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

Arul M. Varman, Lian He, Rhiannon Follenfant, Weihua Wu, Sarah Wemmer, Steven A. Wrobel, Yinjie J. Tang, Seema Singh

Research output: Contribution to journalArticlepeer-review

47 Scopus citations

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 13C-fingerprinting, 13C metabolic flux analysis (13C-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 CO2 release (i.e., carbon loss) from the ligninolysis-based metabolism of SYK-6 is significantly greater than the CO2 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) 13C-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.

Original languageEnglish (US)
Pages (from-to)E5802-E5811
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number40
DOIs
StatePublished - Oct 4 2016
Externally publishedYes

Keywords

  • C-MFA
  • Fingerprinting
  • Gluconeogenesis
  • Lignin
  • NADPH

ASJC Scopus subject areas

  • General

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