Skip to main content
Journal of Wood Science

Official Journal of the Japan Wood Research Society

Download PDF
  • Note
  • Published:

Tetrahydrofolate-dependent vanillate and syringateO-demethylation links tightly to one-carbon metabolic pathway associated with amino acid synthesis and DNA methylation in the lignin metabolism ofSphingomonas paucimobilis SYK-6

Journal of Wood Science volume 48, pages 434–439 (2002)Cite this article

Abstract

Sphingomonas paucimobilis SYK-6 strain can degrade various lignin-related compounds. In the lignin metabolic pathway of this bacterium, vanillate and syringate are demethylated by the tetrahydrofolate (THF)-dependentO-demethylation system, which requires the enzymatic function of LigH. Upstream of theligH gene is the 5,10-methylene-THF reductase gene. Its gene product was essential for one-carbon metabolism involved in the amino acid synthesis and DNA methylation in all organisms. When themetF gene was inactivated in the genome of SYK-6, the resultant mutant, DLmetF, could not grow on vanillate and syringate as a sole carbon source. Furthermore, DLmetF showed significant accumulation of methyl-THF as a result of vanillate and syringateO-demethylation. We report here that THF-dependent vanillate and syringateO-demethylation links tightly to the one-carbon metabolic pathway that is associated with amino acid synthesis and DNA methylation, and the methyl group is the sole one-carbon source inS. paucimobilis SYK-6.

References

  1. Katayama Y, Nishikawa S, Murayama A, Yamasaki M, Morohoshi N, Haraguchi T (1988) The metabolism of biphenyl structure in lignin of the soil bacterium (Pseudomonas paucomobilis SYK-6). FEBS Lett 233:129–133

    Article  Google Scholar 

  2. Masai E, Katayama Y, Nishikawa S, Fukuda M (1999) Characterization ofSphingomonas paucimobilis SYK-6 genes involved in degradation of lignin-related compounds. J Ind Microbiol Biotechnol 23:364–373

    Article  CAS  PubMed  Google Scholar 

  3. Nishikawa S, Sonoki T, Kasahara T, Obi T, Kubota S, Kawai S, Morohoshi N, Katayama Y (1998) Cloning and sequencing ofSphingomonas (Pseudomonas) paucimobilis gene essential for theO-demethylation of vanillate and syringate. Appl Environ Microbiol 64:836–842

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Peng X, Egashira T, Hanashiro K, Masai E, Nishikawa S, Katayama Y, Kimbara K, Fukuda M (1998) Cloning of aSphingomonas paucimobilis SYK-6 gene encoding a novel oxygenase that cleaves lignin-related biphenyl and characterization of the enzyme. Appl Environ Microbiol 64:2520–2527

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Masai E, Shinohara S, Hara H, Nishikawa S, Katayama Y, Fukuda M (1999) Genetic and biochemical characterization of a 2-pyrone4,6-dicarboxylic acid hydrolase involved in the protocatechuate 4,5-cleavage pathway ofSphingomonas paucimobilis SYK-6. J Bacteriol 181:55–62

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Masai E, Kubota S, Katayama Y, Kawai S, Yamasaki M, Morohoshi N (1993) Characterization of the Cα-dehydrogenase gene involved in the cleavage ofβ-aryl ether byPseudomonas paucimobilis. Biotechnol Biophys Biochem 57:1655–1659

    Article  CAS  Google Scholar 

  7. Masai E, Katayama Y, Kawai S, Nishikawa S, Yamasaki M, Morohoshi N (1991) Cloning and sequencing of the gene forPseudomonas paucimobilis enzyme that cleavesβ-aryl ether. J Bacteriol 173:7950–7955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Masai E, Katayama Y, Kubota S. Kawai S, Yamasaki M, Morohoshi N (1993) A bacterial enzyme degrading the model lignin compound beta-etherase is a member of the glutathione-S-transferase superfamily. FEBS Lett 323:135–140

    Article  CAS  PubMed  Google Scholar 

  9. Noda Y, Nishikawa S, Kadokura H, Nakajima H, Yoda K, Katayama Y, Morohoshi N, Yamasaki M (1990) Molecular cloning of the protocatechuate 4,5-dioxygenase genes ofPseudomonas paucimobilis. J Bacteriol 172:2704–2709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Nishikawa S. Katayama Y, Yamasaki M. Morohoshi N, Haraguchi T (1991) Cloning of the genes involved in protocatechuate meta cleavage pathway. In: Proceedings of the 6th International Symposium on Wood and Pulping Chemistry, 2nd ed, pp 311–313

  11. Peng X, Egashira T, Masai E, Katayama Y, Fukuda M (1999) Characterization of the meta-cleavage compound hydrolase gene involved in degradation of the lignin-related biphenyl structure bySphingomonas paucimobilis SYK-6. Appl Environ Microbiol 65:2789–2793

