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Title: Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630

Abstract

Lignin-derived (e.g. phenolic) compounds can compromise the bioconversion of lignocellulosic biomass to fuels and chemicals due to their toxicity and recalcitrance. The lipid-accumulating bacterium Rhodococcus opacus PD630 has recently emerged as a promising microbial host for lignocellulose conversion to value-added products due to its natural ability to tolerate and utilize phenolics. To gain a better understanding of its phenolic tolerance and utilization mechanisms, we adaptively evolved R. opacus over 40 passages using phenol as its sole carbon source (up to 373% growth improvement over wild-type), and extensively characterized two strains from passages 33 and 40. The two adapted strains showed higher phenol consumption rates (~20 mg/l/h) and ~2-fold higher lipid production from phenol than the wild-type strain.Whole-genome sequencing and comparative transcriptomics identified highly-upregulated degradation pathways and putative transporters for phenol in both adapted strains, highlighting the important linkage between mechanisms of regulated phenol uptake, utilization, and evolved tolerance. Our study shows that the R. opacus mutants are likely to use their transporters to import phenol rather than export them, suggesting a new aromatic tolerance mechanism. The identified tolerance genes and pathways are promising candidates for future metabolic engineering in R. opacus for improved lignin conversion to lipid-based products.

Authors:
 [1];  [2];  [1];  [2];  [1];  [2];  [1];  [2];  [3]; ORCiD logo [2]
  1. Washington Univ., St. Louis, MO (United States). St. Louis School of Medicine
  2. Washington Univ., St. Louis, MO (United States)
  3. Washington Univ., St. Louis, MO (United States). St. Louis School of Medicine; Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1255221
Grant/Contract Number:  
SC0012705
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Volume: 44; Journal Issue: 5; Journal ID: ISSN 0305-1048
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Yoneda, Aki, Henson, William R., Goldner, Nicholas K., Park, Kun Joo, Forsberg, Kevin J., Kim, Soo Ji, Pesesky, Mitchell W., Foston, Marcus, Dantas, Gautam, and Moon, Tae Seok. Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630. United States: N. p., 2016. Web. doi:10.1093/nar/gkw055.
Yoneda, Aki, Henson, William R., Goldner, Nicholas K., Park, Kun Joo, Forsberg, Kevin J., Kim, Soo Ji, Pesesky, Mitchell W., Foston, Marcus, Dantas, Gautam, & Moon, Tae Seok. Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630. United States. https://doi.org/10.1093/nar/gkw055
Yoneda, Aki, Henson, William R., Goldner, Nicholas K., Park, Kun Joo, Forsberg, Kevin J., Kim, Soo Ji, Pesesky, Mitchell W., Foston, Marcus, Dantas, Gautam, and Moon, Tae Seok. 2016. "Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630". United States. https://doi.org/10.1093/nar/gkw055. https://www.osti.gov/servlets/purl/1255221.
@article{osti_1255221,
title = {Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630},
author = {Yoneda, Aki and Henson, William R. and Goldner, Nicholas K. and Park, Kun Joo and Forsberg, Kevin J. and Kim, Soo Ji and Pesesky, Mitchell W. and Foston, Marcus and Dantas, Gautam and Moon, Tae Seok},
abstractNote = {Lignin-derived (e.g. phenolic) compounds can compromise the bioconversion of lignocellulosic biomass to fuels and chemicals due to their toxicity and recalcitrance. The lipid-accumulating bacterium Rhodococcus opacus PD630 has recently emerged as a promising microbial host for lignocellulose conversion to value-added products due to its natural ability to tolerate and utilize phenolics. To gain a better understanding of its phenolic tolerance and utilization mechanisms, we adaptively evolved R. opacus over 40 passages using phenol as its sole carbon source (up to 373% growth improvement over wild-type), and extensively characterized two strains from passages 33 and 40. The two adapted strains showed higher phenol consumption rates (~20 mg/l/h) and ~2-fold higher lipid production from phenol than the wild-type strain.Whole-genome sequencing and comparative transcriptomics identified highly-upregulated degradation pathways and putative transporters for phenol in both adapted strains, highlighting the important linkage between mechanisms of regulated phenol uptake, utilization, and evolved tolerance. Our study shows that the R. opacus mutants are likely to use their transporters to import phenol rather than export them, suggesting a new aromatic tolerance mechanism. The identified tolerance genes and pathways are promising candidates for future metabolic engineering in R. opacus for improved lignin conversion to lipid-based products.},
doi = {10.1093/nar/gkw055},
url = {https://www.osti.gov/biblio/1255221}, journal = {Nucleic Acids Research},
issn = {0305-1048},
number = 5,
volume = 44,
place = {United States},
year = {2016},
month = {2}
}

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Cited by: 6 works
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