Antarctic microalgae: physiological acclimation to environmental change

<p>Sea ice algal communities play a very significant role in primary production in the Southern Ocean, being the only source of fixed carbon for all other life in this habitat and contributing up to 22% of Antarctic primary production in ice-covered regions. Therefore it is important to understand how these organisms adapt to this highly variable and harsh environment Previous studies have described their acclimation to changes in environmental conditions but we still do not understand the physiological basis of these responses. This study examines the effects of varying levels of photosynthetically active radiation (PAR), ultraviolet-B (UV-B) radiation and temperature on bottom ice algal communities and individual algal species using pulse-amplitude modulation (PAM) fluorometry, the production of mycosporine-like amino acids (MAAs) and superoxide dismutase (SOD) activity. The experiments conducted in this thesis show that bottom ice algae are capable of acclimating to the higher levels of PAR and temperature that would likely be experienced during sea ice melt As temperature was increased past a threshold temperature of thylakoid integrity, it became the major stressor, causing decreases in photosynthetic yield at around 14°C, even at ambient PAR exposure. Similarly, a thylakoid integrity experiment independently suggested that the critical temperature for the onset of thylakoid damage was 14°C, which correlated well to the 14°C incubation observations, although this is a temperature that sea ice algae are unlikely to encounter in the polar regions. It is likely that sea ice algae produce additional MAAs, known to be cellular sunscreens, in response to increasing levels of UV-B, allowing tolerance of this stressor. This is the first study in the marine environment to demonstrate that algae can produce MAAs in response to increasing PAR and temperature, even in the absence of UV-B, indicating that MAAs may be more than just sunscreen compounds. The levels of UV-B used in this study were representative of those likely to be faced by the algae during sea ice melt. With increasing temperature, the algae maintained photosynthetic yield and decreased MAA production, implying that the rise in temperature aids the algae with another element of photoprotection such as enzymatic repair. As these results contrasted with previous studies of bottom ice algae that showed no additional MAA production in response to higher levels of PAR and UV-B, it was hypothesized that this difference was attributed to variations in species composition that could modify the productivity of the community. The short-term effects of increasing PAR and UV -B on three unialgal cultures of Thalassiosira sp., Fragilariopsis sp. (from the Ross Sea), and Chaetoceros sp. (from the Antarctic Peninsula) were therefore examined. In unialgal culture studies, these three algal species showed higher tolerance to PAR and UV-B compared to that of the mixed culture of bottom ice algae, although there remained species-specific variation. Both Ross Sea species showed increasing photosynthetic yield with increasing PAR and UV-B exposure, but there was a difference in the tolerance shown by the two species. Thalassiosira sp. tolerated higher PAR and lower UV-B and Fragilariopsis tolerated lower PAR and higher UV-B. Both species produced MAAs in response to these stressors, indicating that these compounds allowed the algae to decrease levels of photoinhibition. In comparison to the Ross Sea, the Antarctic Peninsula is an area of higher environmental variability and change, meaning that the species in both regions could have varying acclimatory capabilities. Although data from three species alone cannot conclusively demonstrate that algae from different regions have different acclimatory capabilities, they do illustrate considerable variation between species. Chaetoceros sp. from the Antarctic Peninsula region showed a higher tolerance to PAR and UV-B compared to the Ross Sea species. The former species showed an increase in photosynthetic yield in response to increasing PAR and this was accompanied by a lack of MAA production in response to the experimental levels of PAR, which indicates that the two Ross Sea species have a higher tolerance to PAR compared to the Antarctic Peninsula species. Chaetoceros sp. from the Antarctic Peninsula showed an increase in photosynthetic yield in response to high UV-B exposures, accompanied by MAA production and had no signs of photoinhibition. A further experiment was conducted to address the weaknesses in the initial methodologies, particularly related to control conditions in the short-term experiments. Common species from the Ross Sea, Antarctic Peninsula and the Arctic were exposed to a combination of increased PAR and UV-B over a period of seven days to compare acclimatory abilities using PAM and SOD activity. Thalassiosira antarctica from the Ross Sea, Chaetoceros socialis from the Antarctic Peninsula and C. socialis from the Arctic showed no significant change in quantum yield over the incubation period. This further highlights the importance of running experiments with compounding factors, as an increase in one factor could alleviate the negative effect of the other. There was an unexpected lack of change in SOD activity for all species under all treatments applied, which could indicate that the levels of PAR and UV-B used were not high enough to cause stress in these species. This work also points to the need to assay for various antioxidants, as algae are known to rely on a network of antioxidants in their defence against environmental stresses. The data from this thesis clarify the influence of PAR, UV-B and temperature on sea ice algae, and could help better evaluate the fate of these communities under various climate change scenarios. This study has made important steps towards understanding the acclimatory abilities of sea ice algae. Increasing knowledge of sea ice algal physiology, particularly of photosynthetic health in response to environmental change, will help improve predictions of productivity in the most productive ocean on this planet. Algal tolerance to increasing PAR, UV-B and temperature is remarkable, and this ability could be crucial in the context of future climate change. The productivity of these autotrophic microorganisms strongly influences secondary production that ties their fate to that of all other life in the Southern Ocean.</p>

