Dissecting physiological temperature responses in Arctic Marine Microalgae

The Arctic Ocean is most prone to climate change, which exposes marine organisms to especially high degrees of ocean warming. Phytoplankton, the main primary producers of the Arctic Ocean, experience thermally induced changes in their physiology, and these impacts will likely propagate up the food web and have severe effects on marine biogeochemical cycling. The objective of this dissertation was to unravel how Arctic phytoplankton responds to different warming scenarios with a special emphasis on their underlying physiology. To achieve this, I used a combination of single-strain phytoplankton incubation experiments, including detailed physiological characterizations, and incubation experiments with natural Arctic phytoplankton communities to substantiate overarching temperature responses of phytoplankton physiology also on an ecologically more relevant level.
Publication I aimed to assess temperature response patterns of multiple functional traits in Arctic key phytoplankton species. To this end, I cultivated the centric diatom Thalassiosira hyalina, the mixotrophic picoeukaryote Micromonas pusilla and the ice-algae Nitzschia frigida over a temperature gradient from 0°C to 14°C and measured growth rates, biomass production, quotas of biomass and pigmentation as well as photophysiology. Next to surprisingly high optimal growth temperatures and maximal growth rates in all species, it was found that thermal sensitivities and optimal temperatures varied among species and functional traits. This resulted in distinct temperature response patterns of physiological processes such as cell division and biomass production, with their interplay ultimately shaping distinct temperature response patterns of biomass quotas.
Publication II aimed to identify hypothesized physiological imbalances between photosynthetic and respiratory sub-processes under warming. I further intended to understand how fundamental regulatory mechanisms adjust physiology to explain the high phenotypic plasticity of Arctic phytoplankton in response to increasing temperatures. To this end, I assessed photophysiological characteristics of photosystem II (PSII) as well as gas fluxes of 18O2, 16O2 and CO2 corresponding to photosynthetic O2 production and C-fixation as well as respiratory CO2 release and O2 consumption in T. hyalina at distinct temperatures (2°C, 6°C and 10°C) using fast repetition rate fluorometry (FRRf) and membrane-inlet mass-spectrometry (MIMS). I found two major regulatory strategies of T. hyalina to acclimate to increasing temperatures. First, T. hyalina cells upregulated their light harvesting abilities to compensate for detrimental temperature effects on PSII efficiency, which made cells more prone to light-limitation. Thereby, cells were able to maintain their absolute electron transport rates per PSII, resulting in unchanged O2 production. Second, I found that a metabolic coupling between chloroplasts and mitochondria was essential for cells to dissipate excess reductant towards mitochondrial processes, which was even more prominent under warming. In this situation, the plastidial reductants fueled the mitochondrial electron transport chain directly, which in turn resulted in a redox-mediated downregulation of the respiratory CO2 release, which consequently maximized net biomass retention of the whole cell.
Finally, Publication III and IV aimed to understand how temperature affects phytoplankton physiology on the level of natural Arctic phytoplankton communities. To this end, communities from the open-ocean Fram Strait (Publication III) and a coastal fjord system in Svalbard (Publication IV) were incubated under similar temperature and light conditions as in Publication II. Biomass accumulation, O2 fluxes of photosynthesis and respiration, photophysiology as well as community composition were assessed using a ship-going MIMS system or O2 optodes, FRRf as well as rRNA 18s metabarcoding, respectively. Both communities exhibited a stimulated net biomass retention under warming scenarios, despite a lowered net O2 production, due to strongly increasing respiratory O2 consumption. These responses were not accompanied by distinct species shifts, e.g. towards more heterotrophic communities, indicating that the opposing temperature responses of O2- and C-fluxes in the communities were likely a result of the same physiological regulatory mechanisms as observed in the single-strain experiment.
Findings from single-strain as well as community experiments strongly indicate that a metabolic coupling of chloroplasts and mitochondria is a fundamental mechanism across communities to plastically respond to ocean warming, that allows Arctic phytoplankton to thrive under increasing temperatures. In line with this, all Publications also revealed that optimal temperatures for growth and biomass production exceeded those in the present Arctic Ocean, suggesting a stimulation of biomass accumulation at least under moderate warming. Data of photophysiological assessments further signify synergistic beneficial effects on photosynthetic processes under a combined increase of temperature and light intensity, as it is projected for the future Arctic Ocean.