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Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton

Anupam Sengupta, Jayabrata Dhar, Francesco Danza, Arkajyoti Ghoshal, Sarah Müller, Narges Kakavand
doi: https://doi.org/10.1101/2021.10.17.463831
Anupam Sengupta
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
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  • For correspondence: anupam.sengupta@uni.lu
Jayabrata Dhar
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
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Francesco Danza
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
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Arkajyoti Ghoshal
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
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Sarah Müller
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
2Swiss Nanoscience lnstitute, University of Basel, 82, Klingelbergslrasse, 4056 Basel, Switzerland
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Narges Kakavand
1Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, 162A, Avenue de la Faïencerie, 1511 Luxembourg City, Luxembourg
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Abstract

As open oceans continue to warm, modified currents and enhanced stratification exacerbate nitrogen and phosphorus limitation, constraining primary production. The ability to migrate vertically bestows motile phytoplankton a crucial–albeit energetically expensive–advantage toward vertically redistributing for optimal growth, uptake and resource storage in nutrient-limited water columns. However, this traditional view discounts the possibility that the phytoplankton migration strategy may be actively selected by the storage dynamics when nutrients turn limiting. Here we report that storage and migration in phytoplankton are coupled traits, whereby motile species harness energy storing lipid droplets (LDs) to biomechanically regulate migration in nutrient limited settings. LDs grow and translocate–directionally–within the cytoplasm to accumulate below the cell nucleus, tuning the speed, trajectory and stability of swimming cells. Nutrient reincorporation reverses the LD translocation, restoring the homeostatic migratory traits measured in population-scale millifluidic experiments. Combining intracellular LD tracking and quantitative morphological analysis of red-tide forming alga, Heterosigma akashiwo, along with a model of cell mechanics, we discover that the size and spatial localization of growing LDs govern the ballisticity and orientational stability of migration. The strain-specific shifts in migration which we identify here are amenable to a selective emergence of mixotrophy in nutrient-limited phytoplankton. We rationalize these distinct behavioral acclimatization in an ecological context, relying on concomitant tracking of the photophysiology and reactive oxygen species (ROS) levels, and propose a dissipative energy budget for motile phytoplankton alleviating nutrient limitation. The emergent resource acquisition strategies, enabled by distinct strain-specific migratory acclimatizing mechanisms, highlight the active role of the reconfigurable cytoplasmic LDs in guiding vertical movement. By uncovering the mechanistic coupling between dynamics of intracellular changes to physiologically-governed migration strategies, this work offers a tractable framework to delineate diverse strategies which phytoplankton may harness to maximize fitness and resource pool in nutrient-limited open oceans of the future.

One sentence summary Phytoplankton harness reconfigurable lipid droplets to biomechanically tune migratory strategies in dynamic nutrient landscapes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Funding: This work was supported by the ATTRACT Investigator Grant (Grant no. A17/MS/11572821/MBRACE), the PRIDE Doctoral Training Unit (project PRIDE19/14063202/ACTIVE), and the AFR Grant (Grant no. 13563560) of the Luxembourg National Research Fund. The work received generous support from the Human Frontier Science Program Cross Disciplinary Fellowship (to J.D., LT000368/2019-C), and the Swiss National Science Foundation Early Postdoc Mobility (to F.D., project number: P2GEP3_184481).

  • Competing interests: Authors declare no competing interests.

  • Data and materials availability: Data and codes are available in the main text, or upon resquests made to the corresponding author.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 18, 2021.
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Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton
Anupam Sengupta, Jayabrata Dhar, Francesco Danza, Arkajyoti Ghoshal, Sarah Müller, Narges Kakavand
bioRxiv 2021.10.17.463831; doi: https://doi.org/10.1101/2021.10.17.463831
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Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton
Anupam Sengupta, Jayabrata Dhar, Francesco Danza, Arkajyoti Ghoshal, Sarah Müller, Narges Kakavand
bioRxiv 2021.10.17.463831; doi: https://doi.org/10.1101/2021.10.17.463831

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