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DRAFT A biological tissue-inspired tunable photonic fluid Xinzhi Li, Amit Das, and Dapeng Bi 1 Department of Physics, Northeastern University, MA 02115, USA This manuscript was compiled on January 30, 2018 Inspired by how cells pack in dense biological tissues, we design 2D and 3D amorphous materials which possess a complete photonic band gap. A physical parameter based on how cells adhere with one another and regulate their shapes can continuously tune the photonic band gap size as well as the bulk mechanical properties of the material. The material can be tuned to go through a solid-fluid phase transition characterized by a vanishing shear modulus. Remarkably, the photonic band gap per- sists in the fluid phase, giving rise to a photonic fluid that is robust to flow and rearrangements. Experimentally this design should lead to the engineering of self-assembled non-rigid photonic structures with pho- tonic band gaps that can be controlled in real time via mechanical and thermal tuning. amorphous materials | photonic band gap | photonic fluid P hotonic band gap (PBG) materials have remained an intense focus of research since their introduction (1, 2) and have given rise to a wide range of applications such as radiation sources (3), sensors, wave guides, solar arrays and optical computer chips (4). Most studies have been devoted to the design and optimization of photonic crystals – a periodic arrangement of dielectric scattering materials that have photonic bands due to multiple Bragg scatterings. However, periodicity is not necessary to form PBGs and amorphous structures with PBGs (58) can offer many advantages over their crystalline counterparts (7). For example amorphous photonic ma- terials can exhibit band gaps that are directionally isotropic (9, 10) and are more robust to defects and errors in fabrication (7). Currently there are few existing protocols for designing amorphous photonic materials. They include structures obtained from a dense packing of spheres (3D) or disks (2D) (5, 1114), tailor-designed protocols that generate hyperuniform patterns (9, 10, 14) and spinodal-decomposed structures (15, 16). While these designs yield PBGs, such structures are typically static, rigid constructions that do not allow tuning of photonic properties in real time and are unstable to structural changes such as large scale flows and positional rearrangements. In this work, we propose a new design for amorphous 2D and 3D PBG materials that is inspired by how cells pack in dense tissues in biology. We generate structures that exhibit broad PBGs based on a simple model that has been shown to describe cell shapes and tissue mechanical behavior. An advantage of this design is that the photonic and mechanical properties of the material are closely coupled. The material can also be tuned to undergo a density-independent solid-fluid transition and the PBG persists well into the fluid phase. With recent advances in tunable self-assembly of nanoparticles or biomimetic emulsion droplets, this design can be used to create a ‘photonic fluid’. Results Model for epithelial cell packing in 2D. When epithelial and en- dothelial cells pack densely in 2D to form a confluent monolayer, the structure of the resulting tissue can be described by a polygo- nal tiling (17). A great variety of cell shape structures have been observed in tissue monolayers, ranging from near-regular tiling of cells that resembles a dry foam or honeycomb lattice (18) to highly irregular tilings of elongated cells (19). To better understand how cell shapes arise from cell-level interactions, a framework called the Self- Propelled Voronoi (SPV) model has been developed recently (20). In the SPV model, the basic degrees of freedom are the set of 2D cell centers {r i } and cell shapes are given by the resulting Voronoi tessellation. The complex biomechanics that govern intracellular and intercellular interactions can be coarse-grained (17, 18, 2125) and expressed in terms of a mechanical energy functional for individual cell shapes. E = N i=1 h K A (A i - A 0 ) 2 + K P (P i - P 0 ) 2 i . [1] The SPV energy functional is quadratic in both cell areas ({A i }) with modulus K A and cell perimeters ({P i }) with modulus K P . The pa- rameters A 0 and P 0 set the preferred values for area and perimeter, respectively. Changes to cell perimeters are directly related to the deformation of the acto-myosin cortex concentrated near the cell membrane. After expanding equation Eq. (1), the term K P P 2 i corre- sponds to the elastic energy associated with deforming the cortex. The linear term in cell perimeter, -2K 0 P 0 P i , represents the effective line tension in the cortex and gives rise to a ‘preferred perimeter’ P 0 . The value of P 0 can be decreased by up-regulating the contractile tension in the cortex (18, 22, 25) and it can be increased by up-regulating cell-cell adhesion. We simulate tissues containing N cells under periodic boundary conditions, the value of N has been varied from N = 64 to 1600 to check for finite-size effects. A 0 is set to be equal to the average area per cell, i.e. and A 0 is used as the unit of length. After non-dimensionalizing Eq. 1 by K A A 2 0 as the unit energy scale, we choose K P /(K A A 0 )= 1 such that the perimeter and area terms contribute equally to the cell shapes. The choice of K P does not af- fect the results presented. The preferred cell perimeter is rescaled p 0 = P 0 / A 0 and varied between 3.7 (corresponding to the perimeter of a regular hexagon with unit area) and 4.6 (corresponding to the perimeter of an equilateral triangle with unit area) (25). We obtain disordered ground states of the SPV model by minimizing E using the L-BFGS method (26) starting from a random Poisson point pattern. We also test the finite temperature behavior of the SPV model by Significance Statement We design an amorphous material with a full photonic band gap inspired by how cells pack in biological tissues. The size of the photonic band gap could be manipulated through thermal and mechanical tuning. The photonic band gap is also directionally isotropic and persists in solid and fluid phases. This property gives rise to a photonic fluid which overcomes many of the limitations of previously proposed photonic crystalline materials due to its insensitivity to structural defects and robustness with respect to fluid flow, rearrangements and thermal fluctuations. The authors declare no conflict of interest here. 1 To whom correspondence should be addressed. E-mail: [email protected] www.pnas.org/cgi/doi/10.1073/pnas.XXXXXXXXXX PNAS | January 30, 2018 | vol. XXX | no. XX | 1–6
Transcript
Page 1: Abiologicaltissue-inspiredtunablephotonicfluid › ... › 01 › photonics_full.pdf · Abiologicaltissue-inspiredtunablephotonicfluid Xinzhi Li, Amit Das, and Dapeng Bi1 Department

