Microrheology reveals microscale viscosity gradients in planktonic systems

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.

Fore-aft clearance controls how three-dimensional confinement affects micropropulsion

“…In yield-stress materials a swimmer also can create a nearby fluidized region [89], and swimmers moving across an interface of fluids with different viscosities may drag a surrounding amount of different-viscosity fluid with them [90]. Active remodeling of local material properties can also be caused by thermal or chemical effects; plankton and bacteria can exude or consume viscosity-altering substances [57][58][59][60], thermal heating of microrobots can locally decrease viscosity, and the degelling strategy of H. pylori has been mimicked in magnetically rotated microrobots [56].…”

“…1b). Local modification of material parameters also occurs chemically near microrobots [56], in the phycospheres of plankton [57][58][59][60], and by thermal [61,62] and mechanical effects [26,63].…”

OptoRheo: Simultaneousin situmicro-mechanical sensing and imaging of live 3D biological systems

“…The inert probes can be embedded in the hydrogel during encapsulation 6,[19][20][21] or even internalised into cells 22 to probe intra-cellular viscoelasticity. In suspension cultures, an optical trap can be used to hold the probe in the field of view within the cells' microniche during the measurement time-window 23 . This approach makes the instrument suitable for micro-mechanical sensing in a wide range of cell culture substrates such as those commonly employed in the biomedical field.…”

Microrheology With an Anisotropic Optical Trap

“…Another successful application of optical tweezers is in the field of "hybrid" microrheology, whereby an optically trapped bead acts as a probe, revealing the thermal fluctuations of the molecules in the suspending fluid. Microrheology with OT (MOT) has been used with growing popularity to study the rheology of complex biological materials such as the vitreous humor [11], biopolymer networks [12], and extracellular secretions from phytoplankton [13] at the microscale.…”