Ice gliding diatoms establish record-low temperature limits for motility in a eukaryotic cell

Despite periods of permanent darkness and extensive ice coverage in polar
environments, photosynthetic ice diatoms display a remarkable capability
of living inside the ice matrix. How these organisms navigate such hostile
conditions with limited light and extreme cold remains unknown. Using a
custom sub-zero temperature microscope during an Arctic expedition, we
present the discovery of motility at record-low temperatures in a
Eukaryotic cell. By characterizing the gliding motility of several ice
diatom species, collected from ice cores in the Chukchi Sea, we record
that they retain motility at temperatures as low as –15 °C.
Remarkably, ice diatoms can glide on ice substrates, a capability absent
in temperate diatoms of the same genus. This unique ability arises from
adaptations in extracellular mucilage that allow ice diatoms to adhere to
ice, essential for gliding. Even on glass substrates where both cell types
retain motility at freezing temperatures, ice diatoms move an order of
magnitude faster, with their optimal motility shifting toward colder
temperatures. Combining field and laboratory experiments with
thermo-hydrodynamic modeling, we reveal adaptive strategies that enable
gliding motility at extreme cold temperatures. These strategies involve
increasing internal energy efficiency with minimal changes in heat
capacity and activation enthalpy, and reducing external dissipation by
minimizing the temperature sensitivity of mucilage viscosity. The
discovery of diatoms' ice gliding motility opens new routes for
understanding their survival within a harsh ecological niche and their
migratory responses to rapid environmental changes. Our work highlights
the robust adaptability of ice diatoms in one of Earth's most extreme
settings.