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Photophysiological responses of marine phytoplankton and ice algae to temperature, iron and light availability in subpolar and polar regions

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Yoshida, K ORCID: 0000-0001-5768-8561 2019 , 'Photophysiological responses of marine phytoplankton and ice algae to temperature, iron and light availability in subpolar and polar regions', PhD thesis, University of Tasmania.

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Abstract

Global warming increases sea temperatures and intensifies stratification of the water column, which directly and indirectly affects marine ecosystems and biogeochemistry, for example, less nutrient supply due to stratification. It has been suggested that the effects of climate change may emerge earlier in the highly productive and ecologically important subpolar and polar regions. In these regions, an increase in temperature may benefit some algal primary producers but a reduction in the extent of sea ice will limit the habitat of ice-associated biota. Light is also a crucial factor for all photosynthetic organisms and its availability can change dramatically when sea ice melts. Iron (Fe) as a micro-nutrient plays a key role in algal metabolic processes, including photosynthesis. This study thus aimed at clarifying the effects of temperature, light and Fe availability on the photophysiology of phytoplankton and ice algae in the changing subpolar and polar oceans.
The effects of temperature on a spring diatom bloom in the coastal Oyashio (COY) were investigated as a representative subpolar coastal spring bloom. The spring diatom blooms in COY waters are highly productive in spite of the low sea surface temperature (SST) (−1−2 ºC in early spring). This study thus focused on the photophysiology and community composition of phytoplankton in COY waters during the pre-bloom and bloom periods from March to April 2015. Next-generation sequencing, targeting the 18S rRNA gene, revealed that the diatom genus Thalassiosira generally dominated the phytoplankton community. Additionally, the relative contribution of Thalassiosira to the total diatom assemblages showed a positive correlation with maximum photosynthetic rates (P\(^B\)\(_{max}\)) throughout this study, suggesting that the genus was the largest contributor to the bloom. A short-term on-deck incubation experiment was also conducted to clarify the role of temperature in determining the photosynthetic functioning of phytoplankton. Here, rising temperature led to an increase in P\(^B\)\(_{max}\) and transcription levels of the diatom-specific rbcL gene coding the large subunit of RuBisCO. It is suggested that the rising temperature upregulated the diatom-specific rbcL gene and then triggered the higher P\(^B\)\(_{max}\) as well as the spring diatom bloom.
In summer, Fe availability is a crucial factor for the dynamics of spring diatom blooms in the western subarctic Pacific, including the Oyashio region. The western subarctic Pacific is known as one of the largest High Nutrient Low Chlorophyll (HNLC) regions. At present, little is known about Fe deficiency in phytoplankton in neritic zones because of the existence of multiple Fe sources and strong vertical mixing along the Kuril Islands. This study also examined the effects of Fe on the community composition and photophysiology of phytoplankton in the western subarctic Pacific near the Kuril Islands and the eastern Kamchatka Peninsula during bloom and post-bloom phases from June to July 2014. An HNLC water was observed outside of the shelf slope. High Chl α concentrations were observed in the coastal region in early June, whereas spring diatom blooms seemed to be terminated in the coastal region near the Kamchatka Peninsula. Detailed scanning electron microscopy demonstrated a clear biogeographical difference in plankton community composition between the coastal and offshore areas. The diatom Chaetoceros was abundant in the Ferich coastal waters, while the genera Fragilariopsis and Pseudo-nitzschia were dominant in the HNLC water outside of the shelf slope. Light availability was also important for primary productivity of phytoplankton, we thus conducted on-deck Fe enrichment bottle incubation experiments at stations with the second shallowest and the deepest surface mixed layer depths (MLD). Fe addition at the second shallowest station did not affect biomass and photochemical efficiency of photosystem II (F\(_v\)/F\(_m\)), whereas Chl α biomass and F\(_v\)/F\(_m\) were increased at the deepest MLD station. These results suggest the Fe-light interaction occurred at the station with the deepest MLD, a result also supported by the photophysiological parameters (E\(_k\): light saturation index of photosynthesis versus irradiance curve). At the study area, it was found that light availability can significantly affect Fe deficiency in the phytoplankton assemblages (i.e., Fe-light co-limitations).
Sea-ice algae contribute 10–25% of the annual primary production of polar seas, and seed large-scale ice-edge blooms. Large fluctuations in temperature, salinity, light and Fe availability, associated with freezing and melting of sea ice, can significantly change the photophysiology of ice algae. Therefore, the effects of multiple co-stressors (i.e., freezing temperature and high brine salinity in a freezing event; and sudden high light exposure during ice melting as well as Fe starvation) on the photophysiology of ice algae were investigated in a series of ice tank experiments with the polar diatom Fragilariopsis cylindrus under different light intensities as well as different Fe availability. When algal cells were frozen into the ice, the maximum quantum yield of photosystem II (PSII) (F\(_v\)/F\(_m\)) decreased regardless of the treatments, possibly due to the damage of PSII reaction centers or subsequent suppression of photochemistry with the reduced capacity of downstream components of PSII due to the high brine salinity stress. Gene expression of the rbcL gene was highly upregulated, suggesting a survival strategy for acclimating to the cold ice environment in the ice. The algae within the ice showed almost the same levels of F\(_v\)/F\(_m\) regardless of the treatment. When the ice melted and the cells were exposed to high light (800 μmol photons m\(^{−2}\) s\(^{−1}\)), F\(_v\)/F\(_m\) sharply decreased, while nonphotochemical quenching (NPQ) was upregulated to dissipate the excess light energy. Interestingly, the psbA gene encoding the D1 protein of PSII was upregulated under high Fe conditions and vice versa. These results suggest that Fe repletion accelerated de novo synthesis of the D1 protein, whereas Fe starvation inhibited repair of the PSII damaged by the high light. The results imply that Fe-starved cells cannot well regulate their photosynthetic plasticity to the environmental changes during ice melting, and would little contribute to ice-edge blooms.

Item Type: Thesis - PhD
Authors/Creators:Yoshida, K
Keywords: Aquatic photosynthesis, Active chlorophyll a fluorescence, Gene expression, Psychrophilic microalgae, Iron availability, Sea ice, Subarctic, Antarctic
Copyright Information:

Copyright 2019 the author

Additional Information:

The author studied for and was awarded a conjoint doctoral degree at both the University of Tasmania and the Hokkaido University

Chapter 2 appears to be the equivalent of a pre-print version of an article published as: Yoshida, K., Endo, H., Lawrenz, E., Isada, T, Hooker, S. B., Prášil, O., Suzuki, K., 2018. Community composition and photophysiology of phytoplankton assemblages in coastal Oyashio waters of the western North Pacific during early spring, Estuarine, coastal and shelf science, 212, 80-94

Chapter 3 appears to be the equivalent of a pre-print version of an article published as: Yoshida, K., Nakamura, S., Nishioka, J., Hooker, S. B., Suzuki, K., 2020. Community composition and photosynthetic physiology of phytoplankton in the western subarctic Pacific near the Kuril Islands with special reference to iron availability, Journal of geophysical research: Biogeosciences, 125, e2019JG005525 An edited version of this paper was published by AGU. Copyright 2020 American Geophysical Union.

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