Mimicking Biological Phenol Reaction Cascades to Confer Mechanical Function

Biotechnology enables the creation of proteinand nucleicacid-based materials to perform functions such as recognition, catalysis, signaling, and information storage/transfer. Interestingly, neither proteins nor nucleic acids are Nature’s most abundant biopolymers. Polysaccharides and polymeric phenolics (e.g., lignins) are more abundant. We contend that the reaction cascades that generate phenolic materials are understudied but offer a potentially useful route to functional materials. In this work, we mimic poorly characterized phenol reaction cascades that are common in Nature with the goal of controllably altering the mechanical properties of a polysaccharide film. In Nature, phenol reaction cascades are initiated by the enzymatic oxidation of phenols into reactive intermediates that undergo subsequent, uncatalyzed reactions. The initiating enzymes include tyrosinases, peroxidases, and laccases, and the reactive intermediates are typically quinones or free radicals. While the reaction cascades are difficult to study and sometimes controversial, there is little doubt of the product’s mechanical functions. For instance, lignification is initiated by the enzymatic oxidation of phenylpropanes and yields a complex 3D network that confers strength to trees. Sclerotization is initiated by the enzyme-catalyzed oxidization of low-molecularweight phenols that appear to crosslink polymeric components of the insect’s integument to yield hardened (i.e., quinonetanned) “shells”. Curing of the mussel’s adhesive protein is initiated by the enzymatic oxidation of some of its phenolic moieties (i.e., tyrosine or dihydroxyphenylalanine residues) to yield the crosslinked network needed for cohesive strength. Over the years there have been several technological efforts to enlist these reactions to confer mechanical properties upon materials (e.g., to generate crosslinked adhesives, fibers, or gels). We contend that phenol reaction cascades could be more effectively exploited if their initiation could be controlled spatially and temporally. Nature controls cascade initiation by compartmentalization (the phenols and initiating enzymes are stored separately), or by the localized activation of inactive pro-enzymes. Compartmentalization is illustrated by the separate storage of polyphenol oxidase enzymes and phenolic reactants in plant tissue, and the requirement for tissue disruption for contact. Pro-enzyme activation is illustrated by the in-