Rapid Multi-plane Phase-contrast Microscopy Reveals Torsional Dynamics in Flagellar Motion

Overview

Journal Biomed Opt Express

Specialty Radiology

Date 2021 Jul 5

PMID 34221652

Citations 7

Authors

Soheil Mojiri

Sebastian Isbaner

Steffen Muhle

Hongje Jang

Albert Johann Bae

Ingo Gregor

Azam Gholami

Jorg Enderlein

Affiliations

Soon will be listed here.

Abstract

High speed volumetric optical microscopy is an important tool for observing rapid processes in living cells or for real-time tracking of sub-cellular components. However, the 3D imaging capability often comes at the price of a high technical complexity of the imaging system and/or the requirement of demanding image analysis. Here, we propose a combination of conventional phase-contrast imaging with a customized multi-plane beam-splitter for enabling simultaneous acquisition of images in eight different focal planes. Our method is technically straightforward and does not require complex post-processing image analysis. We apply our multi-plane phase-contrast microscope to the real-time observation of the fast motion of reactivated axonemes with sub-µm spatial and 4 ms temporal resolution. Our system allows us to observe not only bending but also the three-dimensional torsional dynamics of these micro-swimmers.

Citing Articles

Swimming by Spinning: Spinning-Top Type Rotations Regularize Sperm Swimming Into Persistently Progressive Paths in 3D.

Ren X, Bloomfield-Gadelha H Adv Sci (Weinh). 2024; 12(6):e2406143.

PMID: 39696833 PMC: 11809349. DOI: 10.1002/advs.202406143.

Bi-Plane Multicolor Scanning Illumination Microscopy with Multispot Excitation and a Distorted Diffraction Grating.

Li S, Zhang Y, Liao Z, Tian Z, Hashim H, Zeng Y Biosensors (Basel). 2024; 14(11).

PMID: 39590009 PMC: 11592293. DOI: 10.3390/bios14110550.

Fluorescence Microscopy: a statistics-optics perspective.

Fazel M, Grussmayer K, Ferdman B, Radenovic A, Shechtman Y, Enderlein J ArXiv. 2023; .

PMID: 37064525 PMC: 10104198.

Flagellum-driven cargoes: Influence of cargo size and the flagellum-cargo attachment geometry.

Bae A, Ahmad R, Bodenschatz E, Pumir A, Gholami A PLoS One. 2023; 18(3):e0279940.

PMID: 36897856 PMC: 10004597. DOI: 10.1371/journal.pone.0279940.

Generation of ciliary beating by steady dynein activity: the effects of inter-filament coupling in multi-filament models.

Woodhams L, Shen Y, Bayly P J R Soc Interface. 2022; 19(192):20220264.

PMID: 35857924 PMC: 9257587. DOI: 10.1098/rsif.2022.0264.

References

Geissbuehler S, Sharipov A, Godinat A, Bocchio N, Sandoz P, Huss A . Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging. Nat Commun. 2014; 5:5830. PMC: 4284648. DOI: 10.1038/ncomms6830. View

Abrahamsson S, McQuilken M, Mehta S, Verma A, Larsch J, Ilic R . MultiFocus Polarization Microscope (MF-PolScope) for 3D polarization imaging of up to 25 focal planes simultaneously. Opt Express. 2015; 23(6):7734-54. PMC: 5802244. DOI: 10.1364/OE.23.007734. View

Abrahamsson S, Chen J, Hajj B, Stallinga S, Katsov A, Wisniewski J . Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat Methods. 2012; 10(1):60-3. PMC: 4161287. DOI: 10.1038/nmeth.2277. View

Hansen J, Gong A, Wachten D, Pascal R, Turpin A, Jikeli J . Multifocal imaging for precise, label-free tracking of fast biological processes in 3D. Nat Commun. 2021; 12(1):4574. PMC: 8319204. DOI: 10.1038/s41467-021-24768-4. View

