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Title: Discovery of Potential Pathways for Biological Conversion of Poplar Wood to Lipids by Co-Fermentation of Rhodococci Strains

Abstract

Biological routes for utilizing both carbohydrates and lignin are important to reach the ultimate goal of bioconversion of full carbon in biomass to biofuels and biochemicals. Recent biotechnology advances have shown promises toward facilitating biological transformation of lignin to lipids. In this study, a series of natural and engineered Rhodococcus strains (e.g. R. opacus PD630, R. jostii RHA1, and R. jostii RHA1 VanA-) with lignin degradation and/or lipid biosynthesis capacities were selected to establish a co-fermentation module that enabled a platform for fundamental understanding of bioconversion pathways of glucose and lignin to lipids. Profiles of metabolites produced by Rhodococcus strains following growth on different carbon sources (e.g. alkali lignin, flowthrough pretreated poplar slurry) revealed several unexpected fermentation products, suggesting novel metabolic capacities and unexplored metabolic pathways in these organisms. Although Rhodococci showed preference to glucose over lignin, nearly half of the lignin was quickly depolymerized to monomers by these strains for cell growth and lipid accumulation after glucose was nearly exhausted. Proteomic profiles showed that lignin depolymerization by Rhodococci involved multiple peroxidases with accessory oxidases. Besides the ß-ketoadipate pathway, the phenylacetic acid (PAA) pathway played a predominant role in the in vivo ring cleavage activity. Deficiency of reducing power andmore » cellular oxidative stress led to lower lipid production while using lignin as the sole carbon source compared with that of using glucose. This work thus suggests that synthetic reconstruction and balanced modification of key regulators and enzymes in lignin depolymerization, aromatic compound metabolism, lipid biosynthesis, and other relevant processes will enable efficient conversion of both lignin and carbohydrates to lipids by Rhodococci.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [3];  [4];  [4];  [5]; ORCiD logo [3];  [6]
  1. Washington State University Tri-Cities
  2. WASHINGTON STATE UNIV TC
  3. BATTELLE (PACIFIC NW LAB)
  4. Hubei University
  5. Texas A & M University
  6. WASHINGTON STATE UNIV
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1523189
Report Number(s):
PNNL-SA-136201
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 12
Country of Publication:
United States
Language:
English
Subject:
Lignin, Lipid, Rhodococcus opacus PD630, Rhodococcus jostii RHA1, Co-fermentation

Citation Formats

Li, Xiaolu, He, Yucai, Zhang, Libing, Xu, Zhangyang, Ben, Haoxi, Gaffrey, Matthew J., Yang, Yongfu, Yang, Shihui, Yuan, Joshua, Qian, Weijun, and Yang, Bin. Discovery of Potential Pathways for Biological Conversion of Poplar Wood to Lipids by Co-Fermentation of Rhodococci Strains. United States: N. p., 2019. Web. doi:10.1186/s13068-019-1395-x.
Li, Xiaolu, He, Yucai, Zhang, Libing, Xu, Zhangyang, Ben, Haoxi, Gaffrey, Matthew J., Yang, Yongfu, Yang, Shihui, Yuan, Joshua, Qian, Weijun, & Yang, Bin. Discovery of Potential Pathways for Biological Conversion of Poplar Wood to Lipids by Co-Fermentation of Rhodococci Strains. United States. doi:10.1186/s13068-019-1395-x.
Li, Xiaolu, He, Yucai, Zhang, Libing, Xu, Zhangyang, Ben, Haoxi, Gaffrey, Matthew J., Yang, Yongfu, Yang, Shihui, Yuan, Joshua, Qian, Weijun, and Yang, Bin. Tue . "Discovery of Potential Pathways for Biological Conversion of Poplar Wood to Lipids by Co-Fermentation of Rhodococci Strains". United States. doi:10.1186/s13068-019-1395-x.
@article{osti_1523189,
title = {Discovery of Potential Pathways for Biological Conversion of Poplar Wood to Lipids by Co-Fermentation of Rhodococci Strains},
author = {Li, Xiaolu and He, Yucai and Zhang, Libing and Xu, Zhangyang and Ben, Haoxi and Gaffrey, Matthew J. and Yang, Yongfu and Yang, Shihui and Yuan, Joshua and Qian, Weijun and Yang, Bin},
abstractNote = {Biological routes for utilizing both carbohydrates and lignin are important to reach the ultimate goal of bioconversion of full carbon in biomass to biofuels and biochemicals. Recent biotechnology advances have shown promises toward facilitating biological transformation of lignin to lipids. In this study, a series of natural and engineered Rhodococcus strains (e.g. R. opacus PD630, R. jostii RHA1, and R. jostii RHA1 VanA-) with lignin degradation and/or lipid biosynthesis capacities were selected to establish a co-fermentation module that enabled a platform for fundamental understanding of bioconversion pathways of glucose and lignin to lipids. Profiles of metabolites produced by Rhodococcus strains following growth on different carbon sources (e.g. alkali lignin, flowthrough pretreated poplar slurry) revealed several unexpected fermentation products, suggesting novel metabolic capacities and unexplored metabolic pathways in these organisms. Although Rhodococci showed preference to glucose over lignin, nearly half of the lignin was quickly depolymerized to monomers by these strains for cell growth and lipid accumulation after glucose was nearly exhausted. Proteomic profiles showed that lignin depolymerization by Rhodococci involved multiple peroxidases with accessory oxidases. Besides the ß-ketoadipate pathway, the phenylacetic acid (PAA) pathway played a predominant role in the in vivo ring cleavage activity. Deficiency of reducing power and cellular oxidative stress led to lower lipid production while using lignin as the sole carbon source compared with that of using glucose. This work thus suggests that synthetic reconstruction and balanced modification of key regulators and enzymes in lignin depolymerization, aromatic compound metabolism, lipid biosynthesis, and other relevant processes will enable efficient conversion of both lignin and carbohydrates to lipids by Rhodococci.},
doi = {10.1186/s13068-019-1395-x},
journal = {Biotechnology for Biofuels},
number = ,
volume = 12,
place = {United States},
year = {2019},
month = {3}
}