DRAFT

A biological tissue-inspired tunable photonic fluidXinzhi Li, Amit Das, and Dapeng Bi1

Department of Physics, Northeastern University, MA 02115, USA

This manuscript was compiled on January 30, 2018

Inspired by how cells pack in dense biological tissues, we design 2D and3D amorphous materials which possess a complete photonic band gap.A physical parameter based on how cells adhere with one another andregulate their shapes can continuously tune the photonic band gap sizeas well as the bulk mechanical properties of the material. The materialcan be tuned to go through a solid-fluid phase transition characterizedby a vanishing shear modulus. Remarkably, the photonic band gap per-sists in the fluid phase, giving rise to a photonic fluid that is robust toflow and rearrangements. Experimentally this design should lead to theengineering of self-assembled non-rigid photonic structures with pho-tonic band gaps that can be controlled in real time via mechanical andthermal tuning.

amorphous materials | photonic band gap | photonic fluid

Photonic band gap (PBG) materials have remained an intensefocus of research since their introduction (1, 2) and have given

rise to a wide range of applications such as radiation sources (3),sensors, wave guides, solar arrays and optical computer chips (4).Most studies have been devoted to the design and optimization ofphotonic crystals – a periodic arrangement of dielectric scatteringmaterials that have photonic bands due to multiple Bragg scatterings.However, periodicity is not necessary to form PBGs and amorphousstructures with PBGs (5–8) can offer many advantages over theircrystalline counterparts (7). For example amorphous photonic ma-terials can exhibit band gaps that are directionally isotropic (9, 10)and are more robust to defects and errors in fabrication (7). Currentlythere are few existing protocols for designing amorphous photonicmaterials. They include structures obtained from a dense packing ofspheres (3D) or disks (2D) (5, 11–14), tailor-designed protocols thatgenerate hyperuniform patterns (9, 10, 14) and spinodal-decomposedstructures (15, 16). While these designs yield PBGs, such structuresare typically static, rigid constructions that do not allow tuning ofphotonic properties in real time and are unstable to structural changessuch as large scale flows and positional rearrangements.

In this work, we propose a new design for amorphous 2D and 3DPBG materials that is inspired by how cells pack in dense tissues inbiology. We generate structures that exhibit broad PBGs based on asimple model that has been shown to describe cell shapes and tissuemechanical behavior. An advantage of this design is that the photonicand mechanical properties of the material are closely coupled. Thematerial can also be tuned to undergo a density-independent solid-fluidtransition and the PBG persists well into the fluid phase. With recentadvances in tunable self-assembly of nanoparticles or biomimeticemulsion droplets, this design can be used to create a ‘photonic fluid’.

Results

Model for epithelial cell packing in 2D. When epithelial and en-dothelial cells pack densely in 2D to form a confluent monolayer,the structure of the resulting tissue can be described by a polygo-nal tiling (17). A great variety of cell shape structures have beenobserved in tissue monolayers, ranging from near-regular tiling ofcells that resembles a dry foam or honeycomb lattice (18) to highly

irregular tilings of elongated cells (19). To better understand how cellshapes arise from cell-level interactions, a framework called the Self-Propelled Voronoi (SPV) model has been developed recently (20).In the SPV model, the basic degrees of freedom are the set of 2Dcell centers {rrri} and cell shapes are given by the resulting Voronoitessellation. The complex biomechanics that govern intracellular andintercellular interactions can be coarse-grained (17, 18, 21–25) andexpressed in terms of a mechanical energy functional for individualcell shapes.

E =N

∑i=1

[KA(Ai−A0)

2 +KP(Pi−P0)2]. [1]

The SPV energy functional is quadratic in both cell areas ({Ai}) withmodulus KA and cell perimeters ({Pi}) with modulus KP. The pa-rameters A0 and P0 set the preferred values for area and perimeter,respectively. Changes to cell perimeters are directly related to thedeformation of the acto-myosin cortex concentrated near the cellmembrane. After expanding equation Eq. (1), the term KPP2

i corre-sponds to the elastic energy associated with deforming the cortex. Thelinear term in cell perimeter, −2K0P0Pi, represents the effective linetension in the cortex and gives rise to a ‘preferred perimeter’ P0. Thevalue of P0 can be decreased by up-regulating the contractile tensionin the cortex (18, 22, 25) and it can be increased by up-regulatingcell-cell adhesion. We simulate tissues containing N cells underperiodic boundary conditions, the value of N has been varied fromN = 64 to 1600 to check for finite-size effects. A0 is set to be equalto the average area per cell, i.e. and

√A0 is used as the unit of length.

After non-dimensionalizing Eq. 1 by KAA20 as the unit energy scale,

we choose KP/(KAA0) = 1 such that the perimeter and area termscontribute equally to the cell shapes. The choice of KP does not af-fect the results presented. The preferred cell perimeter is rescaledp0 = P0/

√A0 and varied between 3.7 (corresponding to the perimeter

of a regular hexagon with unit area) and 4.6 (corresponding to theperimeter of an equilateral triangle with unit area) (25). We obtaindisordered ground states of the SPV model by minimizing E using theL-BFGS method (26) starting from a random Poisson point pattern.We also test the finite temperature behavior of the SPV model by

Significance Statement

We design an amorphous material with a full photonic band gapinspired by how cells pack in biological tissues. The size of thephotonic band gap could be manipulated through thermal andmechanical tuning. The photonic band gap is also directionallyisotropic and persists in solid and fluid phases. This property givesrise to a photonic fluid which overcomes many of the limitationsof previously proposed photonic crystalline materials due to itsinsensitivity to structural defects and robustness with respect tofluid flow, rearrangements and thermal fluctuations.

