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Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics

Key Points

  • Motility is one of the most dynamic features of the microbial world. The ability to swim in liquid or crawl on surfaces frequently governs how microorganisms interact with their physical and chemical environment, and underpins a myriad of microbial processes.

  • The ability to resolve temporal dynamics through time-lapse imaging and the precise control of the physicochemical microenvironment afforded by microfluidics offer powerful new opportunities to study the motility adaptations of microorganisms and thereby further our understanding of their ecology.

  • Dynamic microscale imaging has shown how individual swimming microorganisms disturb the fluid in their surroundings, and how this hydrodynamic signature affects their motility near surfaces as well as in dense-cell suspensions. The same technique has revealed new motility adaptations of microorganisms, in particular the flicking behaviour used by many marine bacteria to turn.

  • Tracking swimming microorganisms in precisely controlled chemical gradients created using microfluidic devices has revealed that microorganisms are capable of refined rescaling responses in their chemotactic behaviour, which ensure high performance under a wide range of environmental conditions. In the environment, and in particular in the ocean, the strong chemotactic responses of microorganisms can be important in determining associations with larger organisms, consuming dissolved organic matter and ultimately affecting biogeochemistry.

  • An important but often neglected set of microbial interactions are those between cells and their physical environment — chiefly, surfaces and fluid flow. Recent imaging-based microfluidic studies have revealed that hydrodynamic and surface-induced forces can strongly bias the direction of migration of microorganisms. These forces, for example, induce upstream swimming or preferential cell accumulations in regions of high-velocity gradients, affecting the transport of microorganisms and the colonization of surfaces that leads to biofilm formation.

Abstract

Motility is one of the most dynamic features of the microbial world. The ability to swim or crawl frequently governs how microorganisms interact with their physical and chemical environments, and underpins a myriad of microbial processes. The ability to resolve temporal dynamics through time-lapse video microscopy and the precise control of the physicochemical microenvironment afforded by microfluidics offer powerful new opportunities to study the many motility adaptations of microorganisms and thereby further our understanding of their ecology. In this Review, we outline recent insights into the motility strategies of microorganisms brought about by these techniques, including the hydrodynamic signature of microorganisms, their locomotion mechanics, chemotaxis, their motility near and on surfaces, swimming in moving fluids and motility in dense microbial suspensions.

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Figure 1: Microbial flow fields and motility mechanics.
Figure 2: Microbial chemotaxis.
Figure 3: Microbial interactions with surfaces.
Figure 4: Microbial motility in moving fluids.
Figure 5: Upstream motility and downstream bending in flowing fluids.

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Acknowledgements

The authors gratefully acknowledge support through a Samsung Scholarship (to K.S.), a Human Frontier Science Program (HFSP) Cross-Disciplinary Fellowship (to D.R.B.) and a Marine Microbiology Initiative Investigator Award from the Gordon and Betty Moore Foundation (GBMF3783, to R.S.). The authors also thank G. Gorick for help with some of the figures.

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Correspondence to Roman Stocker.

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Supplementary information

Supplementary information S1 (movie)

Motility mechanics. Many marine bacteria reorient by a 'flick', an off-axis deformation of the flagellum that enables bacteria with a single flagellum to change their direction of swimming. This video shows the flick process of Vibrio alginolyticus (see also Fig. 1c–f), recorded using high-speed, high-intensity dark-field microscopy (40X objective lens, 420 frames s−1). On the left is the raw video, on the right a processed version showing the (single, polar) flagellum in magenta. Note the buckling of the flagellum (see also Fig. 1e, 50–70 ms) shortly after the reversal in swimming direction ( Fig. 1e, 20 ms). This movie is reproduced from Ref. 2, Nature Publishing Group. (MOV 8234 kb)

Supplementary information S2 (movie)

Chemotaxis. Using chemotaxis, natural marine bacteria can cluster around photosynthetic diatoms, here Chaetoceros affinis, in response to the gradients in dissolved organic matter originating from the diatom (see also Fig. 2a). Courtesy of Steven Smriga and Vicente Fernandez, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, 8093 Zurich, Switzerland. (MOV 1950 kb)

