title: Biomimetic cilia arrays generate simultaneous pumping and mixing regimes.
abstract: Living systems employ cilia to control and to sense the flow of fluids for many purposes, such as pumping, locomotion, feeding, and tissue morphogenesis. Beyond their use in biology, functional arrays of artificial cilia have been envisaged as a potential biomimetic strategy for inducing fluid flow and mixing in lab-on-a-chip devices. Here we report on fluid transport produced by magnetically actuated arrays of biomimetic cilia whose size approaches that of their biological counterparts, a scale at which advection and diffusion compete to determine mass transport. Our biomimetic cilia recreate the beat shape of embryonic nodal cilia, simultaneously generating two sharply segregated regimes of fluid flow: Above the cilia tips their motion causes directed, long-range fluid transport, whereas below the tips we show that the cilia beat generates an enhanced diffusivity capable of producing increased mixing rates. These two distinct types of flow occur simultaneously and are separated in space by less than 5 microm, approximately 20% of the biomimetic cilium length. While this suggests that our system may have applications as a versatile microfluidics device, we also focus on the biological implications of our findings. Our statistical analysis of particle transport identifying an enhanced diffusion regime provides novel evidence for the existence of mixing in ciliated systems, and we demonstrate that the directed transport regime is Poiseuille-Couette flow, the first analytical model consistent with biological measurements of fluid flow in the embryonic node.
authors.affiliation: Department of Physics and Astronomy, University of North Carolina, Chapel Hill, 27599, USA.
authors.forename: A R
authors.initials: AR
authors.lastname: Shields
authors.forename: B L
authors.initials: BL
authors.lastname: Fiser
authors.forename: E E
authors.initials: EE
authors.lastname: Evans
authors.forename: M R
authors.initials: MR
authors.lastname: Falvo
authors.forename: S
authors.initials: S
authors.lastname: Washburn
authors.forename: R
authors.initials: R
authors.lastname: Superfine
mesh_terms: D002923:Cilia / Q000502:physiology*; D008855:Microscopy, Electron, Scanning; D018716:Molecular Mimicry
references.citation: Science. 2007 Jan 26;315(5811):487-90
references.pmid: 17255505
references.citation: Science. 2009 Aug 28;325(5944):1131-4
references.pmid: 19628819
references.citation: Methods Cell Biol. 2009;91:265-85
references.pmid: 20409791
references.citation: Dev Dyn. 1994 Nov;201(3):260-78
references.pmid: 7881129
references.citation: Langmuir. 2008 Nov 4;24(21):12102-6
references.pmid: 18847292
references.citation: Eur Phys J E Soft Matter. 2009 Feb;28(2):231-42
references.pmid: 19030903
references.citation: Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1353-8
references.pmid: 16421211
references.citation: Biophys J. 1980 Jun;30(3):463-72
references.pmid: 6973365
references.citation: Science. 2006 Feb 3;311(5761):629-32
references.pmid: 16410488
references.citation: Nature. 2005 May 12;435(7039):172-7
references.pmid: 15889083
references.citation: Bull Math Biol. 2007 Jul;69(5):1477-510
references.pmid: 17473955
references.citation: Nano Lett. 2007 May;7(5):1428-34
references.pmid: 17419660
references.citation: Curr Opin Cell Biol. 2003 Feb;15(1):105-10
references.pmid: 12517711
references.citation: Biophys J. 2004 Mar;86(3):1863-70
references.pmid: 14990512
references.citation: Annu Rev Genomics Hum Genet. 2006;7:125-48
references.pmid: 16722803
references.citation: IMA J Math Appl Med Biol. 2001 Sep;18(3):293-325
references.pmid: 11817746
references.citation: Cell. 2005 May 20;121(4):633-644
references.pmid: 15907475
references.citation: Nano Lett. 2005 Nov;5(11):2149-54
references.pmid: 16277443
references.citation: Biophys J. 2008 Aug;95(4):L29-31
references.pmid: 18556762
references.citation: PLoS Biol. 2005 Aug;3(8):e268
references.pmid: 16035921
references.citation: Lab Chip. 2009 Dec 7;9(23):3413-21
references.pmid: 19904409
references.citation: Nat Mater. 2009 Aug;8(8):677-82
references.pmid: 19561599
references.citation: Lab Chip. 2009 Jun 7;9(11):1561-6
references.pmid: 19458863
references.citation: Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17524-9
references.pmid: 17959775
references.citation: J Membr Biol. 2001 Nov 1;184(1):71-9
references.pmid: 11687880
references.citation: Nature. 2002 Jul 4;418(6893):96-9
references.pmid: 12097914
references.citation: Lab Chip. 2008 Apr;8(4):533-41
references.pmid: 18369507
references.citation: J R Soc Interface. 2007 Feb 22;4(12):49-55
references.pmid: 17015289
references.citation: J R Soc Interface. 2008 May 6;5(22):567-73
references.pmid: 18211867
references.citation: Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):1844-7
references.pmid: 19934055
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2007 Jul;76(1 Pt 2):016313
references.pmid: 17677569
references.citation: Phys Rev Lett. 2006 Apr 21;96(15):158101
references.pmid: 16712201
references.citation: Annu Rev Physiol. 2007;69:377-400
references.pmid: 17009929
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Apr;79(4 Pt 2):046304
references.pmid: 19518330
references.citation: Proc Natl Acad Sci U S A. 2004 May 11;101(19):7234-9
references.pmid: 15118088