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Title: Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization

Abstract

Sphingobium sp. SYK-6 is a soil bacterium boasting a well-studied ligninolytic pathway and the potential for development into a microbial chassis for lignin valorization. An improved understanding of its metabolism will help researchers in the engineering of SYK-6 for the production of value-added chemicals through lignin valorization. We used 13 C-fingerprinting, 13 C metabolic flux analysis ( 13 C-MFA), and RNA-sequencing differential expression analysis to uncover the following metabolic traits: ( i ) SYK-6 prefers alkaline conditions, making it an efficient host for the consolidated bioprocessing of lignin, and it also lacks the ability to metabolize sugars or organic acids; ( ii ) the CO 2 release (i.e., carbon loss) from the ligninolysis-based metabolism of SYK-6 is significantly greater than the CO 2 release from the sugar-based metabolism of Escherichia coli ; ( iii ) the vanillin catabolic pathway (which is the converging point of majority of the lignin catabolic pathways) is coupled with the tetrahydrofolate-dependent C1 pathway that is essential for the biosynthesis of serine, histidine, and methionine; ( iv ) catabolic end products of lignin (pyruvate and oxaloacetate) must enter the tricarboxylic acid (TCA) cycle first and then use phosphoenolpyruvate carboxykinase to initiate gluconeogenesis; and ( v )more » 13 C-MFA together with RNA-sequencing differential expression analysis establishes the vanillin catabolic pathway as the major contributor of NAD(P)H synthesis. Therefore, the vanillin catabolic pathway is essential for SYK-6 to obtain sufficient reducing equivalents for its healthy growth; cosubstrate experiments support this finding. This unique energy feature of SYK-6 is particularly interesting because most heterotrophs rely on the transhydrogenase, the TCA cycle, and the oxidative pentose phosphate pathway to obtain NADPH.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1325317
Alternate Identifier(s):
OSTI ID: 1239396
Report Number(s):
SAND-2016-0538J
Journal ID: ISSN 0027-8424; /pnas/113/40/E5802.atom
Grant/Contract Number:  
16-0758; AC04-94AL85000
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 113 Journal Issue: 40; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 60 APPLIED LIFE SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 13C-MFA; fingerprinting; gluconeogenesis; NADPH; TCA

Citation Formats

Varman, Arul M., He, Lian, Follenfant, Rhiannon, Wu, Weihua, Wemmer, Sarah, Wrobel, Steven A., Tang, Yinjie J., and Singh, Seema. Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization. United States: N. p., 2016. Web. doi:10.1073/pnas.1606043113.
Varman, Arul M., He, Lian, Follenfant, Rhiannon, Wu, Weihua, Wemmer, Sarah, Wrobel, Steven A., Tang, Yinjie J., & Singh, Seema. Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization. United States. doi:10.1073/pnas.1606043113.
Varman, Arul M., He, Lian, Follenfant, Rhiannon, Wu, Weihua, Wemmer, Sarah, Wrobel, Steven A., Tang, Yinjie J., and Singh, Seema. Thu . "Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization". United States. doi:10.1073/pnas.1606043113.
@article{osti_1325317,
title = {Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization},
author = {Varman, Arul M. and He, Lian and Follenfant, Rhiannon and Wu, Weihua and Wemmer, Sarah and Wrobel, Steven A. and Tang, Yinjie J. and Singh, Seema},
abstractNote = {Sphingobium sp. SYK-6 is a soil bacterium boasting a well-studied ligninolytic pathway and the potential for development into a microbial chassis for lignin valorization. An improved understanding of its metabolism will help researchers in the engineering of SYK-6 for the production of value-added chemicals through lignin valorization. We used 13 C-fingerprinting, 13 C metabolic flux analysis ( 13 C-MFA), and RNA-sequencing differential expression analysis to uncover the following metabolic traits: ( i ) SYK-6 prefers alkaline conditions, making it an efficient host for the consolidated bioprocessing of lignin, and it also lacks the ability to metabolize sugars or organic acids; ( ii ) the CO 2 release (i.e., carbon loss) from the ligninolysis-based metabolism of SYK-6 is significantly greater than the CO 2 release from the sugar-based metabolism of Escherichia coli ; ( iii ) the vanillin catabolic pathway (which is the converging point of majority of the lignin catabolic pathways) is coupled with the tetrahydrofolate-dependent C1 pathway that is essential for the biosynthesis of serine, histidine, and methionine; ( iv ) catabolic end products of lignin (pyruvate and oxaloacetate) must enter the tricarboxylic acid (TCA) cycle first and then use phosphoenolpyruvate carboxykinase to initiate gluconeogenesis; and ( v ) 13 C-MFA together with RNA-sequencing differential expression analysis establishes the vanillin catabolic pathway as the major contributor of NAD(P)H synthesis. Therefore, the vanillin catabolic pathway is essential for SYK-6 to obtain sufficient reducing equivalents for its healthy growth; cosubstrate experiments support this finding. This unique energy feature of SYK-6 is particularly interesting because most heterotrophs rely on the transhydrogenase, the TCA cycle, and the oxidative pentose phosphate pathway to obtain NADPH.},
doi = {10.1073/pnas.1606043113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 40,
volume = 113,
place = {United States},
year = {2016},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1073/pnas.1606043113

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Cited by: 9 works
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