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    Works referencing / citing this record:

    Comparative and Functional Genomics of Rhodococcus opacus PD630 for Biofuels Development
    journal, September 2011


    Biological conversion of the aqueous wastes from hydrothermal liquefaction of algae and pine wood by Rhodococci
    journal, January 2017


    Identification and characterization of a NADH oxidoreductase involved in phenylacetic acid degradation pathway from Streptomyces peucetius
    journal, October 2010


    Utilization of simultaneous saccharification and fermentation residues as feedstock for lipid accumulation in Rhodococcus opacus
    journal, September 2017


    Lignin valorization through integrated biological funneling and chemical catalysis
    journal, August 2014

    • Linger, J. G.; Vardon, D. R.; Guarnieri, M. T.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018
    • DOI: 10.1073/pnas.1410657111

    Lignin-degrading enzymes
    journal, February 2015

    • Pollegioni, Loredano; Tonin, Fabio; Rosini, Elena
    • FEBS Journal, Vol. 282, Issue 7
    • DOI: 10.1111/febs.13224

    Structural basis of enzyme encapsulation into a bacterial nanocompartment
    journal, August 2008

    • Sutter, Markus; Boehringer, Daniel; Gutmann, Sascha
    • Nature Structural & Molecular Biology, Vol. 15, Issue 9
    • DOI: 10.1038/nsmb.1473

    Biosynthesis of storage compounds by Rhodococcus jostii RHA1 and global identification of genes involved in their metabolism
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    • Hernández, Martín A.; Mohn, William W.; Martínez, Eliana
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    MS-GF+ makes progress towards a universal database search tool for proteomics
    journal, October 2014

    • Kim, Sangtae; Pevzner, Pavel A.
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms6277

    Discovery and Characterization of Heme Enzymes from Unsequenced Bacteria: Application to Microbial Lignin Degradation
    journal, November 2011

    • Brown, Margaret E.; Walker, Mark C.; Nakashige, Toshiki G.
    • Journal of the American Chemical Society, Vol. 133, Issue 45
    • DOI: 10.1021/ja203972q

    Identification of DypB from Rhodococcus jostii RHA1 as a Lignin Peroxidase
    journal, June 2011

    • Ahmad, Mark; Roberts, Joseph N.; Hardiman, Elizabeth M.
    • Biochemistry, Vol. 50, Issue 23
    • DOI: 10.1021/bi101892z

    Advanced Chemical Design for Efficient Lignin Bioconversion
    journal, January 2017


    Bacterial enzymes involved in lignin degradation
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    • Elias, Joshua E.; Gygi, Steven P.
    • Nature Methods, Vol. 4, Issue 3
    • DOI: 10.1038/nmeth1019