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Sonoki T, Obi T, Kubota S, Higashi M, Masai E, Katayama Y (2000) Coexistence of two differentO-demethylation systems in the lignin metabolism ofSphingomonas paucimobilis SYK-6: cloning and sequencing of lignin biphenyl specificO-demethylase (LigX). Appl Environ Microbiol 66:2125–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hara H, Masai E, Katayama Y, Fukuda M (2000) The 4-oxalomesaconate hydratase gene, involved in the protocatechuate 4,5-cleavage pathway, is essential to vanillate and syringate degradation inSphingomonas paucimobilis SYK-6. J Bacteriol 182:6950–6957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Masai E, Momose K, Hara H, Nishikawa S, Katayama Y. Fukuda M (2000) Genetic and biochemical characterization of the 4-carboxy-2-hydroxymuconate-6-semialdehyde dehydrogenase and its role in the protocatechuate 4,5-cleavage pathway inSphingomonas paucimobilis SYK-6. J Bacteriol 182:6651–6658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nagy PL, Marolewski A, Benkovic SJ, Zalkin H (1995) Formyltetrahydrofolate hydrolase, a regulatory enzyme that functions to balance pools of tetrahydrofolate and one-carbon tetrahydrofolate adducts inEscherichia coli. J Bacteriol 177:1292–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dean RA, Jesse CR (1985) Regulation of expression of the ADE3 gene for yeast Cl-tetrahydrofolate synthase, a trifunctional enzyme involved in one-carbon metabolism. J Biol Chem 260: 1248–1256

    Google Scholar 

  17. Andrew DH, Douglas AG, Yair SH (2000) Plant one-carbon metabolism and its engineering. Trends Plant Sci 5:206–213

    Article  Google Scholar 

  18. Yano K. Nishi T (1980) pKJ1, a naturally occurring conjugative plasmid coding for toluene degradation and resistance to streptomycin and sulfonamides. J Bacteriol 143:552–560

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  20. Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A (1994) Small mobilizable multi-purpose cloning vectors derived from theEscherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome ofCorynebaclerium glutamicum. Gene 145:69–73

    Article  CAS  PubMed  Google Scholar 

  21. Vannelli T, Messmer M, Studer A, Vuilleumier S, Leisinger T (1999) A corrinoid-dependent catabolic pathway for growth of aMethylobacterium strain with chloromethane. Proc Natl Acad Sci USA 96:4615–4620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. McAnulla C, Woodall CA, McDonald IR, Studer A, Vuilleuminer S, Leisinger T, Murrell JC (2001) Chloromethane utilization gene cluster fromHyphomicrobium chloromethanicum strain CM2T and development of functional gene probes to detect halomethane-degrading bacteria. Appl Environ Microbiol 67:307–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tizon B, Rodriguez-Torres AM, Rodriguez-Belmonte E, Cadahia JL, Cerdan E (1996) Identification of a putative methylenetetrahydrofolate reductase by sequence analysis of a 6.8kb DNA fragment of yeast chromosome. VII. Yeast 12:1047–1051

    Article  CAS  PubMed  Google Scholar 

  24. Deckert G, Warren PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M, Huber R, Feldman RA, Short JM, Olson GJ, Swanson RV (1998) The complete genome of the hyperthermophilic bacteriumAquifex aeolicus. Nature 392:353–358

    Article  CAS  PubMed  Google Scholar 

  25. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacteriumMesorhizobium loti. DNA Res 7:331–338

    Article  CAS  PubMed  Google Scholar 

  26. May BJ, Zhang Q, Li L, Paustian ML, Whittam TS, Kapur VS (2001) Complete nucleotide sequence of an avian isolatePasteurella multocida. Proc Natl Acad Sci USA 98:3460–3465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Saint-Girons I, Duchange N, Zakin MM, Park I, Margarita D, Ferrara P, Cohen GN (1983) Nucleotide sequence ofmetF, theE. coli structural gene for 5,10-methylene tetrahydrofolate reductase and its control region. Nucleic Acids Res 11:6723–6732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, 184-8588, Tokyo, Japan

    Tomonori Sonoki, Yuichiro Otsuka, Seiichiro Ikeda, Shinya Kajita & Yoshihiro Katayama

  2. Department of Bioengineering, Nagaoka University of Engineering, 940-2188, Nigata, Japan

    Eiji Masai

Authors
  1. Tomonori Sonoki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuichiro Otsuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seiichiro Ikeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eiji Masai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shinya Kajita
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshihiro Katayama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomonori Sonoki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sonoki, T., Otsuka, Y., Ikeda, S. et al. Tetrahydrofolate-dependent vanillate and syringateO-demethylation links tightly to one-carbon metabolic pathway associated with amino acid synthesis and DNA methylation in the lignin metabolism ofSphingomonas paucimobilis SYK-6. J Wood Sci 48, 434–439 (2002). https://doi.org/10.1007/BF00770706

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00770706

Key words