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.