    High cell density cultivation of Rhodococcus opacus for lipid production at a pilot-plant scale
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    • Voss, I.; Steinbüchel, A.
    • Applied Microbiology and Biotechnology, Vol. 55, Issue 5
    • DOI: 10.1007/s002530000576

    Lignin Valorization: Improving Lignin Processing in the Biorefinery
    journal, May 2014

    • Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
    • Science, Vol. 344, Issue 6185, p. 1246843-1246843
    • DOI: 10.1126/science.1246843

    Lignin to lipid bioconversion by oleaginous Rhodococci
    journal, January 2013

    • Kosa, Matyas; Ragauskas, Arthur J.
    • Green Chemistry, Vol. 15, Issue 8
    • DOI: 10.1039/c3gc40434j

    Characterization of lignin derived from water-only and dilute acid flowthrough pretreatment of poplar wood at elevated temperatures
    journal, December 2015


    High-cell-density batch fermentation of Rhodococcus opacus PD630 using a high glucose concentration for triacylglycerol production
    journal, June 2010


    Lipid Production from Dilute Alkali Corn Stover Lignin by Rhodococcus Strains
    journal, January 2017


    Membrane transport of hydrogen peroxide
    journal, August 2006

    • Bienert, Gerd P.; Schjoerring, Jan K.; Jahn, Thomas P.
    • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 8
    • DOI: 10.1016/j.bbamem.2006.02.015

    Rapid metabolic analysis of Rhodococcus opacus PD630 via parallel 13 C-metabolite fingerprinting
    journal, September 2015

    • Hollinshead, Whitney D.; Henson, William R.; Abernathy, Mary
    • Biotechnology and Bioengineering, Vol. 113, Issue 1
    • DOI: 10.1002/bit.25702

    Rhodococcus opacus strain PD630 as a new source of high-value single-cell oil? Isolation and characterization of triacylglycerols and other storage lipids
    journal, May 2000


    Enhancement of total sugar and lignin yields through dissolution of poplar wood by hot water and dilute acid flowthrough pretreatment
    journal, January 2014

    • Yan, Lishi; Zhang, Libing; Yang, Bin
    • Biotechnology for Biofuels, Vol. 7, Issue 1
    • DOI: 10.1186/1754-6834-7-76

    Designer synthetic media for studying microbial-catalyzed biofuel production
    journal, January 2015

    • Tang, Xiaoyu; da Costa Sousa, Leonardo; Jin, Mingjie
    • Biotechnology for Biofuels, Vol. 8, Issue 1
    • DOI: 10.1186/s13068-014-0179-6

    Accumulation of storage lipids in species ofRhodococcus andNocardia and effect of inhibitors and polyethylene glycol
    journal, January 1997

    • Alvarez, Hector M.; Kalscheuer, Rainer; Steinbüchel, Alexander
    • Fett/Lipid, Vol. 99, Issue 7
    • DOI: 10.1002/lipi.19970990704

    Integrated omics study delineates the dynamics of lipid droplets in Rhodococcus opacus PD630
    journal, October 2013

    • Chen, Y.; Ding, Y.; Yang, L.
    • Nucleic Acids Research, Vol. 42, Issue 2
    • DOI: 10.1093/nar/gkt932

    Pathways for degradation of lignin in bacteria and fungi
    journal, January 2011

    • Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M.
    • Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896
    • DOI: 10.1039/c1np00042j

    Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders
    journal, January 2010

    • Ahmad, Mark; Taylor, Charles R.; Pink, David
    • Molecular BioSystems, Vol. 6, Issue 5
    • DOI: 10.1039/b908966g

    Lignocellulose degradation mechanisms across the Tree of Life
    journal, December 2015


    Breaking Down Lignin to High-Value Chemicals: The Conversion of Lignocellulose to Vanillin in a Gene Deletion Mutant of Rhodococcus jostii RHA1
    journal, August 2013

    • Sainsbury, Paul D.; Hardiman, Elizabeth M.; Ahmad, Mark
    • ACS Chemical Biology, Vol. 8, Issue 10
    • DOI: 10.1021/cb400505a

    Bioconversion of lignin model compounds with oleaginous Rhodococci
    journal, December 2011


    under dependency
    journal, August 2001


    Identifying and creating pathways to improve biological lignin valorization
    journal, May 2019


    Cultivation of lipid-producing bacteria with lignocellulosic biomass: Effects of inhibitory compounds of lignocellulosic hydrolysates
    journal, June 2014


