Tracking single cells undergoing vertical migrations: Connecting Cell Biology to Ocean Ecology

Planktonic single cells, despite their miniscule size are the engines behind biogeochemical cycles in the ocean, and form the base of the marine food web. Despite being 1% of terrestrial primary producing bio-mass, these cells are responsible for fixing half of global carbon. Remarkably, despite being termed “planktonic”, these cells are capable of using active swimming or buoyancy changes to migrate vertically in the water column, over distances of tens to hundreds of meters to position themselves in a suitable ecological niche. However, mechanistically connecting cell state to vertical behavior and hence depth in the water column is a fundamental experimental challenge due to the immense scales involved (microns to meters). Towards solving this challenge we introduce and demonstrate a novel, scale-free vertical tracking microscopy method to image single cells at sub-cellular resolution while tracking their three-dimensional trajectories with no bounds for motion along the axis of gravity. Using our tool, we demonstrate novel biophysical measurements in two classes of ecologically relevant plankton. In single-celled diatoms spanning four species, we discovered rapid density fluctuations over milliseconds time-scale by concurrently measuring cell behavior (vertical sinking speed) and cell’s molecular state by combining our tracking microscopy method with fluorescence imaging of signaling reporters. In the dinoflagellate cells P. noctiluca, we observed, for the first time, cell-division in suspension, far from substrates and resolved microscale fluctuations in cell density during division and rapid changes in cell volume post-division. In other ecologically important dinoflagellates which are active swimmers, including A. sanguinea, we measured microscale cell behaviors that showed rapid switching from upward to downward swimming, or vice versa, shedding light on the biophysical mechanisms behind previous population-scale measurements in dinoflagellates. Finally, we combined our tracking methodology with environmental patterning of light, chemical species and ambient pressure to bring the virtual-reality paradigm, which is well-established in neuroscience, to cell biology in the ocean.