Antarctic microalgae: physiological acclimation to environmental change

<p>Sea ice algal communities play a very significant role in primary production in the Southern Ocean, being the only source of fixed carbon for all other life in this habitat and contributing up to 22% of Antarctic primary production in ice-covered regions. Therefore it is important to understand how these organisms adapt to this highly variable and harsh environment Previous studies have described their acclimation to changes in environmental conditions but we still do not understand the physiological basis of these responses. This study examines the effects of varying levels of photosynthetically active radiation (PAR), ultraviolet-B (UV-B) radiation and temperature on bottom ice algal communities and individual algal species using pulse-amplitude modulation (PAM) fluorometry, the production of mycosporine-like amino acids (MAAs) and superoxide dismutase (SOD) activity. The experiments conducted in this thesis show that bottom ice algae are capable of acclimating to the higher levels of PAR and temperature that would likely be experienced during sea ice melt As temperature was increased past a threshold temperature of thylakoid integrity, it became the major stressor, causing decreases in photosynthetic yield at around 14°C, even at ambient PAR exposure. Similarly, a thylakoid integrity experiment independently suggested that the critical temperature for the onset of thylakoid damage was 14°C, which correlated well to the 14°C incubation observations, although this is a temperature that sea ice algae are unlikely to encounter in the polar regions. It is likely that sea ice algae produce additional MAAs, known to be cellular sunscreens, in response to increasing levels of UV-B, allowing tolerance of this stressor. This is the first study in the marine environment to demonstrate that algae can produce MAAs in response to increasing PAR and temperature, even in the absence of UV-B, indicating that MAAs may be more than just sunscreen compounds. The levels of UV-B used in this study were representative of those likely to be faced by the algae during sea ice melt. With increasing temperature, the algae maintained photosynthetic yield and decreased MAA production, implying that the rise in temperature aids the algae with another element of photoprotection such as enzymatic repair. As these results contrasted with previous studies of bottom ice algae that showed no additional MAA production in response to higher levels of PAR and UV-B, it was hypothesized that this difference was attributed to variations in species composition that could modify the productivity of the community. The short-term effects of increasing PAR and UV -B on three unialgal cultures of Thalassiosira sp., Fragilariopsis sp. (from the Ross Sea), and Chaetoceros sp. (from the Antarctic Peninsula) were therefore examined. In unialgal culture studies, these three algal species showed higher tolerance to PAR and UV-B compared to that of the mixed culture of bottom ice algae, although there remained species-specific variation. Both Ross Sea species showed increasing photosynthetic yield with increasing PAR and UV-B exposure, but there was a difference in the tolerance shown by the two species. Thalassiosira sp. tolerated higher PAR and lower UV-B and Fragilariopsis tolerated lower PAR and higher UV-B. Both species produced MAAs in response to these stressors, indicating that these compounds allowed the algae to decrease levels of photoinhibition. In comparison to the Ross Sea, the Antarctic Peninsula is an area of higher environmental variability and change, meaning that the species in both regions could have varying acclimatory capabilities. Although data from three species alone cannot conclusively demonstrate that algae from different regions have different acclimatory capabilities, they do illustrate considerable variation between species. Chaetoceros sp. from the Antarctic Peninsula region showed a higher tolerance to PAR and UV-B compared to the Ross Sea species. The former species showed an increase in photosynthetic yield in response to increasing PAR and this was accompanied by a lack of MAA production in response to the experimental levels of PAR, which indicates that the two Ross Sea species have a higher tolerance to PAR compared to the Antarctic Peninsula species. Chaetoceros sp. from the Antarctic Peninsula showed an increase in photosynthetic yield in response to high UV-B exposures, accompanied by MAA production and had no signs of photoinhibition. A further experiment was conducted to address the weaknesses in the initial methodologies, particularly related to control conditions in the short-term experiments. Common species from the Ross Sea, Antarctic Peninsula and the Arctic were exposed to a combination of increased PAR and UV-B over a period of seven days to compare acclimatory abilities using PAM and SOD activity. Thalassiosira antarctica from the Ross Sea, Chaetoceros socialis from the Antarctic Peninsula and C. socialis from the Arctic showed no significant change in quantum yield over the incubation period. This further highlights the importance of running experiments with compounding factors, as an increase in one factor could alleviate the negative effect of the other. There was an unexpected lack of change in SOD activity for all species under all treatments applied, which could indicate that the levels of PAR and UV-B used were not high enough to cause stress in these species. This work also points to the need to assay for various antioxidants, as algae are known to rely on a network of antioxidants in their defence against environmental stresses. The data from this thesis clarify the influence of PAR, UV-B and temperature on sea ice algae, and could help better evaluate the fate of these communities under various climate change scenarios. This study has made important steps towards understanding the acclimatory abilities of sea ice algae. Increasing knowledge of sea ice algal physiology, particularly of photosynthetic health in response to environmental change, will help improve predictions of productivity in the most productive ocean on this planet. Algal tolerance to increasing PAR, UV-B and temperature is remarkable, and this ability could be crucial in the context of future climate change. The productivity of these autotrophic microorganisms strongly influences secondary production that ties their fate to that of all other life in the Southern Ocean.</p>