    Engineering xylose metabolism in triacylglycerol-producing Rhodococcus opacus for lignocellulosic fuel production
    journal, January 2013

    • Kurosawa, Kazuhiko; Wewetzer, Sandra J.; Sinskey, Anthony J.
    • Biotechnology for Biofuels, Vol. 6, Issue 1
    • DOI: 10.1186/1754-6834-6-134

    The β-Ketoadipate Pathway And The Biology Of Self-Identity
    journal, October 1996


    Lignin: untapped biopolymers in biomass conversion technologies
    journal, June 2013

    • Ayyachamy, Manimaran; Cliffe, Finola E.; Coyne, Jessica M.
    • Biomass Conversion and Biorefinery, Vol. 3, Issue 3
    • DOI: 10.1007/s13399-013-0084-4

    Label-free and redox proteomic analyses of the triacylglycerol-accumulating Rhodococcus jostii RHA1
    journal, March 2015

    • Dávila Costa, José Sebastián; Leichert, Lars; Alvarez, Héctor M.
    • Microbiology, Vol. 161, Issue 3
    • DOI: 10.1099/mic.0.000028

    Proteome analysis reveals differential expression of proteins involved in triacylglycerol accumulation by Rhodococcus jostii RHA1 after addition of methyl viologen
    journal, March 2017

    • Dávila Costa, José Sebastián; Silva, Roxana A.; Leichert, Lars
    • Microbiology, Vol. 163, Issue 3
    • DOI: 10.1099/mic.0.000424

    Strengths, challenges, and opportunities for hydrothermal pretreatment in lignocellulosic biorefineries
    journal, October 2017

    • Yang, Bin; Tao, Ling; Wyman, Charles E.
    • Biofuels, Bioproducts and Biorefining, Vol. 12, Issue 1
    • DOI: 10.1002/bbb.1825

    Theoretic studies on decomposition mechanism of o -methoxy phenethyl phenyl ether: Primary and secondary reactions
    journal, January 2016


    Identification of Manganese Superoxide Dismutase from Sphingobacterium sp. T2 as a Novel Bacterial Enzyme for Lignin Oxidation
    journal, July 2015

    • Rashid, Goran M. M.; Taylor, Charles R.; Liu, Yangqingxue
    • ACS Chemical Biology, Vol. 10, Issue 10
    • DOI: 10.1021/acschembio.5b00298

    The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse
    journal, October 2006

    • McLeod, M. P.; Warren, R. L.; Hsiao, W. W. L.
    • Proceedings of the National Academy of Sciences, Vol. 103, Issue 42, p. 15582-15587
    • DOI: 10.1073/pnas.0607048103

    Pathways for biomass-derived lignin to hydrocarbon fuels
    journal, July 2013

    • Laskar, Dhrubojyoti D.; Yang, Bin; Wang, Huamin
    • Biofuels, Bioproducts and Biorefining, Vol. 7, Issue 5
    • DOI: 10.1002/bbb.1422

    Development of Chemical and Metabolite Sensors for Rhodococcus opacus PD630
    journal, June 2017

    • DeLorenzo, Drew M.; Henson, William R.; Moon, Tae Seok
    • ACS Synthetic Biology, Vol. 6, Issue 10
    • DOI: 10.1021/acssynbio.7b00192

    Characterization of key triacylglycerol biosynthesis processes in rhodococci
    journal, April 2016

    • Amara, Sawsan; Seghezzi, Nicolas; Otani, Hiroshi
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep24985

    Induction and carbon catabolite repression of phenol degradation genes in Rhodococcus erythropolis and Rhodococcus jostii
    journal, June 2014

    • Szőköl, Juraj; Rucká, Lenka; Šimčíková, Michaela
    • Applied Microbiology and Biotechnology, Vol. 98, Issue 19
    • DOI: 10.1007/s00253-014-5881-6

    Opportunities and challenges in biological lignin valorization
    journal, December 2016


    Normalization Approaches for Removing Systematic Biases Associated with Mass Spectrometry and Label-Free Proteomics
    journal, February 2006

    • Callister, Stephen J.; Barry, Richard C.; Adkins, Joshua N.
    • Journal of Proteome Research, Vol. 5, Issue 2
    • DOI: 10.1021/pr050300l

    Biological valorization of low molecular weight lignin
    journal, December 2016


    Efficient coagulation of microalgae in cultures with filamentous fungi
    journal, January 2013