The authors declare no conflict of interest here.

1To whom correspondence should be addressed. E-mail: [email protected]

www.pnas.org/cgi/doi/10.1073/pnas.XXXXXXXXXX PNAS | January 30, 2018 | vol. XXX | no. XX | 1–6

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DRAFT

performing Brownian dynamics (20).In the ground states of Eq. 1 are amorphous tilings where the cells

have approximately equal area, but varying perimeters as dictated bythe preferred cell perimeter p0. It has been shown that at a criticalvalue of the p∗0 ≈ 3.81, the tissue collectively undergoes a solid-fluidtransition (25). When p0 < p∗0, cells must overcome finite energybarriers to rearrange and the tissue behaves as a solid , while abovep∗0, the tissue becomes a fluid with a vanishing shear modulus as wellas vanishing energy barriers for rearrangements (25). Coupled tothese mechanical changes is a clear signature in cell shapes at thetransition (20, 27, 28): the shape-based order parameter calculatedby averaging the observed cell perimeter-to-area ratio s = 〈P/

√A〉

grows linearly with p0 when p0 > p∗0 in the fluid phase but remainsat a constant (s≈ p∗0) in the solid phase. In Fig. 1(a) we show threerepresentative snapshots of the ground state at various values of p0.We take advantage of the diversity and tunability of the point patternsand cell structures (Fig. 1(a)) produced by the SPV model and usethem as templates to engineer photonic materials.

Characterization of 2D structure. To better understand the groundstates of the SPV model, we first probe short-range order by analyzingthe pair-correlation function g(r) of cell centers (SI). In Fig. 1(c),g(r) for the solid phase (p0 < 3.81) shows mutual exclusion betweennearest neighbors and becomes constant at large distances. These fea-tures are similar to those observed in other amorphous materials withshort-range repulsion and a lack of long range positional order, such asjammed granular packings (29) and dense colloidal arrays (30). Whenp0 is increased, the tissue enters into the fluid phase at p0 > 3.81. Inorder to satisfy the higher preferred perimeters, cells must becomemore elongated. And when two neighboring elongated cells aligninglocally, their centers can be near each other whereas cells not alignedwill have centers that are further apart. As a result, the first peak ofg(r) broadens. Hence as p0 is increased, short range order is reduced.Deeper in the fluid regime, when p0 > 4.2, g(r) starts to develop apeak close to r = 0 which means that cell centers can come arbitrarilyclose. Interestingly the loss of short range order does not coincidewith the solid-fluid transition, which yields an intermediate fluid statethat retains short range order.

Next we focus on the structural order at long lengthscales. Whilethe SPV ground states are aperiodic by construction, they show in-teresting long range density correlations. The structure factor S(q)(SI) is plotted for various p0 values in Figs. 1(b) & (d). Strikingly,for all p0 values tested, the structure factor vanishes as q→ 0, cor-responding to a persistent density correlation at long distances. Thistype of ‘hidden’ long range order is characteristic of patterns that areknown as hyperuniformity (31, 32). In real space, hyperuniformityis equivalent to when the variance of the number of points σ2

R in anobservation window of radius R grows as function of the surface areaof the window, i.e. σ2

R ∝ Rd−1, where d is the space dimension. (31).This is in contrast to the σ2

R ∝ Rd scaling that holds for uncorrelatedrandom patterns. Indeed, real space measurements in the SPV modelalso confirm that the distribution of cell centers is strongly hyperuni-form for all values of p0 tested that include both solid and fluid states(SI Fig. S1).

It has been suggested that hyperuniform amorphous patterns canbe used to design photonic materials that yield PBGs (9, 10). Florescu& coworkers (9) further conjectured that hyperuniformity is necessaryfor the creation of PBGs. However, recent work by Froufe-Pérez etal (14) have demonstrated that short-range order rather than hyperuni-formity may be more important for PBGs. The SPV model provides aunique example of a hyperuniform point pattern with a short-rangeorder that can be turned on-and-off, this tunability will allow a direct

test of the ideas proposed in refs (9, 10, 14).

2D Photonic Material Design and Properties. For any point pattern(crystalline or amorphous), the first step in the engineering of PBGsis to decorate it with a high dielectric contrast material. The simplestprotocol is to place cylinders centered at each point {rrri = (xi,yi)} thatare infinitely tall in the z−direction. Such design typically yield bandgaps in the Transverse Magnetic (TM) polarization (the magneticfield is parallel to the xy-plane) (33). Based on this design, we firstconstruct a material using SPV point patterns. In order to maximizethe size of the band gap, the cylinders are endowed with dielectricconstant ε = 11.56 and radius r/D = 0.189 (14). We will refer to thisconstruction as “TM-optimized". We also use a second decorationmethod (9, 14) which has been shown to yield complete PBGs, i.e.gaps in both TM and Transverse Electric (TE) polarizations. Weuse a design based on the Delaunay triangulation of a point pattern.Cylinders with ε = 11.56 and radius r/D = 0.18 are placed at thenodes of the Delaunay triangulation while walls with ε = 11.56 andthickness w/D = 0.05 are placed on the bonds of this trivalent net-work. We refer to this construction as “TM+TE optimized". Photonicproperties are numerically calculated using the plane wave expansionmethod (34) implemented in the MIT Photonic Bands program. Weuse the supercell approximation in which a finite sample of N cellsis repeated periodically. The photonic band structure is calculatedby following the path of kkk‖ = (0,0)→ ( 1

2 ,12 )→ (− 1

3 ,13 )→ (0,0) in

reciprocal space. The SI includes a sample script used for photonicband calculations.

