Universal entrainment mechanism controls contact times with motile cells

Abstract

Contact between particles and motile cells underpins a wide variety of biological processes, from nutrient capture and ligand binding, to grazing, viral infection and cell-cell communication. The window of opportunity for these interactions depends on the basic mechanism determining contact time, which is currently unknown. By combining experiments on three different species -Chlamydomonas reinhardtii, Tetraselmis subcordiforms, and Oxyrrhis marina-simulations and analytical modelling, we show that the fundamental physical process regulating proximity to a swimming microorganism is hydrodynamic particle entrainment. The resulting distribution of contact times is derived within the framework of Taylor dispersion as a competition between advection by the cell surface and microparticle diffusion, and predicts the existence of an optimal tracer size that is also observed experimentally. Spatial organisation of flagella, swimming speed, swimmer and tracer size influence entrainment features and provide trade-offs that may be tuned to optimise the estimated probabilities for microbial interactions like predation and infection. * A.M. and R.J. contributed equally to this work and are joint lead authors. A.M., R.J. and M.P. designed the study, analysed results, developed the theory, wrote the manuscript; R.J. performed the experiments; A.M. developed the model, performed simulations. † R.J. Current Address: IMEDEA, University of the Balearic Islands, Carrer de Miquel Marquès, 21 07190 Esporles, Illes Balears ‡ Correspondence: M.Polin@warwick.ac.uk (S) J above the length L (S) M at the peak of the distribution. Exponential fits to these curves give L (CR) J = 9.2 ± 0.6 µm for CR, L (TS) J = 7.4 ± 1.2 µm for TS and L (OM) J = 11.7 ± 1.4 µm for OM, while we find L (CR) M ≈ 6.7 µm, L (TS) M ≈ 8.6 µm and L (OM) M ≈ 7.5 µm. Unexpectedly, the characteristic entrainment length L (S) J

Nutrient Transport Driven by Microbial Active Carpets

“…where the dipole strength is |κ| ∼ 3v s a 2 s /4 in terms of the swimmer's speed v s and size a s [23]. The no-slip condition at the wall is accounted for using the Blake tensor B(r, r s ) formalism [62,63] [see Supplementary Information (SI) §1].…”

“…To our knowledge, the idea that accrued groups of such organisms could optimise the attraction of nutrients collectively has not been explored much in the current literature. In conjunction with that point, there is often a trade-off between swimming faster or capturing more prey [12,13,23,101,102].…”

“…The collective motion of microorganisms and active colloids has sparked great interest, as biological functions can emerge from self-organisation of local power injection [1][2][3][4][5][6][7][8][9]. To sustain these processes, self-propelled particles increase nutrient uptake [10][11][12][13] and redistribute oxygen [14] by hydrodynamically enhanced mixing [15][16][17], bioconvection [18][19][20], and particle entrainment [21][22][23][24]. The vast majority of these flow-driving swimmers accumulate at surfaces [25][26][27][28][29][30][31][32][33][34][35], at concentrations an order of magnitude larger than in the bulk [25,27,30], and thus form 'active carpets'.…”

Structural Properties of the Fluid Mixture Confined by a Semipermeable Membrane: A Density Functional Study

“…Especially in biomedical researches, the interaction of motile particles with biological membranes should be fully understood to explain the delivery of cargo to the interior of the cells [21,22]. Moreover, the mechanism for the penetration of active particles through the membrane remains an open question [23][24][25][26]. To a large extent, the fluid structure near the membrane influences the penetration of the particles [27][28][29][30].…”

State diagram of a three-sphere microswimmer in a channel

“…The strength of this design lies in the possible experimental realizations involving colloids trapped in optical tweezers 18,19 . Similar bead-model designs have been proposed involving elastic deformations of one or both of the arms [20][21][22][23][24][25][26][27] , non-collinear conformations leading to rotational motion [28][29][30][31][32] , or new models with complex swimmer bodies and external propulsion forces 33,34 . A simple model for free-swimming animalcules composed of beads, subject to periodic forces has further been considered 35,36 .…”