J. Vermaas, R. Dixon, F. Chen, S. Mansfield, W. Boerjan, J. Ralph, M. Crowley, G. Beckham
Proceedings of the National Academy of Sciences, 2019
Significance In nature, plants and microbes process substantial amounts of aromatic carbon for lignin biosynthesis and breakdown, respectively. These natural processes have important implications in the pursuit of lignin valorization, which is crucial for a vibrant, global bioeconomy. In both plant and microbial systems, an open question remains regarding how lignin-related aromatic compounds are transported across compartmental membranes, either by active membrane transporters or via passive membrane crossing. In this study, we predict that passive transport processes in plants and bacteria for uncharged aromatic compounds are likely sufficient for lignin biosynthesis and catabolism, thus implying that membrane translocation rates are controlled by compound delivery and utilization rates and membrane concentration gradients. Lignin is an abundant aromatic polymer found in plant secondary cell walls. In recent years, lignin has attracted renewed interest as a feedstock for bio-based chemicals via catalytic and biological approaches and has emerged as a target for genetic engineering to improve lignocellulose digestibility by altering its composition. In lignin biosynthesis and microbial conversion, small phenolic lignin precursors or degradation products cross membrane bilayers through an unidentified translocation mechanism prior to incorporation into lignin polymers (synthesis) or catabolism (bioconversion), with both passive and transporter-assisted mechanisms postulated. To test the passive permeation potential of these phenolics, we performed molecular dynamics simulations for 69 monomeric and dimeric lignin-related phenolics with 3 model membranes to determine the membrane partitioning and permeability coefficients for each compound. The results support an accessible passive permeation mechanism for most compounds, including monolignols, dimeric phenolics, and the flavonoid, tricin. Computed lignin partition coefficients are consistent with concentration enrichment near lipid carbonyl groups, and permeability coefficients are sufficient to keep pace with cellular metabolism. Interactions between methoxy and hydroxy groups are found to reduce membrane partitioning and improve permeability. Only carboxylate-modified or glycosylated lignin phenolics are predicted to require transporters for membrane translocation. Overall, the results suggest that most lignin-related compounds can passively traverse plant and microbial membranes on timescales commensurate with required biological activities, with any potential transport regulation mechanism in lignin synthesis, catabolism, or bioconversion requiring compound functionalization.
Cited by 27 publications.
Field of study: Medicine