Self-organisation and convection of confined magnetotactic bacteria.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 08 2020
11 08 2020
Historique:
received:
15
05
2020
accepted:
27
07
2020
entrez:
13
8
2020
pubmed:
13
8
2020
medline:
19
12
2020
Statut:
epublish
Résumé
Collective motion is found at all scales in biological and artificial systems, and extensive research is devoted to describing the interplay between interactions and external cues in collective dynamics. Magnetotactic bacteria constitute a remarkable example of living organisms for which motion can be easily controlled remotely. Here, we report a new type of collective motion where a uniform distribution of magnetotactic bacteria is rendered unstable by a magnetic field. A new state of "bacterial magneto-convection" results, wherein bacterial plumes emerge spontaneously perpendicular to an interface and develop into self-sustained flow convection cells. While there are similarities to gravity driven bioconvection and the Rayleigh-Bénard instability, these rely on a density mismatch between layers of the fluids. Remarkably, here no external forces are applied on the fluid and the magnetic field only exerts an external torque aligning magnetotactic bacteria with the field. Using a theoretical model based on hydrodynamic singularities, we capture quantitatively the instability and the observed long-time growth. Bacterial magneto-convection represents a new class of collective behaviour resulting only from the balance between hydrodynamic interactions and external alignment.
Identifiants
pubmed: 32782266
doi: 10.1038/s41598-020-70270-0
pii: 10.1038/s41598-020-70270-0
pmc: PMC7419309
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13578Références
Vicsek, T. & Zafeiris, A. Collective motion. Phys. Rep.517, 71–140. https://doi.org/10.1016/j.physrep.2012.03.004 (2012).
doi: 10.1016/j.physrep.2012.03.004
Sumpter, D. J. The principles of collective animal behaviour. Philos. Trans. R. Soc. B Biol. Sci. https://doi.org/10.1098/rstb.2005.1733 (2005).
doi: 10.1098/rstb.2005.1733
Mora, T. et al. Local equilibrium in bird flocks. Nat. Phys.12, 1153. https://doi.org/10.1038/nphys3846 (2016).
doi: 10.1038/nphys3846
pubmed: 27917230
pmcid: 5131848
Lopez, U., Gautrais, J., Couzin, I. D. & Theraulaz, G. From behavioural analyses to models of collective motion in fish schools. Interface Focus2, 693–707. https://doi.org/10.1098/rsfs.2012.0033 (2012).
doi: 10.1098/rsfs.2012.0033
pubmed: 24312723
pmcid: 3499128
Trepat, X. et al. Physical forces during collective cell migration. Nat. Phys.5, 426. https://doi.org/10.1038/nphys1269 (2009).
doi: 10.1038/nphys1269
Lauga, E. & Powers, T. R. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys.72, 096601. https://doi.org/10.1088/0034-4885/72/9/096601 (2009).
doi: 10.1088/0034-4885/72/9/096601
Cisneros, L. H., Cortez, R., Dombrowski, C., Goldstein, R. E. & Kessler, J. O. Fluid dynamics of self-propelled micro-organisms, from individuals to concentrated populations. Exp. Fluids43, 737–753. https://doi.org/10.1007/s00348-007-0387-y (2007).
doi: 10.1007/s00348-007-0387-y
Koch, D. L. & Subramanian, G. Collective hydrodynamics of swimming microorganisms: living fluids. Annu. Rev. Fluid Mech.43, 637–659. https://doi.org/10.1146/annurev-fluid-121108-145434 (2011).
doi: 10.1146/annurev-fluid-121108-145434
Sokolov, A., Aranson, I. S., Kessler, J. O. & Goldstein, R. E. Concentration dependence of the collective dynamics of swimming bacteria. Phys. Rev. Lett.98, 158102. https://doi.org/10.1103/physrevlett.98.158102 (2007).
