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      Fluid viscoelasticity promotes collective swimming of sperm

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          Abstract

          From flocking birds to swarming insects, interactions of organisms large and small lead to the emergence of collective dynamics. Here, we report striking collective swimming of bovine sperm in dynamic clusters, enabled by the viscoelasticity of the fluid. Sperm oriented in the same direction within each cluster, and cluster size and cell-cell alignment strength increased with viscoelasticity of the fluid. In contrast, sperm swam randomly and individually in Newtonian (nonelastic) fluids of low and high viscosity. Analysis of the fluid motion surrounding individual swimming sperm indicated that sperm-fluid interaction was facilitated by the elastic component of the fluid. In humans, as well as cattle, sperm are naturally deposited at the entrance to the cervix and must swim through viscoelastic cervical mucus and other mucoid secretions to reach the site of fertilization. Collective swimming induced by elasticity may thus facilitate sperm migration and contribute to successful fertilization. We note that almost all biological fluids (e.g. mucus and blood) are viscoelastic in nature, and this finding highlights the importance of fluid elasticity in biological function.

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          Micro- and macrorheology of mucus.

          Samuel Lai, Ying-Ying Wang, Denis Wirtz … (2009)
          Mucus is a complex biological material that lubricates and protects the human lungs, gastrointestinal (GI) tract, vagina, eyes, and other moist mucosal surfaces. Mucus serves as a physical barrier against foreign particles, including toxins, pathogens, and environmental ultrafine particles, while allowing rapid passage of selected gases, ions, nutrients, and many proteins. Its selective barrier properties are precisely regulated at the biochemical level across vastly different length scales. At the macroscale, mucus behaves as a non-Newtonian gel, distinguished from classical solids and liquids by its response to shear rate and shear stress, while, at the nanoscale, it behaves as a low viscosity fluid. Advances in the rheological characterization of mucus from the macroscopic to nanoscopic levels have contributed critical understanding to mucus physiology, disease pathology, and the development of drug delivery systems designed for use at mucosal surfaces. This article reviews the biochemistry that governs mucus rheology, the macro- and microrheology of human and laboratory animal mucus, rheological techniques applied to mucus, and the importance of an improved understanding of the physical properties of mucus to advancing the field of drug and gene delivery.
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            Emergence of macroscopic directed motion in populations of motile colloids

            Antoine Bricard, Jean-Baptiste Caussin, Nicolas Desreumaux … (2013)
            From the formation of animal flocks to the emergence of coordinated motion in bacterial swarms, populations of motile organisms at all scales display coherent collective motion. This consistent behaviour strongly contrasts with the difference in communication abilities between the individuals. On the basis of this universal feature, it has been proposed that alignment rules at the individual level could solely account for the emergence of unidirectional motion at the group level. This hypothesis has been supported by agent-based simulations. However, more complex collective behaviours have been systematically found in experiments, including the formation of vortices, fluctuating swarms, clustering and swirling. All these (living and man-made) model systems (bacteria, biofilaments and molecular motors, shaken grains and reactive colloids) predominantly rely on actual collisions to generate collective motion. As a result, the potential local alignment rules are entangled with more complex, and often unknown, interactions. The large-scale behaviour of the populations therefore strongly depends on these uncontrolled microscopic couplings, which are extremely challenging to measure and describe theoretically. Here we report that dilute populations of millions of colloidal rolling particles self-organize to achieve coherent motion in a unique direction, with very few density and velocity fluctuations. Quantitatively identifying the microscopic interactions between the rollers allows a theoretical description of this polar-liquid state. Comparison of the theory with experiment suggests that hydrodynamic interactions promote the emergence of collective motion either in the form of a single macroscopic 'flock', at low densities, or in that of a homogenous polar phase, at higher densities. Furthermore, hydrodynamics protects the polar-liquid state from the giant density fluctuations that were hitherto considered the hallmark of populations of self-propelled particles. Our experiments demonstrate that genuine physical interactions at the individual level are sufficient to set homogeneous active populations into stable directed motion.
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              Spontaneous motion in hierarchically assembled active matter

              Tim Sanchez, Daniel T. N. Chen, Stephen J. DeCamp … (2012)
              With exquisite precision and reproducibility, cells orchestrate the cooperative action of thousands of nanometer-sized molecular motors to carry out mechanical tasks at much larger length scales, such as cell motility, division and replication 1 . Besides their biological importance, such inherently non-equilibrium processes are an inspiration for developing biomimetic active materials from microscopic components that consume energy to generate continuous motion 2–4 . Being actively driven, these materials are not constrained by the laws of equilibrium statistical mechanics and can thus exhibit highly sought-after properties such as autonomous motility, internally generated flows and self-organized beating 5–7 . Starting from extensile microtubule bundles, we hierarchically assemble active analogs of conventional polymer gels, liquid crystals and emulsions. At high enough concentration, microtubules form a percolating active network characterized by internally driven chaotic flows, hydrodynamic instabilities, enhanced transport and fluid mixing. When confined to emulsion droplets, 3D networks spontaneously adsorb onto the droplet surfaces to produce highly active 2D nematic liquid crystals whose streaming flows are controlled by internally generated fractures and self-healing, as well as unbinding and annihilation of oppositely charged disclination defects. The resulting active emulsions exhibit unexpected properties, such as autonomous motility, which are not observed in their passive analogues. Taken together, these observations exemplify how assemblages of animate microscopic objects exhibit collective biomimetic properties that are starkly different from those found in materials assembled from inanimate building blocks, challenging us to develop a theoretical framework that would allow for a systematic engineering of their far-from-equilibrium material properties.
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                Author and article information

                Contributors
                Chih-kuan Tung: ctung@ncat.edu
                Mingming Wu: mw272@cornell.edu
                Susan S. Suarez: sss7@cornell.edu
                Journal
                Journal ID (nlm-ta): Sci Rep
                Journal ID (iso-abbrev): Sci Rep
                Title: Scientific Reports
                Publisher: Nature Publishing Group UK (London )
                ISSN (Electronic): 2045-2322
                Publication date (Electronic): 9 June 2017
                Publication date PMC-release: 9 June 2017
                Publication date Collection: 2017
                Volume: 7
                Electronic Location Identifier: 3152
                Affiliations
                [1 ]ISNI 000000041936877X, GRID grid.5386.8, Department of Biomedical Sciences, , Cornell University, ; Ithaca, NY 14853 USA
                [2 ]ISNI 000000041936877X, GRID grid.5386.8, Department of Biological and Environmental Engineering, , Cornell University, ; Ithaca, NY 14853 USA
                [3 ]ISNI 0000 0001 0287 4439, GRID grid.261037.1, Department of Physics, , North Carolina A&T State University, ; Greensboro, NC 27411 USA
                [4 ]GRID grid.466925.a, , Mitsubishi Electric Research Laboratories, ; Boston, MA 02139 USA
                Article
                Publisher ID: 3341
                DOI: 10.1038/s41598-017-03341-4
                PMC ID: 5466690
                PubMed ID: 28600487
                SO-VID: d091aa20-9a43-418f-bbe1-aafc66c898f8
                Copyright © © The Author(s) 2017
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 2 February 2017
                Date accepted : 26 April 2017
                Categories
                Subject: Article
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                issue-copyright-statement © The Author(s) 2017

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