The TM-optimized band structure based on a SPV ground statewith N = 64 cells and p0 = 3.85 is shown in Fig. 2(a). Due to theaperiodic nature of the structure, the PBG is isotropic in kkk‖. We alsocalculate the optical density of states (ODOS) (Fig. 2(b)) by binningeigenfrequencies from 10 samples with the same p0 but differentinitial seeds. The relative size of the PBG can be characterized bythe gap-midgap ratio ∆ω/ω0, which is plotted as function of p0 inFig. 3(a) for both TM and TM+TE optimized structures. We find thatthe size of the PBG is constant in the solid phase of the SPV model(p0 < p∗0) with width ∆ω/ω0 ≈ 0.36 for the TM-optimized structureand ∆ω/ω0 ≈ 0.1 in the TM+TE optimized structure. In the fluidphase, ∆ω/ω0 decreases as p0 increases, yet stays finite in the rangeof 3.81 < p0 . 4.0. At even larger p0 values, the PBG vanishes. Thelocation at which the PBG vanishes appears to coincide with the lossof short-range order in the structure. To quantify this, we plot ∆ω/ω0vs the peak height of the pair-correlation g1 in Fig. 3(c). This is inagreement with the findings of Yang et al (11), and suggests that short-range positional order is essential to obtaining a PBGs which allowsfor collective Bragg backscattering of the dielectric material. Thisalso shows that PBGs are absent in states which are hyperuniformbut missing short-range order.

To test for finite-size dependence of the ODOS and the PBG, wecarry out the photonic band calculations at p0 = 3.7 for various sys-tem sizes ranging from N = 64 to N = 1600. At each system size,the ODOS was generated by tabulating TM frequencies along thekkk‖ = (0,0) and kkk‖ = (0.5,0.5) directions in reciprocal space for 10randomly generated states. As shown in SI Fig. S6, while low fre-quency modes may depend on the system size that bigger fluctuationsexist for smaller systems, the PBG is always located between modenumber N and N +1 and has a width that does not change as functionof N.

Since the fluid state has zero shear modulus and can rearrangedue to external driving or thermal perturbations (20, 25), this givesrise to a photonic fluid where a PBG can exist without a static andrigid structure. The solid-fluid transition so far has been driven by

2 | www.pnas.org/cgi/doi/10.1073/pnas.XXXXXXXXXX Li et al.

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DRAFT-4 -3 -2 -1 0 1 2 3 4

qxD/(2π)

-4

-3

-2

-1

0

1

2

3

4

q xD/(2π

)

0

0.5

1

1.5

2

2.5

33.0

2.0

1.0

0.0

p0 = 3.8 p0 = 4.0 p0 = 4.6

S(qx, qy)

0 1 2 30

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0 1 2 30

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0

1

2

p0 = 3.6

p0 = 3.8

p0 = 4.0

p0 = 4.1

p0 = 4.25

p0 = 4.4

p0 = 4.6

r/D qD/2⇡

g(r) S(q)ac d

b

Fig. 1. Tissue structure in the SPV model . (a) Simulation snapshots at 3 different values of the preferred cell perimeters p0. Cell centers are indicated by points and cell shapes aregiven by their Voronoi tessellation (red outlines). (b) Contour plot of the structure factor S(qx,qy) corresponding to the states shown in (a). Scale bar has length 2π/D in reciprocal space,where D is the average spacing between cell centers. (c) Pair-correlation function g(r) at different values of p0. (d) Structure factor S(q) at different values of p0.

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0.35

0.40

0.45

0 0.1 0.2 0.3 0.4

!D

/2⇡c

Opti

calD

.O.S

.

a b

!D/2⇡c

p0 = 3.7

p0 = 3.9

(0, 0)(0, 0) (�1

3,1

3)(

1

2,1

2)

kk

p0 = 3.82

p0 = 3.86

p0 = 3.98

p0 = 3.94

p0 = 4.1

Fig. 2. Characterizing photonic properties in 2D. (a) Photonic band structure of TransverseMagnetic(TM) for the material constructed by placing dielectric cylinders at the cell centersexhibits a PBG. Design is based on a ground state of the SPV at p0 = 3.85. kkk‖ is thein-plane wave vector. (b) The optical density of states of TM at different values of p0. Thewidth of the bandgap ∆ω has a strong dependence on p0, while the midgap frequency ω0

remains constant (SI Fig. S4).

tuning the local interaction p0. Next we study the photonic propertiesof the dynamical fluid phase at finite temperature. At a fixed valueof p0 = 3.7, we simulate Brownian dynamics in the SPV modelat different temperatures T . At each T , we take 10 steady statesamples and construct the TM-optimized structures to calculate theirODOS. In Fig. 3(b), we plot the bandgap size as function of increasingtemperature. Note that even past the melting temperature of T ≈0.25 (20), the PBG does not vanish, again giving rise to a robustphotonic fluid phase. Inside the fluid phase, we also find that the PBGis not affected by the positional changes due to cell rearrangements(SI Fig. S5). Finally, we analyze the effect of heating on the short-

range order. In Fig. 3(c), increasing T results in another ‘path’ inmanipulating the short-range order.

