Discussions
Growth strategies : The Group 2i Isochrysidales global distribution shows that the lineage is restricted to marine and lacustrine habitats with seasonal or perennial ice cover. The time series of water and ice samples from the Baltic Sea shows that Group 2i is a part of the ice algae community and blooms before other Isochrysidales in the early spring. Potential growth strategies that contribute to its prosperity under cold climates in both hemispheres include 1) the forming of resting stages; 2) mixotrophy; 3) a preference for low growing temperatures and adaptability to a wide range of salinities.
Forming of cysts was observed in Group 2 species, which allows the cells to stay in sea ice or surface sediments for a long time33. In an enrichment experiment, Group 2i was triggered out of its resting stage (during which the cells were not active and alkenone production was paused) in the sediment by increasing the light intensity from 100 μmol m2s-1 to 200 μmol m2s-134,35. Group 2i likely forms cysts in the sediment and sea ice during prolonged winters when light availability is limited, and can be activated when light availability increases. This was observed in the Canadian Arctic Archipelago, Baffin Bay, and Greenland fjords, where the bathymetry of these regions enhances vertical mixing from tidal energy which can re-suspend cysts from the sediment and leads to activation of the cysts3,36,37.
Group 2i could potentially use mixotrophy to compensate for reduced photosynthesis under light-limited conditions. Multiple Isochrysidales species are capable of mixotrophy, including Emiliania huxleyi ,Gephyrocapsa oceanica , Isochrysis galbana , andTisochrysis lutea 38–41. Increased biomass production and nutrient conversion efficiency under mixotrophic conditions has been reported in Group 2 species Isochrysis galbana and Tisochrysis lutea 39,40. Mixotrophy of Group 2i has been observed in the McMurdo Dry Valley Lake located in Antarctica 28. Culture enrichment of Isochrysidales isolated from this site could grow in either dark or light conditions but achieved optimal growth under mixotrophic conditions with organic carbon sources such as cereal grass, rice, and yeast extract 28. Group 2i Isochrysidales takes up a significant proportion (80% based on DNA sequencing) of the mixotrophic community in the McMurdo Dry Valley Lake and is an important primary producer in this lake. Moreover, the gene copy abundance of Group 2i measured through qPCR is not correlated with light availability in this lake 28,42. The capability of mixotrophy could give Group 2i an advantage during the early stages of the phytoplankton bloom succession around ice melt where light availability was still low. Mixotrophy could potentially compensate for photosynthesis for Group 2i when photosynthetically active radiation was relatively low27,28.
Culture experiments also demonstrate Group 2i Isochrysidales’ preference for low growing temperatures and adaptability to a wide range of salinities. Liao and Huang 14 cultured the Group 2i strain RCC5486 (isolated from Baffin Bay) at different temperatures from 0-12 ˚C at 31 ppt under light: dark cycle of 16:8 hrs and found that RCC5486 growth rates were high at 0, 3, 6, 9 ˚C, but failed to grow at 10.5 and 12 ˚C. Liao et al. (2022) also tested different salinities (15, 21, 26, 31, and 38 ppt) under 3˚C and did not observe a significant difference in growth rate at different salinities. The preference of low temperature and flexibility with salinity enable Group 2i to survive in sea ice brine channels, melt ponds, and under-ice water, where the temperature is low, and salinity fluctuates greatly when ice forms and melts. The temperature preference explains why Group 2i is not detected in sediments from Chesapeake Bay and temperate lakes and water columns during summer, i.e. Lake George and the Baltic Sea35.
Habitats, bloom successions and implications for paleoclimatology : The seasonal succession of Group 2i in the Gulf of Finland suggests that it does not solely live in the meltwater, in the under-ice water, or was merely ”trapped into” the sea ice. Instead, Group 2i was concentrated into the sea ice during ice formation via certain selective mechanisms, and can thrive in the brine channels under fluctuating salinity 21. In contrast toEmiliania huxleyi , which blooms during warmer temperatures, Group 2i was absent in water samples collected during the summer months in the Gulf of Finland and Skagerrak. Group 2i is not a part of the summer phytoplankton bloom; instead, they are part of the ice algae assemblage and potentially seeded the under-ice bloom through brine drainage in the spring. Group 2i likely permeates all three phases of the ice algal bloom from pre-bloom, bloom, to post-bloom, and is most prominent in the first two phases before the ice starts to break up, as Group 2i was the most abundant lineage among haptophyte in the sea ice during the entire ice season in Gulf of Finland and active Group 2i cells were isolated from an ice core in Baffin bay during pre-bloom and bloom development21,37. The exact timing of Group 2i growth and its role in the bloom succession likely differs depending on available sunlight, ice properties, temperature, and nutrient conditions.
Similar Isochrysidales bloom successions exist in lacustrine environments with seasonal ice cover. In a water column time series from Lake George during the spring, two non-overlapping Isochrysidales blooms were observed 35. The early bloom that consisted of Group 2i peaked shortly after ice melt when the surface water was around 7 ˚C, and the population quickly declined as water temperature continued to rise 35. In contrast, the later bloom consisted of Group 2w, and their DNA read abundance peaked around 15 ˚C. The two separate blooms are also evident in different alkenone profiles, which are dominated by C37:4 and C37:3,respectively 34.
A holistic picture of Group 2i’s ecology greatly extends alkenones as paleoclimate proxies: 1) it reaffirms the underlying basis for using %C37:4 as a sea-ice proxy in high latitude oceans for both Northern Hemisphere and Southern Hemisphere; 2) In temperate regions with seasonal ice where both 2i and 2w are present in saline lakes, interpretation of %C37:4 is less straight forward, as Group 2w is also capable of producing variable amounts of C37:4. However, C39:4Me alkenone has been found exclusively in 2i Isochrysidales and is not present is 2w species 9,14. Thus, the relatively abundance of C39:4Me alkenone (i.e., %C39:4 ) may be better suited for reconstructing past lake ice coverages. 3) In settings where only Group 2i or 2w is present, alkenones may allow reconstruction of cold or warm season temperatures, respectively. For example, in warm settings with no seasonal ice cover that only have Group 2w, such as Spanish lakes and Chesapeake Bay. In such settings, alkenone unsaturation ratios should primarily reflect warm season temperatures.