Ice Algae Model Intercomparison Project phase 2 (IAMIP2)

Ice algae play a fundamental role in shaping sea-ice-associated ecosystems and biogeochemistry. This role can be investigated by field observations; however the influence of ice algae at the regional and global scales remains unclear due to limited spatial and temporal coverage of observations and because ice algae are typically not included in current Earth system models. To address this knowledge gap, we introduce a new model intercomparison project (MIP), referred to here as the Ice Algae Model Intercomparison Project phase 2 (IAMIP2). IAMIP2 is built upon the experience from its previous phase and expands its scope to global coverage (both Arctic and Antarctic) and centennial timescales (spanning the mid-20th century to the end of the 21st century). Participating models are three-dimensional regional and global coupled sea-ice–ocean models that incorporate sea-ice ecosystem components. These models are driven by the same initial conditions and atmospheric forcing datasets by incorporating and expanding the protocols of the Ocean Model Intercomparison Project, an endorsed MIP of the Coupled Model Intercomparison Project phase 6 (CMIP6). Doing so provides more robust estimates of model bias and uncertainty and consequently advances the science of polar marine ecosystems and biogeochemistry. A diagnostic protocol is designed to enhance the reusability of the model data products of IAMIP2. Lastly, the limitations and strengths of IAMIP2 are discussed in the context of prospective research outcomes.

Ice-Associated Amphipods in a Pan-Arctic Scenario of Declining Sea Ice

Sea-ice macrofauna includes ice amphipods and benthic amphipods, as well as mysids. Amphipods are important components of the sympagic food web, which is fuelled by the production of ice algae. Data on the diversity of sea-ice biota have been collected as a part of scientific expeditions over decades, and here we present a pan-Arctic analysis of data on ice-associated amphipods and mysids assimilated over 35 years (1977–2012). The composition of species differed among the 13 locations around the Arctic, with main differences between basins and shelves and also between communities in drift ice and landfast sea ice. The sea ice has been dramatically reduced in extent and thickness during the recorded period, which has resulted in reduced abundance of ice amphipods as well as benthic amphipods in sea ice from the 1980’s to the 2010’s. The decline mainly involved Gammarus wilkitzkii coinciding with the disappearance of much of the multiyear sea ice, which is an important habitat for this long-lived species. Benthic amphipods were most diverse, and also showed a decline over the time-span. They had higher abundance closer to land where they are associated with landfast ice. However, they also occurred in the Central Arctic Ocean, which is likely related to the origin of sea ice over shallow water and subsequent transport in the transpolar ice drift. Recent sampling in the waters east and north of Svalbard has found continued presence of Apherusa glacialis, but almost no G. wilkitzkii. Monitoring by standardized methods is needed to detect further changes in community composition of ice amphipods related to reductions in sea-ice cover and ice type.