Extension to 3D photonic material. In order to further demonstratethe viability and versatility of tissue-inspired structures as designtemplates for photonic materials, we extend this study to 3D. Recently,Merkel and Manning (35) generalized the 2D SPV model to simulatecell shapes in 3D tissue aggregates by replacing the cell area andperimeter with the cell volume and surface area, respectively. Thisresults in a quadratic energy functional that is a direct analog of Eq. 1

E =N

∑i=1

[KS(Si−S0)

2 +KV (Vi−V0)2], [2]

where Si and Vi are the surface area and volume of the i-th cell in3D, with the preferred surface area and volume being S0 and V0,respectively. Similar to the 2D version of the model, we have twomoduli - KS for the surface area and KV for volume. Following (35),we make our model dimensionless by setting V 1/3

0 as the unit of length

and KSV 4/30 as the unit of energy. This gives us a dimensionless

energy and dimensionless shape factor s0 = S0/V 2/30 as the single

tunable parameter in 3D which again is the anaolog of the parameterp0 is the 2D scenario. For the 3D model, we perform Monte-Carlosimulations (36) with the cell centers at a scaled temperature T = 1,expressed in the unit KSV 4/3

0 /kB where kB is the Boltzmann constant.During the simulation, each randomly chosen cell center is given bya displacement following the Metropolis algorithm (37) where theBoltzmann factor is calculated using the energy function in Eq. 2.For this purpose, we extract the cell surface areas and volumes from3D Voronoi tessellations generated using the Voro++ library (38). Nsuch moves constitute a Monte-Carlo step and we perform 105 suchsteps to ensure that the cells have reached a steady-state. Then werun for another 105 steps to compute the g(r) and S(q). The averagevolume per cell is held constant for this procedure. Periodic boundaryconditions were applied in all directions. For all the simulations wekeep the scaled modulus KVV 2/3

0 /KS = 1. It was found (35) thatthe T = 0 ground states undergoe a similar solid-to-fluid transition

Li et al. PNAS | January 30, 2018 | vol. XXX | no. XX | 3

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DRAFT

Photonic Fluid

�!/!

0

T0 0.2 0.4 0.6 0.8 1

0

0.1

0.2

0.3

0.4

0.5a b c

Melting

AmorphousPhotonic Solid Photonic Fluid

p0

�!/!

0

TM optimizedTM+TE optimized

3.6 3.7 3.8 3.9 4 4.1 4.20

0.1

0.2

0.3

0.4

0.5

�!/!

0

g1

Increa

singT

Increasing p0

1 1.5 2 2.5 30

0.1

0.2

0.3

0.4

0.5

Fig. 3. (a) The structure of the PBG as function of p0. The ”TM-optimized” structure corresponds to the size of the TM band gap for a material constructed by placing dielectric cylindersat cell centers. The ”TM+TE Optimized” structure corresponds to complete PBGs for a material constructed using a trivalent network design (see text). Phases are colored according tothe mechanical property of the material. At p0 ≈ 3.81 the material under goes a solid-fluid transition where the shear modulus vanishes. The dependence of ω0 on p0 is weak as shownin SI Fig. S4(a). (b) Effect of heating on the PBG in the TM optimized structure. At fixed p0 = 3.7, temperature T is gradually increased. At T ≈ 0.25 the material begins to fluidizethrough melting while the bandgap still persists into the mechanical fluid phase. (c) The relationship between the bandgap size in the TM optimized structure and the short range order ofthe system. The explicit dependence of short range order on p0 and T is shown in SI Fig. S2 and S3.

at s0 ∼ 5.4, i.e. solid for s0 < 5.4 and fluid when s0 ≥ 5.4. OurMonte-Carlo simulations also recover this transition near s0 = 5.4when we plot an effective diffusivity, extracted from the mean-aquaredisplacement(MSD) of the cells, at different s0 values (SI Fig. S9).States corresponding below the transition (s0 = 5) and above thetransition (s0 = 5.82) are shown in Fig. 4 for a system of N = 100cells.

We characterize the structure of the 3D cell model by calculatingtheir pair-correlation function g(r). In Fig. 4(c), the short range orderbehaves similar to the 2D case. At low values of s0 that correspondto rigid solids, the first peak in g(r) is pronounced suggesting aneffective repulsion between nearest neighbors. As s0 is increased, thisshort-range order gets eroded as a preference for larger surface area tovolume ratio allows nearest neighbors to be close. The s0 = 6.1 statein Fig. 4(c) is an extreme example where it is possible for two cellcenters to be arbitrarily near. However the long-range order remainsthroughout all values of s0 tested as shown by the S(q) in Fig. 4(d).The small value of S(q→ 0) is a consequence of suppressed densityfluctuations across the system when cells all prefer the same volumedictated by Eq. 2. Whether they are truly hyperuniform would requiresampling at higher system sizes, which is beyond the scope of thisstudy.

Next, in order to make a photonic material we decorate the Voronoitessellations to create a connected dielectric network. While a Voronoitessellation is already a connected network made of vertices andedges, it possess a large dispersion of edge lengths. This can result invertices that are arbitrarily close to each other and could hinder thecreation of PBGs (39). To overcome this we adopt a method describedin (9, 40) to make the structure locally more uniform. In a 3DVoronoi tessellation, each vertex is calculated from the circumcenterof the 4 neighboring cell centers and edges are formed by connectingadjacent vertices. In this design protocol, the connectivity of thedielectric network is the same as the network of the vertices andedges in the Voronoi tessellation. However, the vertex positions of thedielectric network are replaced by the center-of-mass (barycenters) ofthe 4 neighboring Voronoi cell-centers. The resulting structure is atetrahedrally connected network where the edges are more uniform inlength, two representative samples are shown in Fig. 5(a). Next we

decorate the network with dielectric rods of width W running alongthe edges. For the dielectric rods we again use ε = 11.56 and theirwidth W is chosen such that the volume filling fraction of the networkis Vrod/Vbox = 20% (39).