Lin J, Okada K, Raytchev M, Smith M, Nicastro D . Structural mechanism of the dynein power stroke. Nat Cell Biol. 2014; 16(5):479-85. PMC: 4102432. DOI: 10.1038/ncb2939. View

Louis B, Camacho R, Bresoli-Obach R, Abakumov S, Vandaele J, Kudo T . Fast-tracking of single emitters in large volumes with nanometer precision. Opt Express. 2020; 28(19):28656-28671. DOI: 10.1364/OE.401557. View

Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N . Computer control of microscopes using µManager. Curr Protoc Mol Biol. 2010; Chapter 14:Unit14.20. PMC: 3065365. DOI: 10.1002/0471142727.mb1420s92. View

Bui K, Yagi T, Yamamoto R, Kamiya R, Ishikawa T . Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J Cell Biol. 2012; 198(5):913-25. PMC: 3432765. DOI: 10.1083/jcb.201201120. View

Kemao Q . Windowed Fourier transform for fringe pattern analysis. Appl Opt. 2004; 43(13):2695-702. DOI: 10.1364/ao.43.002695. View

10.

Brokaw C . Computer simulation of flagellar movement VIII: coordination of dynein by local curvature control can generate helical bending waves. Cell Motil Cytoskeleton. 2002; 53(2):103-24. DOI: 10.1002/cm.10067. View

11.

Elgeti J, Kaupp U, Gompper G . Hydrodynamics of sperm cells near surfaces. Biophys J. 2010; 99(4):1018-26. PMC: 2920720. DOI: 10.1016/j.bpj.2010.05.015. View

12.

Witman G . Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 1986; 134:280-90. DOI: 10.1016/0076-6879(86)34096-5. View

13.

Itano M, Bleck M, Johnson D, Simon S . Readily Accessible Multiplane Microscopy: 3D Tracking the HIV-1 Genome in Living Cells. Traffic. 2015; 17(2):179-86. PMC: 4729623. DOI: 10.1111/tra.12347. View

14.

Abrahamsson S, Ilic R, Wisniewski J, Mehl B, Yu L, Chen L . Multifocus microscopy with precise color multi-phase diffractive optics applied in functional neuronal imaging. Biomed Opt Express. 2016; 7(3):855-69. PMC: 4866461. DOI: 10.1364/BOE.7.000855. View

15.

Montresor S, Memmolo P, Bianco V, Ferraro P, Picart P . Comparative study of multi-look processing for phase map de-noising in digital Fresnel holographic interferometry. J Opt Soc Am A Opt Image Sci Vis. 2019; 36(2):A59-A66. DOI: 10.1364/JOSAA.36.000A59. View

16.

Abrahamsson S, Blom H, Agostinho A, Jans D, Jost A, Muller M . Multifocus structured illumination microscopy for fast volumetric super-resolution imaging. Biomed Opt Express. 2017; 8(9):4135-4140. PMC: 5611928. DOI: 10.1364/BOE.8.004135. View

17.

Sartori P, Geyer V, Howard J, Julicher F . Curvature regulation of the ciliary beat through axonemal twist. Phys Rev E. 2016; 94(4-1):042426. DOI: 10.1103/PhysRevE.94.042426. View

18.

Lin J, Nicastro D . Asymmetric distribution and spatial switching of dynein activity generates ciliary motility. Science. 2018; 360(6387). PMC: 6640125. DOI: 10.1126/science.aar1968. View

19.

Mojiri S, Isbaner S, Muhle S, Jang H, Bae A, Gregor I . Rapid multi-plane phase-contrast microscopy reveals torsional dynamics in flagellar motion. Biomed Opt Express. 2021; 12(6):3169-3180. PMC: 8221972. DOI: 10.1364/BOE.419099. View

20.

Hyams J, Borisy G . Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro. J Cell Sci. 1978; 33:235-53. DOI: 10.1242/jcs.33.1.235. View