Microrheology reveals microscale viscosity gradients in planktonic systems

Guadayol, Òscar; Mendonça, Tânia; Segura-Noguera, Mariona; Wright, Amanda J.; Tassieri, Manlio; Humphries, Stuart

doi:10.1101/2020.04.09.033464

Cited by 5 publications

(4 citation statements)

References 39 publications

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“…Third, the adoption of swimming patterns with a reversal phase and long runs, which are prevalent among marine bacteria (Johansen et al, 2002) can also maximize nutrient exposure around a phycosphere (Figure 4). And finally, the existence of a viscous layer of exopolymers around a phytoplankton cell may minimize the volcano effect (Guadayol et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

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Optimal cell length for exploration and exploitation in chemotactic planktonic bacteria

Guadayol,

Schuech,

Humphries

2023

Preprint

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Elongated morphologies are prevalent among marine motile bacterioplankton. This is often attributed to enhanced chemotactic ability, but how long is best? We hypothesized the existence of an optimal cell length for efficient chemotaxis resulting from shape-imposed physical constraints acting on the trade-off between rapid exploration versus efficient exploitation of nutrient sources. To test this hypothesis, we first evaluated the chemotactic performance of elongated cephalexin-treatedEscherichia colitowards α-methyl-aspartate in an agarose-based microfluidic device that creates linear, stable and quiescent chemical gradients. Our experiments showed that cells of intermediate lengths aggregated most tightly to the chemoattractant source. We then replicated these experimental results with Individual Based Model (IBM) simulations. A sensitivity analysis of the IBM allowed us to gain mechanistic insights into which parameters drive this trend and showed that the poor chemotactic performance of very short cells is caused by loss of directionality, whereas long cells are penalized by brief, slow runs. Finally, we evaluated the chemotactic performance of cells of different length with IBM simulations of a phycosphere – a hotspot of microbial interactions in the ocean. Results indicated that long cells swimming in a run-and-reverse pattern with extended runs and moderate speeds are most efficient at harvesting nutrients in this microenvironment. The combination of microfluidic experiments and IBMs proves thus to be a powerful tool for untangling the physical constraints that motile bacteria are facing in the ocean.

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Section: Discussionmentioning

confidence: 99%

“…6). And finally, the existence of a viscous layer of exopolymers around a phytoplankton cell may minimize the volcano effect (Guadayol et al 2021).…”

Section: Ecological and Evolutionary Implicationsmentioning

confidence: 99%

Optimal cell length for exploration and exploitation in chemotactic planktonic bacteria

Guadayol,

Schuech,

Humphries

2023

Preprint

Self Cite

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“…Viscosity in such environments increases rapidly with the size of the diffusing object, which can suppress diffusive encounters for larger objects, making them relevant only at the nanometre scale (broken blue line in figure 2b). Suppression of diffusion in mucus is a first-line protection mechanism against foreign pathogens [53], in bacterial extracellular polymeric substances it can protect bacteria from external deleterious compounds [55] and has been observed outside phytoplankton cells [56]. royalsocietypublishing.org/journal/rsfs Interface Focus 13: 20220059…”

Section: Encounter Mechanisms In Aquatic Systemsmentioning

confidence: 99%

Encounter rates prime interactions between microorganisms

et al. 2023

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Properties of microbial communities emerge from the interactions between microorganisms and between microorganisms and their environment. At the scale of the organisms, microbial interactions are multi-step processes that are initiated by cell–cell or cell–resource encounters. Quantification and rational design of microbial interactions thus require quantification of encounter rates. Encounter rates can often be quantified through encounter kernels—mathematical formulae that capture the dependence of encounter rates on cell phenotypes, such as cell size, shape, density or motility, and environmental conditions, such as turbulence intensity or viscosity. While encounter kernels have been studied for over a century, they are often not sufficiently considered in descriptions of microbial populations. Furthermore, formulae for kernels are known only in a small number of canonical encounter scenarios. Yet, encounter kernels can guide experimental efforts to control microbial interactions by elucidating how encounter rates depend on key phenotypic and environmental variables. Encounter kernels also provide physically grounded estimates for parameters that are used in ecological models of microbial populations. We illustrate this encounter-oriented perspective on microbial interactions by reviewing traditional and recently identified kernels describing encounters between microorganisms and between microorganisms and resources in aquatic systems.

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“…External forces or torques acting upon cells can also mechanically guide microbes toward favorable conditions: Gravitational fields orient eukaryotic marine microbes within the water column through gravitaxis 18,19 , and magnetic fields serve as a compass for bacteria in sedimentary environments via magnetotaxis 20 . Additionally, swimming cells are widely known to respond to gradients in fluid viscosity 5 , which can vary broadly in scale and strength 21,22 . Mucus layers (≈1 mm thick 23,24 ) exhibit viscosities as low as 2 cP in corals and sessile marine organisms 25 , while in mammals they can range from 5 cP in the trachea to >1,000 cP in the gastrointestinal tract 22 .…”

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Viscophobic turning dictates microalgae transport in viscosity gradients

Stehnach

Waisbord

Walkama

et al. 2020

Preprint

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Gradients in fluid viscosity characterize microbiomes ranging from mucus layers on marine organisms and human viscera to biofilms. While such environments are widely recognized for their protective effects against pathogens and their ability to influence cell motility, the physical mechanisms controlling cell transport in viscosity gradients remain elusive, primarily due to a lack of quantitative observations. Through microfluidic experiments with a model biflagellated microalga (Chlamydomonas reinhardtii), we show that cells accumulate in high viscosity regions of weak gradients as expected, stemming from their locally reduced swimming speed. However, this expectation is subverted in strong viscosity gradients, where a novel viscophobic turning motility - consistent with a flagellar thrust imbalance - reorients the swimmers down the gradient and causes striking accumulation in low viscosity zones. Corroborated by Langevin simulations and a three-point force model of cell propulsion, our results illustrate how the competition between viscophobic turning and viscous slowdown ultimately dictates the fate of population scale microbial transport in viscosity gradients.

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Microrheology reveals microscale viscosity gradients in planktonic systems

Cited by 5 publications

References 39 publications

Optimal cell length for exploration and exploitation in chemotactic planktonic bacteria

Optimal cell length for exploration and exploitation in chemotactic planktonic bacteria

Encounter rates prime interactions between microorganisms

Viscophobic turning dictates microalgae transport in viscosity gradients

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