The photonic properties of the 3D dielectric network are calculatedusing the MIT Photonic Bands program (34). We calculate the ODOSfor structures based on different value of s0. Here we have chosenstructures containing N = 100 cells. Due to the isotropic nature of thephotonic band structure (SI Fig. S7), we generate the ODOS basedon two reciprocal vectors k = (0,0,0) & k = (0.5,0.5,0). At eachvalue of s0, we average over 10 different random samples. We findthe first complete photonic band gap between mode number nV andnV +1, where nV is the number of vertices. In the solid phase of themodel (s0 < 5.4), we find an average gap-midgap ratio of around 6%,this decreases as s0 is increased and becomes vanishingly small whenthe model is in its fluid phase (s0 > 5.4) (Fig. 5(b)). Interestingly,the midgap frequency ω0 also shifts slightly toward lower valueswith increasing s0(Fig. 5(c)). The appearance of the PBG here alsocoincides the presence of short-range order. The PBG vanishes whenthere is no longer a pronounced first peak in the g(r).

Discussion and conclusion

We have shown that structures inspired by how cells pack in densetissues can be used as a template for designing amorphous materialswith full photonic bandgaps. The most striking feature of this designermaterial is the simultaneous tunability of mechanical and photonicproperties. The structures have a short-range order that can be tunedby a single parameter, which governs the ratio between cell surfacearea and cell volume (or perimeter-to-area ratio in 2D). The resultingmaterial can be tuned to transition between a solid and a fluid stateand the PBG can be varied continuously. Remarkably, the PBGpersists even when the material behaves as a fluid. The insensitivityto structural defects and robustness with respect to fluid flow andrearrangements results in a photonic fluid which overcomes many ofthe limitations of photonic crystals. Furthermore, we have exploreddifferent ways of tuning the short-range order in the material includingcooling/heating and changing cell-cell interactions. We propose thatthe results in Fig. 3(c) can be used as a guide map for building a

4 | www.pnas.org/cgi/doi/10.1073/pnas.XXXXXXXXXX Li et al.

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DRAFT0 1 2 3

0

1

2

0

1

2

0

1

2

0

1

2

0

1

2

0 1 2 30

1

2

0

1

2

0

1

2

0

1

2

0

1

2

r/D qD/2⇡

g(r) S(q)

a

b

c d

s0 = 5

s0 = 5.29

s0 = 5.58

s0 = 5.90

s0 = 6.10

Fig. 4. Structure characterization in the 3D Voronoi-cell model. (a) Cell centers and their corresponding Voronoi tessellation as well as the decorated 3D photonic structure are shown fora state at s0 = 5 and N = 100 cells. The cell centers are drawn with a finite size and different colors only to aid visualization. (b) Cell centers and their corresponding Voronoi tessellationas well as the decorated 3D photonic structure are shown for a state at s0 = 5.82 and N = 100 cells. (c) Pair-correlation function g(r) at different values of s0. (d) Structure factor S(q) atdifferent values of s0.

0.15 0.2 0.25 0.3

Opti

calD

.O.S

.

5 5.2 5.4 5.6 5.8 6

0

0.02

0.04

0.06

0.08

5 5.2 5.4 5.6 5.8 60.2

0.22

0.24

0.26

�!/!

0

!L/2⇡c

!0L

/2⇡c

a b

cs0

s0

s0 = 5

s0 = 5.15

s0 = 5.29

s0 = 5.44

s0 = 5.58

Fig. 5. Characterizing photonic properties in the 3D design. (a) The optical density ofstates is shown at various values of s0. Here frequency is in units of 2πc/L, where L is theaverage edge length in the photonic network. (b) The size of the gap-midgap ratio ∆ω/ω0

as function of s0. (c) Midgap frequency ω0 as function of s0.

photonic switch that is either mechano-sensitive (changing p0 or s0)or thermosensitive (cooling/heating).

While they are seemingly devoid of long-range order (i.e. they arealways amorphous and non-aperiodic), these tissue inspired structuresalways exhibit strong hyperuniformity. Most interestingly, there aretwo classes of hyperuniform states found in this work: one that hasshort-range order and one that does not. While the former is similarto hyperuniform structures studied previously, the latter class is newand exotic which has not been observed before. Furthermore, wehave shown that hyperuniformity alone is not sufficient for obtainingPBGs, which complements recent studies (14). Rather, the presenceof short-range order is crucial for a PBG.

It will be straightforward to manufacture static photonic mate-rials based on this design using 3D printing or laser etching tech-niques (10, 13). However an even more exciting possibility is to adaptthis design protocol to self-assemble structures. Recent advances inbiomimetic emulsion droplets (41) and nanoparticles grafted withpolymer brushes (42, 43) may make it possible to tune the effectivesurface tension of individual particles as well as the adhesion strengthsbetween particles. This could allow the mimicking of the interactionbetween cells and give rise to a controllable preferred cell perimeter.Whereas 3D printed materials have scattering units that are millime-ters apart (10) and have PBGs in the microwave spectrum, emulsiondroplets and nanoparticles will be able to push the PBG towards thevisible spectrum.

ACKNOWLEDGMENTS. The authors wish to thank M. Lisa Manning andBulbul Chakraborty for helpful discussions and providing valuable commentson the manuscript. The authors acknowledge the support of the NortheasternUniversity Discovery Cluster.

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DRAFT

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6 | www.pnas.org/cgi/doi/10.1073/pnas.XXXXXXXXXX Li et al.

