Microrheology reveals microscale viscosity gradients in planktonic systems

Guadayol, Oscar; Mendonca, Tania; Segura-Noguera, Mariona; Wright, Amanda J; Tassieri, Manlio; Humphries, Stuart

Abstract

Microbial activity in planktonic systems creates a dynamic and heterogeneous microscale seascape that harbors a diverse community of microorganisms and ecological interactions of global significance. In recent decades great effort has been put into understanding this complex system, particularly focusing on the role of chemical patchiness, while overlooking a physical parameter that governs microbial life and is affected by biological activity: viscosity. Here we reveal spatial heterogeneity of viscosity in planktonic systems by using microrheological techniques that allow measurement of viscosity at length scales relevant to microorganisms. We show the viscous nature and the spatial extent of the phycosphere, the region surrounding phytoplankton. In ∼45% of the phytoplankton cells analyzed we detected increases in viscosity that extended up to 30 μm away from the cell with up to 40 times the viscosity of seawater. We also show how these gradients of viscosity can be amplified around a lysing phytoplankton cell as its viscous contents leak away. Finally, we report conservative estimates of viscosity inside marine aggregates, hotspots of microbial activity, more than an order of magnitude higher than in seawater. Since the diffusivities of dissolved molecules, particles, and microorganisms are inversely related to viscosity, microheterogeneity in viscosity alters the microscale distribution of microorganisms and their resources, with pervasive implications for the functioning of the planktonic ecosystem. Increasing viscosities impacts ecological interactions and processes, such as nutrient uptake, chemotaxis, and particle encounter, that occur at the microscale but influence carbon and nutrient cycles at a global scale.

Citation

Guadayol, O., Mendonca, T., Segura-Noguera, M., Wright, A. J., Tassieri, M., & Humphries, S. (2021). Microrheology reveals microscale viscosity gradients in planktonic systems. Proceedings of the National Academy of Sciences, 118(1), Article e2011389118. https://doi.org/10.1073/pnas.2011389118

• Journal Article Type: Article
• Acceptance Date: Nov 23, 2020
• Online Publication Date: Dec 21, 2020
• Publication Date: Jan 5, 2021
• Deposit Date: Jan 5, 2021
• Publicly Available Date: Jan 5, 2021
• Print ISSN: 0027-8424
• Electronic ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Peer Reviewed: Peer Reviewed
• Volume: 118
• Issue: 1
• Article Number: e2011389118
• DOI: https://doi.org/10.1073/pnas.2011389118
• Keywords: microscale patchiness, phytoplankton, extracellular polymeric substances, viscosity, passive microrheology
• Public URL: https://nottingham-repository.worktribe.com/output/4279456
• Publisher URL: https://www.pnas.org/doi/full/10.1073/pnas.2011389118