Female Pacific walruses (Odobenus rosmarus divergens) show greater partitioning of sea ice organic carbon than males: Evidence from ice algae trophic markers

The expected reduction of ice algae with declining sea ice may prove to be detrimental to the Pacific Arctic ecosystem. Benthic organisms that rely on sea ice organic carbon (iPOC) sustain benthic predators such as the Pacific walrus (Odobenus rosmarus divergens). The ability to track the trophic transfer of iPOC is critical to understanding its value in the food web, but prior methods have lacked the required source specificity. We analyzed the H-Print index, based on biomarkers of ice algae versus phytoplankton contributions to organic carbon in marine predators, in Pacific walrus livers collected in 2012, 2014 and 2016 from the Northern Bering Sea (NBS) and Chukchi Sea. We paired these measurements with stable nitrogen isotopes (δ15N) to estimate trophic position. We observed differences in the contribution of iPOC in Pacific walrus diet between regions, sexes, and age classes. Specifically, the contribution of iPOC to the diet of Pacific walruses was higher in the Chukchi Sea (52%) compared to the NBS (30%). This regional difference is consistent with longer annual sea ice persistence in the Chukchi Sea. Within the NBS, the contribution of iPOC to walrus spring diet was higher in females (~45%) compared to males (~30%) for each year (p < 0.001), likely due to specific foraging behavior of females to support energetic demands associated with pregnancy and lactation. Within the Chukchi Sea, the iPOC contribution was similar between males and females, yet higher in juveniles than in adults. Despite differences in the origin of organic carbon fueling the system (sea ice versus pelagic derived carbon), the trophic position of adult female Pacific walruses was similar between the NBS and Chukchi Sea (3.2 and 3.5, respectively), supporting similar diets (i.e. clams). Given the higher quality of organic carbon from ice algae, the retreat of seasonal sea ice in recent decades may create an additional vulnerability for female and juvenile Pacific walruses and should be considered in management of the species.

Upwelling Irradiance below Sea Ice—PAR Intensities and Spectral Distributions

Upwelling and downwelling spectral (320–920 nm) distributions and photosynthetic active radiation (PAR) intensities were measured below a first-year land-fast sea ice in a western Greenland fjord with and without a snow cover. Time-series of surface upwelling PAR, downwelling PAR, and under-ice PAR were also obtained. Spectral distributions of upwelling and downwelling irradiances were similar except for reduced intensities in the UV, the red, and NIR parts of the spectrum when the ice was snow-covered. Upwelling PAR amounted to about 10% of downwelling intensities, giving 5.1 µmol photons m−2 s−1 at the bottom of the ice with a snow cover and 8.2 µmol photons m−2 s−1 without. PAR partitioning analyses showed that the upwelling was related to scattering by suspended particles in the water column. A snow melt increased under-ice daily maximum downwelling PAR from 50 to 180 µmol photons m−2 s−1 and overall under-ice PAR of 55 and 198 µmol photons m−2 s−1 with 10% upwelling. It is concluded that upwelling PAR below sea ice might be an important factor regarding sea ice algae photophysiology and performance with a 10% higher PAR; specifically when PAR > Ek the light saturation point of the sea ice algae.

Photobiological Effects on Ice Algae of a Rapid Whole-Fjord Loss of Snow Cover during Spring Growth in Kangerlussuaq, a West Greenland Fjord

Snow cover on sea ice is the most important factor controlling light availability for sea ice algae, but it is predicted by climate models to become more variable and stochastic. Here, we document effects of a sudden, complete loss of the entire snow cover on first-year sea ice at Kangerlussuaq Fjord, West Greenland, due to a natural Föhn wind event that caused a ca. 17 °C air temperature increase over 36 h. We applied Imaging-PAM fluorometry to examine effects of snow cover on algal distribution and photobiology and observed a rapid decrease in algal biomass associated with loss of the skeletal ice crystal layer on the underside of the ice that had supported most of the visible algae. Furthermore, the remaining algae were photobiologically stressed, as seen in a significant decrease in the dark-acclimated fluorescence yield (ΦPSII_max) from 0.55 before snow loss to 0.41 after. However, recovery in the dark suggested that non-photosynthetic quenching was successfully dissipating excess energy in the community and that there was little photodamage. An observed decrease in the photosynthetic efficiency α from 0.22 to 0.16 µmol é m−2 s−1 is therefore likely to be due to photoacclimation and the change in community composition. Centric diatoms and flagellates were the main taxa lost in the snow loss event, whereas the sea ice specialist Nitzschia frigida increased in numbers. These observations are similar to those seen in artificial snow-clearing experiments and consistent with snow clearing being a useful approach for investigating the complex interactions between snow cover, irradiance fluctuations, and ice algal performance.