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SI Appendix for A tunable biological tissue-inspired photonic fluid

Xinzhi Li, Amit Das, and Dapeng Bi

Department of Physics,

Northeastern University, MA 02115, USA

1

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I. CHARACTERIZATION OF STRUCTURE

The Pair correlation function is defined as [1]

g(r) =1

⟨∑

i∑i6= j

δ(~r+~ri−~r j)

~ri is the position of the ith particle, N is number of particle and ρ is the average particle density of

the isotropic system. 〈·〉 denotes n ensemble average over different random configurations at the

same parameter set.

The structure factor is given by [2, 3]

S(~q) =1N

⟨∑i, j

ei~q·(~ri−~r j)

〈·〉 denotes n ensemble average over different random configurations at the same parameter set.

S(q) is obtained by further averaging over a sphere of radius q in reciprocal space.

2

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0 1 2 3 4 5 6 7 8 90

2

4

6

8

10 increasing p0

100

101

100

101

R/D

�2 R ⇤

3.6 3.8 4.0 4.2 4.4 4.60.4

0.6

0.8

1.0

1.2

1.4

p0

3.6 3.8 4.0 4.2 4.4 4.60.4

0.6

0.8

1.0

1.2

1.4

3.6 3.8 4.0 4.2 4.4 4.60.4

0.6

0.8

1.0

1.2

1.4

SPV modelTriangular latticeSquare lattice

(a) (b)

FIG. S1. Unusual density fluctuations and hyperuniformity in the SPV model. To characterize hyper-

uniformity, the number of cells contained within an observation window of radius R and centered at rrr0 is

calculated using NR =∫|rrr−rrr0|<R ρ(rrr)drrr, where ρ(rrr) = ∑

Mi=1 δ(rrr− rrri) is the number density. The cell num-

ber variance is then given by σ2R = 〈N2

R〉− 〈NR〉2. Here 〈...〉 averages over random observation windows

and 200 SPV ground state configurations at each p0. Configurations containing 400 cells are used for this

calculation. (a) The cell number variation σ2R is linearly proportional to the observation window size R

at various values of p0. Different lines correspond to p0 = 3.25,3.35,3.813,3.83,3.87,3.89,3.93,3.94,4.5.

Inset shows the same data on a log− log plot, with the dashed line representing a slope of 1. (b) The constant

of proportionality Λ between σ2R and R is plotted as function of p0. The black arrow indicates the location

of the solid-fluid transition for tissues (p0 = 3.81). Values corresponding to Λ in crystalline structures [4]

are given by the dashed lines.

3

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(a) (b)

3.6 3.7 3.8 3.91

1.5

2

2.5

3

3.6 3.7 3.8 3.90

0.5

1

1.5

FIG. S2. The properties of the pair correlation function g(r) for various p0 at zero temperature and

N = 256. (a) Position of the first peak of g(r), defined as r1 , has some deviation from r = 1 with the

increasing of p0. (b) Height of the first peak of g(r), g1, decreases monotonously when p0 is increased,

indicating the loss of short range order .

4

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(a) (b) (c)

0 0.2 0.4 0.6 0.8 11

1.5

2

2.5

3

0 2 4 6 80

0.5

1

1.5

2

2.5

3

0 0.2 0.4 0.6 0.8 10

0.2

0.4

0.6

0.8

1

1.2

FIG. S3. Pair correlation function g(r). (a) g(r) at different temperatures T and fixed p0 = 3.7. To find

a good measure that characterizes the structure of the system, we extract the position and height of the first

peak of g(r), shown in (b) and (c) respectively. We observe that r1 shows very small difference, while g1

decreases monotonously with increasing the temperature. At fixed p0, when heating, the system is also

losing short range order .

5

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(a) (b)

3.6 3.8 4 4.20

0.1

0.2

0.3

0.4

0.5

0 0.2 0.4 0.6 0.8 10

0.1

0.2

0.3

0.4

0.5

FIG. S4. (a) The midgap frequency of the PBG ω0 as function of p0 at T = 0. (b) The midgap frequency of

the PBG ω0 as function of T at fixed p0 = 3.7.

6

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100

101

102

103

104

10-3

10-2

10-1

100

101

m.s

.d.

�t

slope = 1

101

102

103

104

105

0

0.1

0.2

0.3

0.4

0.5

0.6�!/!

0

t

FIG. S5. The photonic bandgap is robust under fluidization. A finite temperature T = 0.006 is applied

to a state at p0 = 3.82. The TM gap-midgap ratio is plotted for different times spanning 4 decades in

simulation time units. The material eventually fluidizes as shown by the mean squared displacement of cell

centers (inset), with a structural relaxation time of t ∼ 103. The snapshots are taken at t = 10,102,103,104.

Here, 10 cells are selected to show relative motion and rearrangements.

7

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0 0.1 0.2 0.3 0.4

!D/2⇡c

Opti

calD

.O.S

.

N = 64

N = 100

N = 225

N = 400

N = 625

N = 900

N = 1600

FIG. S6. Finite-size effects on the photonic bandgap. We measure the ODOS at p0 = 3.7 for various

system sizes ranging from N = 64 to 1600. At each system size, the ODOS was generated by tabulating TM

frequencies along the kkk‖=(0,0) and kkk‖=(0.5,0.5) directions in reciprocal space for 10 randomly generated

states. While low frequency modes may depend on the system size, the photonic bandgap, always located

between mode number N and N +1 spans a frequency range that does not change as function of N.

8

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0

0.05

0.1

0.15

0.2

0.25

0.3

(0, 0.5, 0)

(0,0.625,0.375)

(0, 0.5, 0.5)

(0,0,0)

(0.25, 0.75, 0.5)

(0.375,0.75,0.375)

k

!L

/2⇡

c

o.d.o.s. (au)

(0, 0.5, 0.5)

FIG. S7. The photonic band structure for the decorated 3D dielectric network designed using s0 = 5 and

N = 40 (illustrated in Fig. 5(c)). The eigenfrequencies are calculated along six reciprocal vectors. The

optical density of states is calculated by tabulating all k results at each frequency and shown on the right-

hand side.

