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Title: Passive membrane transport of lignin-related compounds

Abstract

Lignin is an significant aromatic polymer found in plant secondary cell walls. Recently, 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 findings 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 compoundsmore » 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.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [2];  [3];  [4]; ORCiD logo [5];  [1]; ORCiD logo [1]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  2. Univ. of North Texas, Denton, TX (United States)
  3. Univ. of British Columbia, Vancouver, BC (Canada)
  4. Ghent Univ. (Belgium)
  5. Univ. of Wisconsin, Madison, WI (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (EE-3B); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1574194
Report Number(s):
NREL/JA-2700-74621
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 46; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; molecular dynamics; lignin permeability; lignin biosynthesis; biological funneling; free energy calculation; BCPL

Citation Formats

Vermaas, Josh V., Dixon, Richard A., Chen, Fang, Mansfield, Shawn D., Boerjan, Wout, Ralph, John, Crowley, Michael F., and Beckham, Gregg T. Passive membrane transport of lignin-related compounds. United States: N. p., 2019. Web. doi:10.1073/pnas.1904643116.
Vermaas, Josh V., Dixon, Richard A., Chen, Fang, Mansfield, Shawn D., Boerjan, Wout, Ralph, John, Crowley, Michael F., & Beckham, Gregg T. Passive membrane transport of lignin-related compounds. United States. doi:10.1073/pnas.1904643116.
Vermaas, Josh V., Dixon, Richard A., Chen, Fang, Mansfield, Shawn D., Boerjan, Wout, Ralph, John, Crowley, Michael F., and Beckham, Gregg T. Mon . "Passive membrane transport of lignin-related compounds". United States. doi:10.1073/pnas.1904643116.
@article{osti_1574194,
title = {Passive membrane transport of lignin-related compounds},
author = {Vermaas, Josh V. and Dixon, Richard A. and Chen, Fang and Mansfield, Shawn D. and Boerjan, Wout and Ralph, John and Crowley, Michael F. and Beckham, Gregg T.},
abstractNote = {Lignin is an significant aromatic polymer found in plant secondary cell walls. Recently, 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 findings 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.},
doi = {10.1073/pnas.1904643116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 46,
volume = 116,
place = {United States},
year = {2019},
month = {10}
}

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