Molecular Spring-Loaded Coulombic Sensor Governs Smart Biophotonics
Squids and octopi exhibit a remarkable ability to adaptively change skin color for camouflage and communication. We recently discovered the mechanism by which the unique reflectin proteins act as a molecular spring-loaded Coulombic sensor, controlling an osmotic motor that changes the refractive index, thickness and spacing of intracellular Bragg reflectors to smartly tune the “structural color” and intensity of reflected light in squid skin: Reflectin proteins - major constituents of the membrane-bound Bragg lamellae – are block copolymers with repeated canonical domains interspersed with cationic linkers.
Reflectin proteins drive dynamic tuning of color reflected from cells in squid skin. Microscopic image of the tunably reflective cells in squid skin (ca. 30 microns wide x 2-5 microns thick). Diffusion of a drop of neurotransmitter added at the upper right triggered activation of a wave of progressively changing colored reflectance. (The dark area in the center of each cell corresponds to the position of the nucleus.)
Adaptive changes in reflectance from the Bragg lamellae are initiated by a neurotransmitter-activated signal transduction cascade that culminates in catalytic phosphorylation of the reflectins’ cationic linkers. The resulting charge neutralization overcomes the linkers’ Coulombic repulsion, progressively triggering the spring-loaded condensation and secondary folding of the canonical repeat segments to form amphiphilic, bifacially phase-segregated structures, with the emergence of hydrophobic faces that mediate hierarchical molecular assembly. This phase-segregation provides the potential entropic drive, stored in the protein like a stretched spring, while neutralization-tuned Coulombic repulsion of the cationic linkers provides the “stretch.” Once released by charge-neutralization, the resulting condensation, folding and hierarchical assembly trigger Gibbs-Donnan dehydration, shrinking the thickness and spacing of the Bragg lamellae while increasing their refractive index. This progressively changes the color of light reflected from the Bragg lamellae from red to blue, while increasing its intensity.
This process is reversible, cyclable and finely tunable, precisely regulating color across the visible spectrum without chromophores. Employing this tunability, the squid can produce any color in the individually innervated patches of reflective cells in the skin to produce intricate patterns of color for both communication and camouflage. Translation of this recently discovered biomolecular mechanism to practical engineering is opening new approaches to energy efficient technologies like smart, dynamically reconfigurable, nanostructured materials and tunable photonic systems.
(Research supported by DOE-BES and ARO.)
Daniel E. Morse, Distinguished Research Professor of Molecular, Cellular & Developmental Biology