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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.

SUBMITTER: Guadayol O

PROVIDER: S-EPMC7817219 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Microrheology reveals microscale viscosity gradients in planktonic systems.

Guadayol Òscar Ò Mendonca Tania T Segura-Noguera Mariona M Wright Amanda J AJ Tassieri Manlio M Humphries Stuart S

Proceedings of the National Academy of Sciences of the United States of America 20210101 1

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 ...[more]

PMID: 33443173

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Project description:Conventional electrodes and associated positioning systems for intracellular recording from single neurons in vitro and in vivo are large and bulky, which has largely limited their scalability. Further, acquiring successful intracellular recordings is very tedious, requiring a high degree of skill not readily achieved in a typical laboratory. We report here a robotic, MEMS-based intracellular recording system to overcome the above limitations associated with form factor, scalability, and highly skilled and tedious manual operations required for intracellular recordings. This system combines three distinct technologies: (1) novel microscale, glass-polysilicon penetrating electrode for intracellular recording; (2) electrothermal microactuators for precise microscale movement of each electrode; and (3) closed-loop control algorithm for autonomous positioning of electrode inside single neurons. Here we demonstrate the novel, fully integrated system of glass-polysilicon microelectrode, microscale actuators, and controller for autonomous intracellular recordings from single neurons in the abdominal ganglion of Aplysia californica (n = 5 cells). Consistent resting potentials (<-35 mV) and action potentials (>60 mV) were recorded after each successful penetration attempt with the controller and microactuated glass-polysilicon microelectrodes. The success rate of penetration and quality of intracellular recordings achieved using electrothermal microactuators were comparable to that of conventional positioning systems. Preliminary data from in vivo experiments in anesthetized rats show successful intracellular recordings. The MEMS-based system offers significant advantages: (1) reduction in overall size for potential use in behaving animals, (2) scalable approach to potentially realize multi-channel recordings, and (3) a viable method to fully automate measurement of intracellular recordings. This system will be evaluated in vivo in future rodent studies.

Project description:BackgroundCoastal aquatic ecosystems include chemically distinct, but highly interconnected environments. Across a freshwater-to-marine transect, aquatic communities are exposed to large variations in salinity and nutrient availability as tidal cycles create periodic fluctuations in local conditions. These factors are predicted to strongly influence the resident microbial community structure and functioning, and alter the structure of aquatic food webs and biogeochemical cycles. Nevertheless, little is known about the spatial distribution of metabolic properties across salinity gradients, and no study has simultaneously surveyed the sediment and water environments. Here, we determined patterns and drivers of benthic and planktonic prokaryotic and microeukaryotic community assembly across a river and tidal lagoon system by collecting sediments and planktonic biomass at nine shallow subtidal sites in the summer. Genomic and transcriptomic analyses, alongside a suite of complementary geochemical data, were used to determine patterns in the distribution of taxa, mechanisms of salt tolerance, and nutrient cycling.ResultsTaxonomic and metabolic profiles related to salt tolerance and nutrient cycling of the aquatic microbiome were found to decrease in similarity with increasing salinity, and distinct trends in diversity were observed between the water column and sediment. Non-saline and saline communities adopted divergent strategies for osmoregulation, with an increase in osmoregulation-related transcript expression as salinity increased in the water column due to lineage-specific adaptations to salt tolerance. Results indicated a transition from phosphate limitation in freshwater habitats to nutrient-rich conditions in the brackish zone, where distinct carbon, nitrogen and sulfur cycling processes dominated. Phosphorus acquisition-related activity was highest in the freshwater zone, along with dissimilatory nitrate reduction to ammonium in freshwater sediment. Activity associated with denitrification, sulfur metabolism and photosynthesis were instead highest in the brackish zone, where photosynthesis was dominated by distinct microeukaryotes in water (Cryptophyta) and sediment (diatoms). Despite microeukaryotes and archaea being rare relative to bacteria, results indicate that they contributed more to photosynthesis and ammonia oxidation, respectively.ConclusionsOur study demonstrates clear freshwater-saline and sediment-water ecosystem boundaries in an interconnected coastal aquatic system and provides a framework for understanding the relative importance of salinity, planktonic-versus-benthic habitats and nutrient availability in shaping aquatic microbial metabolic processes, particularly in tidal lagoon systems. Video abstract.

Dataset Information

Microrheology reveals microscale viscosity gradients in planktonic systems.

Publications

Microrheology reveals microscale viscosity gradients in planktonic systems.

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