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Active lipids enable intelligent swimming under nutrient limitation

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Published on Monday, 07 November 2022

Biophysicists from the University of Luxembourg have uncovered how microplankton – key photosynthetic organisms which produce nearly 50% of the oxygen we breathe – adopt a thrifty lifestyle when nutrients turn limiting. They strategically harness internal lipids to regulate swimming properties to maximize their fitness.

Prof. Anupam Sengupta and his team discovered this evolutionary trick by monitoring harmful bloom-forming phytoplankton species, using multi-scale quantitative imaging techniques, analytical and physiological measurements, fluid dynamic simulations and mathematical modelling. Precise tracking of the intracellular organelles (both size and position within cells) and the swimming behaviour reveal an emergent synergy between active lipid movement and cell-shape that ultimately enables microplankton to navigate dynamic nutrient landscapes. The groundbreaking findings appear in this week’s edition of Science Advances.

Figure 1. Active regulation of lipid droplets (LD; N is the cell nucleus) enables intelligent swimming in phytoplankton. The size and position of intracellular lipid droplets, in synergy with cell shape, regulate gravitactic properties under limiting nutrient settings. The swimming properties are rapidly restored when nutrients-even a fraction of the optimal level-are reincorporated. Image source: Physics of Living Matter Group, University of Luxembourg.

Microbial nutrients are turning scarce: An unavoidable consequence of climate change

As open oceans continue to warm, modified currents and enhanced stratification exacerbate nutrient limitation, thus limiting primary production. The ability to migrate vertically offers motile phytoplankton a crucial–yet energetically expensive–advantage that allows vertical redistribution for growth, nutrient uptake and energy storage in nutrient-limited water. Over the last years, Prof. Sengupta has pioneered discoveries that point toward exquisite biomechanical strategies which phytoplankton employ to adapt to changes in their habitat, for instance, due to ocean turbulence (Nature 2017), and early-warning protective mechanisms in face of biophysical stresses (Proceedings of the National Academy of Sciences, USA 2021). How these miniscule yet indispensable microbes adapt to evolving nutrient landscapes – driven substantially by the climate change – has remained unknown. Now researchers from the Physics of Living Matter Group, headed by Prof. Sengupta, reveal the fate of phytoplankton through a multi-scale cross-disciplinary investigation spanning microbiology, physics, mathematics and numerical modeling. Based on a red-tide forming microplankton, the study uncovers how species harness lipid droplets (LDs) – so far known to serve as energy-storing organelles – double as biomechanical triggers to regulate swimming properties under nutrient limitation (Figure 1). By actively controlling the position and size of the LDs, cells can decide whether to swim up or down: a key survival trait of photosynthetic microbes as their vertical position in the water column determines light and nutrient availability.

Figure 2. Doctoral students and co-authors, Arkajyoti Ghoshal (L) and Narges Kakavand (R), at the Ocean-in-Lab set up, monitoring microplankton motion under precisely controlled biophysical conditions. Image source: Télécran cover story: Winzige Weltretter (22 June 2022).

Cross-scale and cross-disciplinary approaches were crucial to the discovery

Alongside intracellular tracking and quantification of swimming properties using the custom-built Ocean-in-Lab set up (Figure 2), Prof. Sengupta’s team measured changes in the planktons’ ability to transform light into energy, and production of oxidative molecules, a key marker for physiological stress. Taken together, the results link intracellular reorganization with biomechanics of swimming, and further provide a mechanistic framework to estimate the underlying energetics of resource acquisition under supply constraints. The combination of single-cell time-lapse imaging, particle image velocimetry of swimming populations, numerical simulations and continuum modelling, and a host of microbiology and analytical techniques were crucial for this ground-breaking discovery. This cross-disciplinary research opens new vistas in the research of active and intelligent microbial matter, and provides a fresh perspective on microbial adaptation to environmental variations, including those imposed by climate and lifestyle changes.

Paper:Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton”, Science Advances 8, eabn6005 (2022).