Ecophysiological response of Southern Ocean cryptophytes to temperature, CO2, light and iron availability

Abstract

The Southern Ocean (SO) is one of the most susceptible regions in the world to climate change. The on-going increase in anthropogenic carbon dioxide (CO2) concentrationin the atmosphere and warming have already brought changes in the composition andabundance of phytoplankton communities in the SO. These changes, however, would not only affect the Antarctic food web, but would also influence the ability of the SO to export carbon as well as absorb heat, which on a bigger scale, potentially impact the global climate and global biogeochemical cycles.

The Western Antarctic Peninsula (WAP) is one of the most productive regions in the SO. Over the past decades, the WAP region has been experiencing rapid warming and these warming events have been reported to cause shifts in phytoplankton community structure such as the increasing occurrence and dominance of cryptophytes in coastal WAP waters. Despite already being well-recognized as an important component of the WAP phytoplankton community, cryptophytes still remain less-studied compared to diatomsand haptophytes.

The most dominant cryptophyte species in the SO belongs to the genus Geminigera. So far, the limited studies available on the key Antarctic cryptophyte species Geminigera cryophila have focused mainly on determining the single effects of various environmental drivers (CO2, warming, light, Fe) on its physiology, but studies looking at the interactive effects of these stressors are still lacking. Hence, it is the main objective of this thesis to fill these knowledge gaps by conducting laboratory and field incubation experiments to determine how the combination of multiple climate drivers would affect the ecophysiologyof SO cryptophytes.

Specifically, Publication 1 explored the combined effects of Fe limitation and ocean acidification (OA) which refers to the decrease in oceans’ pH due mainly to the uptake of (CO2) from the atmosphere, on the growth, carbon production, trace metal quotas and photophysiology of G. cryophila in comparison to the response of a key SO diatom species Pseudo-nitzschia subcurvata. Publication 1 reveals that indeed, G. cryophila has a high Fe requirement as it was strongly impacted by low Fe supply, but it also exhibited a modest increase in growth and carbon production in response to OA in conjunction with high Fe condition. In contrast, the Antarctic diatom P. subcurvata coped well with Fe limitation, but it was not able to take advantage of the high CO2 concentration. The trace metal quotas of the two species were also differently affected by OA and Fe limitation. While Cu:C ratios were enhanced in P. subcurvata in response to low Fe supply and OA, G. cryophila maintained similar Cu:C ratios in all treatments. This observation may be associated with the potentially limited suite of Fe uptake strategies that cryptophytes employ (i.e. absence of Cu-dependent high affinity Fe uptake mechanism) compared to diatoms or the inability to reduce its cellular Fe demand (i.e. by replacing the Fe-requiring electron carrier cytochrome c6 with the Cu-containing plastocyanin). Hence, G. cryophila was strongly impacted by low Fe availability.

Publication 2 aimed at characterizing the combined effects of temperature, OA and light availability on G. cryophila. It is shown here that the cryptophyte has a narrow thermal window compared to diatoms and haptophytes, reaching maximum growth at 4 °C while it stopped growing already at 8 °C. Publication 2 demonstrates that increasing temperature (up to 4 °C) alleviated the negative effects of high light (500 μmol photons m-2 s-1) under ambient pCO2. It is also revealed here that G. cryophila is better adapted to medium irradiances (100 μmol photons m-2 s-1) and also corroborates the findings of Publication 1 that this species has a high tolerance to OA.

In Publication 3, shipboard incubation experiments were conducted to examine the responses of two distinct phytoplankton communities in the WAP coastal region and in the Drake Passage, to increasing light and Fe availability as projected by SO climate models. Both communities exhibited enhanced growth and carbon production in response to increasing Fe and light availability, but differed in the magnitude of the increase. The coastal flagellate-dominated assemblage, wherein a significant number of cryptophytes was encountered, displayed a lower degree of carbon production increase compared to the open ocean diatom-dominated community. This could be attributed to the higher Fe requirement of flagellates which was not fulfilled due to their potentially less efficient Fe uptake strategy, in line with the observations in Publication 1. Likewise, in agreement with Publication 2, the flagellate-dominated assemblage also benefited from medium irradiances (80 μmol photons m-2 s-1), but it did not exhibit further enhancement in carbon production at the higher light treatment (150 μmol photons m-2 s-1). This indicates, as also noted in Publication 1, that Fe has a stronger influence on the physiology of cryptophytes compared to that of light.

Overall, the results of this thesis provide an explanation on why cryptophytes are commonly distributed in Fe-rich coastal regions of the SO. In line with the results of previous studies, this thesis also highlights the potential of cryptophytes to take advantage of the on-going OA and warming events in the WAP region. However, given that OA and warming may potentially modify the bioavailability of Fe in the SO, this thesis also emphasizes the need for conducting studies on the Fe requirement and Fe uptake strategies being employed by cryptophytes. Considering the proposed hypothesis that cryptophytes have a limited suite of Fe uptake strategies, it would also be helpful to study the factors that induces mixotrophy in cryptophytes as this is one strategy that they could utilize to access the needed nutrients for growth. A deeper understanding of the ecophysiology of cryptophytes is important to better ascertain its influence on the overall carbon production and export in the SO and its role in shaping the Antarctic trophic food web.