Acclimation potential of the Arctic keystone species Polar cod in a changing ocean: linking transcriptomic plasticity to species performance

As climate change continues to exert significant pressure on ecosystems, understanding the acclimation potential of keystone species is imperative for both ecological research and conservation efforts. The Arctic is expected to be the region most affected by ongoing climate change. Over the past four decades, the Arctic has exhibited a warming trend four times faster than the global average. Furthermore, the loss of sea ice has increased by approximately 50% since the 1980s, leading to an amplified summer stratification of the ocean and the potential for the formation of hypoxic zones in deeper waters. Thus, the present thesis analyses the metabolic and molecular acclimation strategies of the Arctic keystone species, the Polar cod (Boreogadus saida), in response to three critical environmental stressors: warming, ocean acidification and hypoxia. These will be compared, as far as possible, with observations in their natural environment, through transcriptomic analysis conducted along the north and west coasts of the Svalbard archipelago. By investigating, both short- and long-term responses at the physiological and transcriptomic level, a comprehensive overview of the acclimation potential of Polar cod to changing environmental conditions and the relationship between physiological acclimation strategies and the underlying molecular mechanisms will be provided.
To further examine the impact of hypoxia on Polar cod, in the first chapter of this thesis (manuscript I) several metabolic parameters, including standard, routine, and maximum metabolic rates (SMR, RMR, MMR), aerobic scope (AS), and critical oxygen saturations Pcrit, and Pcrit-max were determined. Pcrit is defined as the oxygen saturation at which oxygen supply fails to cover the minimum demand for oxygen, coupled with the onset of anaerobic metabolism, and Pcrit-max determines the oxygen saturation at which oxygen supply fails to cover the maximum demand for oxygen. These parameters were measured under conditions of progressive hypoxia at 2 °C and after acclimation close to the species’ thermal limits (10 °C) using intermittent-flow and swim tunnel respirometry. The findings revealed that Polar cod exhibits oxygen-regulating behavior, maintaining SMR above baseline metabolic levels, with a stable AS across temperature conditions. Pcrit-max exhibited constant stability at both temperatures and reached a value of approximately 100 µmol L-1 at the respective temperatures, corresponding to 27.72 ± 16.79 % air saturation at 2 °C and 37.22 ± 12.92 % air saturation at 10 °C. These results confirmed the assumption that Pcrit-max is solely dependent on oxygen concentration but not on temperature. Notably, Polar cod tolerated oxygen saturations down to a Pcrit of 12.56 ± 1.59 % air saturation at typical habitat temperatures, which increased to 24.37 ± 1.65 % air saturation at elevated temperatures. This indicates a greater resilience to changing environmental conditions, than would be expected for a high-latitude, stenothermic species. It further suggests that low-oxygen zones with cold bottom water temperatures, that persist throughout the summer months, have the potential to function as refuges for the Polar cod in the near future, should the immigration of less hypoxia-tolerant predators, such as the Atlantic cod, Gadus morhua, increase further. Already at 5 °C, the Pcrit of this predator is located at approximately 22 % air saturation, depending on the life stage. However, as Polar cod’s Pcrit is projected to rise with increasing temperatures, their physiological advantages may diminish, particularly in competition with invasive species and predators in a warming world.
As oxygen depletion is not the sole consequence of future warming, and is closely linked to the increase in CO2 levels in water through respiratory processes, it was imperative to incorporate the effects of acidification into the analysis of the adaptive capacity of Polar cod. As part of the BIOACID project, which addressed the physiological resilience of Polar cod to ocean acidification and global warming, Polar cod were long-term acclimated in a comprehensive approach. Three distinct CO2 concentrations representing current (390 ppm) and two projected climate scenarios (780 ppm and 1170 ppm), were chosen in conjunction with four temperature settings (0, 3, 6, and 8 °C). The focus in the second chapter of this thesis (manuscript II) was placed on analyzing hepatic transcriptomic profiles derived from physiologically characterized fish, within the framework of the BIOACID project, to elucidate molecular responses to the environmental stressors. Results indicated a notable resilience of Polar cod to elevated CO2 levels, as no classical stress response was observed in the transcriptomic data and progressing PCO2 generally had no significant influence on transcriptomic responses. Instead, temperature emerged as the more influential factor, triggering molecular responses primarily in metabolic pathways associated with central energy metabolism. Thus, with increasing temperature, a clear shift in energy metabolism away from a lipid-based to a carbohydrate-based metabolism was observed. An adaptation strategy that is already known from Antarctic species such as the Antarctic eelpout, Pachycara brachycephalum, and can therefore be attributed to the stenothermic, cold-adapted nature of the Polar cod. In conjunction with whole animal and physiological parameters from previous studies within the BIOACID project, for example in behavioral impairments, increased energy turnover, increased mitochondrial proton leak and decreased growth, a critical upper temperature of around 8°C could be identified for the long-term performance of the Svalbard population of Polar cod.
In order to gain a comprehensive understanding of the responses of organisms to artificially generated climate scenarios, it is essential to not only consider immediate responses but also acclimatization under natural environmental conditions. Therefore, the transcriptome of Polar cod along an environmental cline from the north and west coasts of the Svalbard archipelago, was investigated in the third chapter of this thesis (manuscript III). This gradient encompassed a range of environmental factors, each of which exhibited significant variation at the sample site. These included temperature (ΔT = 3.20 °C), salinity (ΔS = 0.70 psu), oxygen content (ΔO2 = 25.30 % air saturation), dissolved inorganic carbon (DIC, ΔDIC = 138.86 µmol/kg), as well as bathymetry. The analyses revealed evidence of local adaptation and significant transcriptional variation on an environmental cline. The existence of distinct phenotypic populations (ecotypes) around the Svalbard archipelago can be suggested; however, the nature and extent of genetically manifested differentiation of populations has yet to be confirmed. Further high-resolution population genomic analyses are required to determine the genetic basis of the observed phenotypic plasticity of the local populations.
The aforementioned findings indicate that, while the Polar cod displays a certain degree of resilience to climate change, rising temperatures continue to exert a substantial influence on physiological performance and metabolic regulation, and will remain a critical factor for the species’ survival. The various analyses also suggest that the survival strategy of Polar cod to higher than optimal temperatures seems to be rather passive. The organism seems to prepare itself to wait for the situation to improve; to store and spare energy in case the situation deteriorates further; and to further limit functions such as reproduction, growth, and mobility. Moreover, the capacity for anaerobic metabolism appears to be relatively limited in this species, although the hypoxia tolerance seems to be particularly pronounced at cold temperatures (Pcrit = 12.56 ±1.59 % air saturation at 2 °C). It appears that the species adjusts its behavior (e.g., the reduction of anaerobically fueled burst swimming with progressive hypoxia) and metabolic activity (e.g., metabolic rates that never fall below the SMR, even at Pcrit) in order to avoid anaerobic metabolism. One potential adaptation could be an increased oxygen extraction efficiency, as indicated by an upregulated SMR in the Pcrit-max range at both temperatures, leading to improved oxygen supply at low PO2. This indicates the potential for the existence of as yet unidentified, specialized metabolic adaptations that do not entail an exclusive, short-term transition to energy fluxes from anaerobic metabolic pathways at Pcrit. In addition, evidence of local adaptation and significant transcriptional variation to an environmental gradient was observed. This thesis underscores the phenotypic plasticity in this valuable keystone species, providing a rather optimistic outlook for it in a changing world.