doi: 10.1103/physrevlett.98.158102
pubmed: 17501387
Riedel, I. H., Kruse, K. & Howard, J. A self-organized vortex array of hydrodynamically entrained sperm cells. Science309, 300–303. https://doi.org/10.1016/j.physrep.2012.03.004 0 (2005).
doi: 10.1126/science.1110329
pubmed: 16002619
Keller, E. F. & Segel, L. A. Model for chemotaxis. J. Theor. Biol.30, 225–234. https://doi.org/10.1016/j.physrep.2012.03.004 1 (1971).
doi: 10.1016/0022-5193(71)90050-6
pubmed: 4926701
Witman, G. B. Chlamydomonas phototaxis. Trends Cell Biol.3, 403–408. https://doi.org/10.1016/j.physrep.2012.03.004 2 (1993).
doi: 10.1016/0962-8924(93)90091-e
pubmed: 14731659
Kessler, J. O. Hydrodynamic focusing of motile algal cells. Nature313, 218. https://doi.org/10.1016/j.physrep.2012.03.004 3 (1985).
doi: 10.1038/313218a0
Pedley, T. & Kessler, J. Hydrodynamic phenomena in suspensions of swimming microorganisms. Annu. Rev. Fluid Mech.24, 313–358. https://doi.org/10.1016/j.physrep.2012.03.004 4 (1992).
doi: 10.1146/annurev.fl.24.010192.001525
Vincent, R. & Hill, N. Bioconvection in a suspension of phototactic algae. J. Fluid Mech.327, 343–371. https://doi.org/10.1016/j.physrep.2012.03.004 5 (1996).
doi: 10.1017/s0022112096008579
Childress, S., Levandowsky, M. & Spiegel, E. A. Pattern formation in a suspension of swimming microorganisms: equations and stability theory. J. Fluid Mech.69, 591–613. https://doi.org/10.1016/j.physrep.2012.03.004 6 (1975).
doi: 10.1017/s0022112075001577
Hill, N. & Pedley, T. Bioconvection. Fluid Dyn. Res.37, 1–20. https://doi.org/10.1016/j.physrep.2012.03.004 7 (2005).
doi: 10.1016/j.fluiddyn.2005.03.002
Mogami, Y., Yamane, A., Gino, A. & Baba, S. A. Bioconvective pattern formation of tetrahymena under altered gravity. J. Exp. Biol.207, 3349–3359. https://doi.org/10.1016/j.physrep.2012.03.004 8 (2004).
doi: 10.1242/jeb.01167
pubmed: 15326211
Wioland, H., Lushi, E. & Goldstein, R. E. Directed collective motion of bacteria under channel confinement. New J. Phys.18, 075002. https://doi.org/10.1016/j.physrep.2012.03.004 9 (2016).
doi: 10.1088/1367-2630/18/7/075002
Lushi, E., Wioland, H. & Goldstein, R. E. Fluid flows created by swimming bacteria drive self-organization in confined suspensions. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.1405698111 (2014).
doi: 10.1073/pnas.1405698111
pubmed: 24958878
Drescher, K., Dunkel, J., Cisneros, L. H., Ganguly, S. & Goldstein, R. E. Fluid dynamics and noise in bacterial cell-cell and cell-surface scattering. Proc. Natl. Acad. Sci.108, 10940–10945. https://doi.org/10.1073/pnas.1019079108 (2011).
doi: 10.1073/pnas.1019079108
pubmed: 21690349
Drescher, K. et al. Dancing volvox: hydrodynamic bound states of swimming algae. Phys. Rev. Lett.102, 168101. https://doi.org/10.1103/physrevlett.102.168101 (2009).
doi: 10.1103/physrevlett.102.168101
pubmed: 19518757
pmcid: 4833199
Petroff, A. P., Wu, X.-L. & Libchaber, A. Fast-moving bacteria self-organize into active two-dimensional crystals of rotating cells. Phys. Rev. Lett.114, 158102. https://doi.org/10.1103/physrevlett.114.158102 (2015).
