments, the slight reduction in cellular POC resulted in no net effect on POC production. In addition, relatively few genes were differentially expressed due to OA. Finally, this study demonstrates that, under our culture conditions, OA did not affect inorganic Fe or humic-acid-like substances in seawater but triggered the production of humic-acid-like substances by P. antarctica. This species is well adapted to OA under all Fe conditions, giving it a competitive advantage over more sensitive species in a future ocean. In 30–50% of the world’s oceans phytoplankton, biomass is low, even though concentrations of nitrate and phosphate are plentiful (de Baar et al. 2005). Rather than macronutrients, in these high-nutrient low-chlorophyll (HNLC) regions, it is the scarcity of certain trace metals (TMs), such as iron (Fe), which governs primary production and/or plankton species composition (Bertrand et al. 2007; de Baar et al. 2005; Koch et al. 2011; Martin and Fitzwater 1988). Fe is required for vital cellular processes such as carbon and nitrogen fixation, nitrate and nitrite reduction, and chlorophyll synthesis. It is also an integral part of the electron transport chain of respiration and photosynthesis (Raven et al. 1999; Behrenfeld and Milligan 2013; Twining and Baines 2013). The majority of metaloproteins, however, have yet to be discovered (Cvetkovic et al. 2010; Lelandais et al. 2016). The Southern Ocean (SO) is the world’s largest HNLC region, responsible for roughly 40% of all oceanic uptake of anthropogenic carbon (Landschutzer et al. 2015; Sabine et al. 2004) and an area where Fe limitation of phytoplankton has been reported (Martin et al. 1990; de Baar et al. 2005; Boyd and Ellwood 2010). It is also an important region, which contributes disproportionally to upwelling of deep water and formation of intermediate and bottom waters and links the Pacific, Indian, and Atlantic Oceans. The SO is thus of global importance in climate regulation, biodiversity, and biogeochemical cycles (Buesseler 1998; Lumpkin and Speer 2007). Atmospheric CO2 concentrations have risen sharply since the beginning of the industrial revolution and, due to anthropogenic activity, partial pressure of CO2 (pCO2) in seawater is said to increase from present day ~ 400 to 750 μatm by the end of this century (RCP 6.0; IPCC 2014). This will be accompanied by an increase in hydrogen ions (drop in pH) by almost 100% over present-day concentrations (Wolf-Gladrow et al. 1999), a phenomenon, which has been coined ocean acidification (OA). Even though the effects of OA on varying aspects of physiology on SO phytoplankton such as growth, photosynthesis, elemental stoichiometry, and photophysiology (Boelen et al. 2011; *Correspondence: [email protected] This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Additional Supporting Information may be found in the online version of this article.