Winter Carnivory and Diapause Counteract the Reliance on Ice Algae by Barents Sea Zooplankton

The Barents Sea is a hotspot for environmental change due to its rapid warming, and information on dietary preferences of zooplankton is crucial to better understand the impacts of these changes on food-web dynamics. We combined lipid-based trophic marker approaches, namely analysis of fatty acids (FAs), highly branched isoprenoids (HBIs) and sterols, to compare late summer (August) and early winter (November/December) feeding of key Barents Sea zooplankters; the copepods Calanus glacialis, C. hyperboreus and C. finmarchicus and the amphipods Themisto libellula and T. abyssorum. Based on FAs, copepods showed a stronger reliance on a diatom-based diet. Phytosterols, produced mainly by diatoms, declined from summer to winter in C. glacialis and C. hyperboreus, indicating the strong direct linkage of their feeding to primary production. By contrast, C. finmarchicus showed evidence of year-round feeding, indicated by the higher winter carnivory FA ratios of 18:1(n-9)/18:1(n-7) than its larger congeners. This, plus differences in seasonal lipid dynamics, suggests varied overwintering strategies among the copepods; namely diapause in C. glacialis and C. hyperboreus and continued feeding activity in C. finmarchicus. Based on the absence of sea ice algae-associated HBIs (IP25 and IPSO25) in the three copepod species during both seasons, their carbon sources were likely primarily of pelagic origin. In both amphipods, increased FA carnivory ratios during winter indicated that they relied strongly on heterotrophic prey during the polar night. Both amphipod species contained sea ice algae-derived HBIs, present in broadly similar concentrations between species and seasons. Our results indicate that sea ice-derived carbon forms a supplementary food rather than a crucial dietary component for these two amphipod species in summer and winter, with carnivory potentially providing them with a degree of resilience to the rapid decline in Barents Sea (winter) sea-ice extent and thickness. The weak trophic link of both zooplankton taxa to sea ice-derived carbon in our study likely reflects the low abundance and quality of ice-associated carbon during late summer and the inaccessibility of algae trapped inside the ice during winter.

Low Fe Availability for Photosynthesis of Sea-Ice Algae: Ex situ Incubation of the Ice Diatom Fragilariopsis cylindrus in Low-Fe Sea Ice Using an Ice Tank

Sea-ice algae play a crucial role in the ecology and biogeochemistry of sea-ice zones. They not only comprise the base of sea-ice ecosystems, but also seed populations of extensive ice-edge blooms during ice melt. Ice algae must rapidly acclimate to dynamic light environments, from the low light under sea ice to high light within open waters. Recently, iron (Fe) deficiency has been reported for diatoms in eastern Antarctic pack ice. Low Fe availability reduces photosynthetic plasticity, leading to reduced ice-algal primary production. We developed a low-Fe ice tank to manipulate Fe availability in sea ice. Over 20 days in the ice tank, the Antarctic ice diatom Fragilariopsis cylindrus was incubated in artificial low-Fe sea ice ([total Fe] = 20 nM) in high light (HL) and low light (LL) conditions. Melted ice was also exposed to intense light to simulate light conditions typical for melting ice in situ. When diatoms were frozen in, the maximum photochemical quantum efficiency of photosystem II (PSII), Fv/Fm, was suppressed by freezing stress. However, the diatoms maintained photosynthetic capability throughout the ice periods with a stable Fv/Fm value and increased photoprotection through non-photochemical quenching (NPQ) via photoprotective xanthophyll cycling (XC) and increased photoprotective carotenoid levels compared to pre-freeze-up. Photoprotection was more pronounced in the HL treatment due to greater light stress. However, the functional absorption cross section of PSII, σPSII, in F. cylindrus consistently increased after freezing, especially in the LL treatment (σPSII &gt; 10 nm2 PSII–1). Our study is the first to report such a large σPSII in ice diatoms at low Fe conditions. When the melted sea ice was exposed to high light, Fv/Fm was suppressed. NPQ and XC were slightly upregulated, but not to values normally observed when Fe is not limiting, which indicates reduced photosynthetic flexibility to adapt to environmental changes during ice melt under low Fe conditions. Although ice algae can optimize their photosynthesis to sea-ice environments, chronic Fe starvation led to less flexibility of photoacclimation, particularly in low light conditions. This may have detrimental consequences for ice algal production and trophic interactions in sea-ice ecosystems if the recent reduction in sea-ice extent continues.