doi: 10.1103/physrevlett.114.158102
pubmed: 25933342
Klumpp, S., Lefèvre, C. T., Bennet, M. & Faivre, D. Swimming with magnets: from biological organisms to synthetic devices. Phys. Rep.789, 1–54. https://doi.org/10.1016/j.physrep.2018.10.007 (2019).
doi: 10.1016/j.physrep.2018.10.007
Uebe, R. & Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nat. Rev. Microbiol.14, 621. https://doi.org/10.1038/nrmicro.2016.99 (2016).
doi: 10.1038/nrmicro.2016.99
pubmed: 27620945
Bazylinski, D. A. & Trubitsyn, D. Magnetotactic bacteria and magnetosomes. In Magnetic Nanoparticles in Biosensing and Medicine (eds Darton, N. J. et al.) 251–284 (Cambridge University Press, Cambridge, 2019). https://doi.org/10.1017/9781139381222.009 .
doi: 10.1017/9781139381222.009
Blakemore, R. P. Magnetotactic bacteria. Annu. Rev. Microbiol.36, 217–238. https://doi.org/10.1146/annurev.mi.36.100182.001245 (1982).
doi: 10.1146/annurev.mi.36.100182.001245
pubmed: 6128956
Lefevre, C. T., Song, T., Yonnet, J.-P. & Wu, L.-F. Characterization of bacterial magnetotactic behaviors by using a magnetospectrophotometry assay. Appl. Environ. Microbiol.75, 3835–3841. https://doi.org/10.1128/aem.00165-09 (2009).
doi: 10.1128/aem.00165-09
pubmed: 19376916
pmcid: 2698362
Alphandéry, E. Applications of magnetosomes synthesized by magnetotactic bacteria in medicine. Front. Bioeng. Biotechnol.2, 5. https://doi.org/10.3389/fbioe.2014.00005 (2014).
doi: 10.3389/fbioe.2014.00005
pubmed: 25152880
pmcid: 4126476
Felfoul, O. et al. Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nat. Nanotechnol.11, 941. https://doi.org/10.1038/nnano.2016.137 (2016).
doi: 10.1038/nnano.2016.137
pubmed: 27525475
pmcid: 6094936
Pierce, C. et al. Tuning bacterial hydrodynamics with magnetic fields. Phys. Rev. E95, 062612 (2017).
doi: 10.1103/PhysRevE.95.062612
Pierce, C. et al. Hydrodynamic interactions, hidden order, and emergent collective behavior in an active bacterial suspension. Phys. Rev. Lett.121, 188001. https://doi.org/10.1103/physreve.95.062612 (2018).
doi: 10.1103/physreve.95.062612
pubmed: 30444412
Belovs, M., Livanovics, R. & Cēbers, A. Synchronized rotation in swarms of magnetotactic bacteria. Phys. Rev. E96, 042408. https://doi.org/10.1103/physreve.96.042408 (2017).
doi: 10.1103/physreve.96.042408
pubmed: 29347499
Waisbord, N., Lefèvre, C. T., Bocquet, L., Ybert, C. & Cottin-Bizonne, C. Destabilization of a flow focused suspension of magnetotactic bacteria. Phys. Rev. Fluids1, 053203. https://doi.org/10.1103/physrevfluids.1.053203 (2016).
doi: 10.1103/physrevfluids.1.053203
Meng, F., Matsunaga, D. & Golestanian, R. Clustering of magnetic swimmers in a poiseuille flow. Phys. Rev. Lett.120, 188101. https://doi.org/10.1103/physrevlett.120.188101 (2018).
doi: 10.1103/physrevlett.120.188101
pubmed: 29775341
Vincenti, B. et al. Magnetotactic bacteria in a droplet self-assemble into a rotary motor. Nat. Commun.10, 1–8. https://doi.org/10.1017/9781139381222.009 0 (2019).
