Active microrheology of Chaetopterus mucus determines three intrinsic lengthscales that govern material properties

We characterize the scale-dependent rheological properties of mucus from the Chaetopterus sea annelid and determine the intrinsic lengthscales controlling distinct rheological and structural regimes. The mucus produced by this ubiquitous filter feeder serves a host of roles including filtration, protection and trapping nutrients. The ease of clean mucus extraction coupled with similarities to human mucus rheology also make Chaetopterus mucus a potential model system for elucidating human mucus mechanics. We use optically trapped microsphere probes, 2-10 μm in size, to induce oscillatory microscopic strains and measure the stress response of the mucus as a function of oscillation amplitude and frequency. We show that the viscoelastic properties are highly dependent on the scale (l) of the strain with three distinct regimes emerging: microscale: l1 ≤ 4 μm, mesoscale: l2 ≈ 4-10 μm, and macroscale: l3 ≥ 10 μm. While the mucus response is similar to water for l1 indicating that oscillating probes rarely contact the mucus mesh, for l2 the response is distinctly more viscous and independent of probe size, demonstrating that the mucus network behaves as a continuum. However, this principally viscous mesoscale response at l2 is distinct from the largely elastic macroscopic mucus response. Only for l3 does the response mimic the macroscopic elasticity, with rigid constraints strongly resisting microsphere displacement. Our results demonstrate that a uniform biopolymer mesh model for mucus with a single lengthscale modulating the crossover from water-like to elastic response is too simplistic. Rather, the mucus responds as a hierarchical network with a loose microscopic mesh controlling mechanics for l2, coupled with a mesoscale rigid scaffold responsible for the macroscopic gel-like mechanics beyond l3. Our results shed important new light onto the design of drug delivery platforms, preventing pathogen penetration, and improving filtration, coating and clearance capabilities of mucus.