9

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0 1 2 3 40

1

2

3

FIG. S8. In order to contrast and compare the hyperuniform patterns of the tissue model with patterns that

are known to be non-hyperuniform, we generate 2D bi-dispersed jammed disk configurations with packing

density φ = 0.86, particle size ratio 1.4 at 50:50 mixture ratio[5]. To calculate S(q), we use a system with

N = 1600 particles and 10 different random configurations. S(q) appears to be not hyperuniform.

10

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10 1 10 2 10 3 10 4 10 510 -4

10 -3

10 -2

10 -1

10 0

10 1

S0=3.50004.00004.5004.80005.00005.14555.29095.43645.55185.72735.9000

3.5 4 4.5 5 5.5 60

0.2

0.4

0.6

0.8

1

1.2 10 -5

FIG. S9. Mean-square displacements 〈∆r(t)2〉 (left) and effective diffusivity De f f (right) of the cells in our

simulations in three dimensions, at different s0 values. The transition from soild-like to fluid-like behavior,

around s0 = 5.4, is quite prominent. Here, D is the unit of length in the simulations defined as D = V 1/30 ,

where V0 is the preferred volume of the cells (also the average volume of the cells in our case). The effective

diffusivity is calculated using Einstein’s result: De f f = 〈∆r(t)2〉/6t in the limit of large time t, or as in our

simulations a large number of Monte-Carlo steps.

11

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II. MPB SAMPLE CODE

Sample MIT Photonic Bands (MPB) code for calculation of the TM eigenspectrum for a sys-

tem of 16 dielectric rods is included below. The rod positions are based on the 2D SPV ground

state at p0 = 3.7. The code is based on the open source script from the MPB [6] website:

https://mpb.readthedocs.io/en/latest/

1 ( def ine−param eps 1 1 . 5 6 ) ; setting the dielectric constant of rods

2 ( d e f i n e GaAs ( make d i e l e c t r i c ( e p s i l o n eps ) ) )

3 ( set ! g e o m e t r y− l a t t i c e ( make l a t t i c e ( s i z e 4 4 no−s ize ) ) ) ; 2d super-cell

4 ( def ine−param r 0 . 1 8 9 ) ; radius of the rods

5 ( set ! geomet ry ; listing rod positions and geometry

6 ( list

7 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 2 .5588 0 . 9 0 6 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

8 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 0 .43963 1 . 3 4 3 4 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

9 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 1 .7984 0 . 0 2 6 3 7 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

10 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 3 .0053 0 . 1 0 9 6 8 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

11 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 1 .9216 2 . 7 4 1 4 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

12 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 3 .8384 0 . 6 8 8 6 9 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

13 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 3 .5071 1 . 6 2 4 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

14 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 1 . 31 2 2 . 1 0 1 5 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

15 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 3 .2054 2 . 5 3 9 1 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

16 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 0 .96737 3 . 2 3 8 3 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

17 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 0 .80395 0 . 2 0 1 4 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

18 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 2 . 25 2 1 . 8 1 4 2 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

19 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 2 .7571 3 . 3 1 8 1 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

20 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 0 .21168 2 . 4 9 0 5 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

21 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 1 .5498 0 . 9 4 8 6 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

22 ( make c y l i n d e r ( m a t e r i a l GaAs ) ( c e n t e r 3 .9663 3 . 4 2 2 2 ) ( r a d i u s r ) ( h e i g h t i n f i n i t y ) )

23 ) )

24 ( set ! k−po in t s ( v e c t o r 3 0 0 0) ) ; define wave vector(s) for calculation of eigenspectrum

25 ( set−param ! r e s o l u t i o n 16) ; resolution sets the grid size for the calculation

26 ( set−param ! num−bands 18) ; number of eigenfrequencies to calculate

27 ( run−tm ) ; begins calculation the eigenspectrum for the transverse-magnetic polarization

[1] Jean-Pierre Hansen and Ian R. McDonald, “Chapter 2 - statistical mechanics,” in Theory of Simple

Liquids (Fourth Edition), edited by Jean-Pierre Hansen and Ian R. McDonald (Academic Press, Oxford,

2013) fourth edition ed., pp. 13 – 59.

[2] Jean-Pierre Hansen and Ian R. McDonald, “Chapter 4 - distribution function theories,” in Theory of

Simple Liquids (Fourth Edition), edited by Jean-Pierre Hansen and Ian R. McDonald (Academic Press,

Oxford, 2013) fourth edition ed., pp. 105 – 147.

[3] Jin-Kyu Yang, Carl Schreck, Heeso Noh, Seng-Fatt Liew, Mikhael I. Guy, Corey S. O’Hern, and Hui

Cao, “Photonic-band-gap effects in two-dimensional polycrystalline and amorphous structures,” Phys.

Rev. A 82, 053838 (2010).

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[4] Salvatore Torquato and Frank H. Stillinger, “Local density fluctuations, hyperuniformity, and order

metrics,” Phys. Rev. E 68, 041113 (2003).

[5] Corey S. O’Hern, Leonardo E. Silbert, Andrea J. Liu, and Sidney R. Nagel, “Jamming at zero temper-

ature and zero applied stress: The epitome of disorder,” Phys. Rev. E 68, 011306 (2003).

[6] Steven G. Johnson and J. D. Joannopoulos, “Block-iterative frequency-domain methods for maxwell’s

equations in a planewave basis,” Opt. Express 8, 173–190 (2001).

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