doi: 10.1038/s41467-019-13031-6
Normand, C., Pomeau, Y. & Velarde, M. G. Convective instability: a physicists approach. Rev. Mod. Phys.49, 581. https://doi.org/10.1103/RevModPhys.49.581 (1977).
doi: 10.1103/RevModPhys.49.581
Matsunaga, T., Sakaguchi, T. & Tadakoro, F. Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl. Microbiol. Biotechnol.35, 651–655. https://doi.org/10.1007/bf00169632 (1991).
doi: 10.1007/bf00169632
Wolfe, R., Thauer, R. & Pfennig, N. A capillary racetrack method for isolation of magnetotactic bacteria. FEMS Microbiol. Lett.3, 31–35. https://doi.org/10.1111/j.1574-6968.1987.tb02335.x (1987).
doi: 10.1111/j.1574-6968.1987.tb02335.x
Murat, D. et al. Opposite and coordinated rotation of amphitrichous flagella governs oriented swimming and reversals in a magnetotactic spirillum. J. Bacteriol.197, 3275–3282. https://doi.org/10.1128/jb.00172-15 (2015).
doi: 10.1128/jb.00172-15
pubmed: 26240070
pmcid: 4573727
Cortez, R. The method of regularized stokeslets. SIAM J. Sci. Comput.23, 1204–1225. https://doi.org/10.1137/s106482750038146x (2001).
doi: 10.1137/s106482750038146x
Drescher, K., Goldstein, R. E., Michel, N., Polin, M. & Tuval, I. Direct measurement of the flow field around swimming microorganisms. Phys. Rev. Lett.105, 168101. https://doi.org/10.1103/PhysRevLett.105.168101 (2010).
doi: 10.1103/PhysRevLett.105.168101
pubmed: 21231017
Costanzo, A., Di Leonardo, R., Ruocco, G. & Angelani, L. Transport of self-propelling bacteria in micro-channel flow. J. Phys. Condens. Matter24, 065101. https://doi.org/10.1088/0953-8984/24/6/065101 (2012).
doi: 10.1088/0953-8984/24/6/065101
pubmed: 22231718
Ainley, J., Durkin, S., Embid, R., Boindala, P. & Cortez, R. The method of images for regularized stokeslets. J. Comput. Phys.227, 4600–4616. https://doi.org/10.1016/j.jcp.2008.01.032 (2008).
doi: 10.1016/j.jcp.2008.01.032
Blake, J. A note on the image system for a stokeslet in a no-slip boundary. Math. Proc. Cambr. Philos. Soc.70, 303–310. https://doi.org/10.1017/s0305004100049902 (1971).
doi: 10.1017/s0305004100049902
Squires, T. M. & Brenner, M. P. Like-charge attraction and hydrodynamic interaction. Phys. Rev. Lett.85, 4976. https://doi.org/10.1103/physrevlett.85.4976 (2000).
doi: 10.1103/physrevlett.85.4976
pubmed: 11102165
Le Nagard, L., Morillo-López, V., Fradin, C. & Bazylinski, D. A. Growing magnetotactic bacteria of the genus magnetospirillum: strains msr-1, amb-1 and ms-1. J. Vis. Exper. https://doi.org/10.3791/58536 (2018).
doi: 10.3791/58536
Le Nagard, L. et al. Misalignment between the magnetic dipole moment and the cell axis in the magnetotactic bacterium magnetospirillum magneticum amb-1. Phys. Biol.16, 066008. https://doi.org/10.1088/1478-3975/ab2858 (2019).
doi: 10.1088/1478-3975/ab2858
pubmed: 31181559
Thielicke, W. & Stamhuis, E. J. Pivlab-towards user-friendly, affordable and accurate digital particle image velocimetry in matlab. J. Open Res. Softw. https://doi.org/10.5334/jors.bl (2014).
doi: 10.5334/jors.bl