Supplementary information S3 (movie)

Surface motility. Two-point tracking of a single Pseudomonas aeruginosa bacterium as it crawls along a surface (see also Fig. 3d). Markers 1 and 2 represent the leading and trailing poles, respectively. The video corresponds to 700 s in real time, with playback sped up by a factor of 40. This movie is reproduced with permission from Ref. 6, National Academy of Sciences. (AVI 6123 kb)

Supplementary information S4 (movie)

Motility in flow. Trajectory of a smooth-swimming Bacillus subtilis bacterium in a microfluidic channel (see also Fig. 4b). The raw video of the motile cell is shown first, followed by a replay in which the tracked cell trajectory (green) and position and orientation (red) are included. The flow in the channel is from left to right, and the video is recorded in the reference frame comoving with the mean speed of the flow (mean speed = 500 μm s−1, mean absolute shear rate = 2.5 s−1). The looped trajectory results from the velocity gradient generating a hydrodynamic torque that continually reorients the cell while it swims. The video was captured at 70.6 frames s−1 using dark-field microscopy, and is replayed 1.7 times slower than real time. This movie is reproduced from Ref. 63, Nature Publishing Group. (AVI 452 kb)

PowerPoint slides

Glossary

Soft lithography

A technique used for fabricating, at the micrometre to nanometre scale, features in elastomeric materials such as polydimethylsiloxane (PDMS).

Defocused microscopy

A microscopic imaging technique whereby the distance of a microorganism ('into the plane') from the imaging plane is determined by matching its defocused ring size with a reference stack.

Particle image velocimetry

(PIV). A method to measure the velocity field of a fluid based on the motion of many small passive tracer particles.

Thermal fluctuations

A source of random noise in a system at equilibrium that induces diffusion of small particles.

Rotational diffusion

For a swimming microorganism, this describes the continuous, random changes in swimming direction owing to thermal fluctuations (passive rotational diffusion) or to intrinsic imperfections (for example, wobbling) in the locomotion system (termed active rotational diffusion).

Buckling

A sudden sideways failure of a structure subjected to compressive load.

Logarithmic sensing

A sensing property in which cells respond to the relative gradient in a stimulus, C/C, in which C is the magnitude and C is the gradient magnitude of the stimulus.

Förster resonance energy transfer

(FRET). A mechanism quantifying energy transfer between two light-sensitive molecules in which excitation is transferred from a donor molecule to an acceptor molecule without emission of a photon. In chemotactic transduction studies of Escherichia coli, FRET is used to measure the level of the chemotaxis signalling molecule phospho-CheY (CheYP) that controls flagellar reversals.

Chemokinesis

The modulation of swimming speed in response to changes in the concentration of a chemical.

Twitching

Crawling motion of bacteria on surfaces by means of pili.

Digital holographic microscopy

A microscopic imaging technique where the position of an object 'into the plane' is encoded by the interference fringes it creates by diffracting light and can be reconstructed in post-processing to yield 3D information.

Torque

The moment of the forces that act on an object, which quantifies their tendency to rotate the object.

Mannose-sensitive haemagglutinin pili

(MSHA pili). One of three type IV pili, which play an important part in biofilm formation.

Type IV pili

Thin, hair-like appendages present on the surface of many bacteria, involved in adherence to and motility on substrates.

Jeffery orbit

Periodic rotational trajectory of an elongated particle (in this case, a microorganism) in a fluid velocity gradient, in which the angular speed varies with orientation relative to the flow.

Laminar flow

Fluid motion devoid of turbulence and typically occurring as a smooth, orderly flow.

Biofilm streamers

Conglomerates of cells and cell-secreted polymeric substances (exopolysaccharide) that are attached by one end to a surface and otherwise suspended in the flow. These biofilm structures exist in topographically complex environments exposed to fluid flow.

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Son, K., Brumley, D. & Stocker, R. Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics. Nat Rev Microbiol 13, 761–775 (2015). https://doi.org/10.1038/nrmicro3567

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