1887

Abstract

A bacterial isolate, B1D3A, was isolated from river sediment collected from the Hiwassee River near Calhoun, TN, by enrichment culturing with a model 5–5′ lignin dimer, dehydrodivanillate, as its sole carbon source. B1D3A was also shown to utilize several model lignin-derived monomers and dimers as sole carbon sources in a variety of minimal media. Cells were Gram-stain-negative, aerobic, motile, rod-shaped and formed yellow/cream-coloured colonies on rich agar. Optimal growth occurred at 30 °C, pH 7–8, and in the absence of NaCl. The major fatty acids of B1D3A were C ω7 and C ω6. The predominant hydroxy fatty acids were C 2-OH and C 2-OH. The polar lipid profile consisted of a mixture of phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, phosphatidyldimethylethanolamine and sphingoglycolipid. B1D3A contained spermidine as the only major polyamine. The major isoprenoid quinone was Q-10 with minor amounts of Q-9 and Q-11. The genomic DNA G+C content of B1D3A was 65.6 mol%. Phylogenetic analyses based on 16S rRNA gene sequences and coding sequences of 49 core, universal genes defined by Clusters of Orthologous Groups gene families indicated that B1D3A was a member of the genus . B1D3A was most closely related to sp. SYK-6, with a 100 % 16S rRNA gene sequence similarity. B1D3A showed 78.1–89.9 % average nucleotide identity and 19.5–22.2% digital DNA–DNA hybridization identity with other type strains from the genus . On the basis of phenotypic and genotypic properties and phylogenetic inference, strain B1D3A should be classified as representing a novel species of the genus , for which the name sp. nov. is proposed. The type strain is strain B1D3A (ATCC TSD-279=DSM 111877).

Funding
This study was supported by the:
  • Biological and Environmental Research
    • Principle Award Recipient: JoshuaK. Michener
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2023-02-15
2024-05-19
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References

  1. Glaeser SP, Kämpfer P. The family Sphingomonadaceae. In The Prokaryotes Berlin, Heidelberg: Springer Berlin Heidelberg; pp 641–707
    [Google Scholar]
  2. Takeuchi M, Hamana K, Hiraishi A. Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 2001; 51:1405–1417 [View Article] [PubMed]
    [Google Scholar]
  3. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F et al. Lignin valorization: improving lignin processing in the biorefinery. Science 2014; 344:1246843 [View Article]
    [Google Scholar]
  4. Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R. Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 2011; 28:1883–1896 [View Article] [PubMed]
    [Google Scholar]
  5. Kamimura N, Takahashi K, Mori K, Araki T, Fujita M et al. Bacterial catabolism of lignin-derived aromatics: new findings in a recent decade: update on bacterial lignin catabolism. Environ Microbiol Rep 2017; 9:679–705 [View Article]
    [Google Scholar]
  6. Masai E, Katayama Y, Fukuda M. Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem 2007; 71:1–15 [View Article] [PubMed]
    [Google Scholar]
  7. Higuchi Y, Aoki S, Takenami H, Kamimura N, Takahashi K et al. Bacterial catabolism of β-hydroxypropiovanillone and β-hydroxypropiosyringone produced in the reductive cleavage of arylglycerol-β-aryl ether in lignin. Appl Environ Microbiol 2018; 84:1–21 [View Article]
    [Google Scholar]
  8. Sato Y, Moriuchi H, Hishiyama S, Otsuka Y, Oshima K et al. Identification of three alcohol dehydrogenase genes involved in the stereospecific catabolism of arylglycerol-beta-aryl ether by Sphingobium sp. strain SYK-6. Appl Environ Microbiol 2009; 75:5195–5201 [View Article]
    [Google Scholar]
  9. Masai E, Ichimura A, Sato Y, Miyauchi K, Katayama Y et al. Roles of the enantioselective glutathione S-transferases in cleavage of beta-aryl ether. J Bacteriol 2003; 185:1768–1775 [View Article] [PubMed]
    [Google Scholar]
  10. Masai E, Katayama Y, Nishikawa S, Yamasaki M, Morohoshi N et al. Detection and localization of a new enzyme catalyzing the beta-aryl ether cleavage in the soil bacterium (Pseudomonas paucimobilis SYK-6). FEBS Lett 1989; 249:348–352 [View Article] [PubMed]
    [Google Scholar]
  11. Masai E, Katayama Y, Kubota S, Kawai S, Yamasaki M et al. A bacterial enzyme degrading the model lignin compound beta-etherase is a member of the glutathione-S-transferase superfamily. FEBS Lett 1993; 323:135–140 [View Article]
    [Google Scholar]
  12. Sonoki T, Obi T, Kubota S, Higashi M, Masai E et al. Coexistence of two different O demethylation systems in lignin metabolism by Sphingomonas paucimobilis SYK-6: cloning and sequencing of the lignin biphenyl-specific O-demethylase (LigX) gene. Appl Environ Microbiol 2000; 66:2125–2132 [View Article] [PubMed]
    [Google Scholar]
  13. Yoshikata T, Suzuki K, Kamimura N, Namiki M, Hishiyama S et al. Three-component O-demethylase system essential for catabolism of a lignin-derived biphenyl compound in Sphingobium sp. strain SYK-6. Appl Environ Microbiol 2014; 80:7142–7153 [View Article]
    [Google Scholar]
  14. Katayama Y, Nishikawa S, Murayama A, Yamasaki M, Morohoshi N et al. The metabolism of biphenyl structures in lignin by the soil bacterium (Pseudomonas paucimobilis SYK-6). FEBS Lett 1988; 233:129–133 [View Article]
    [Google Scholar]
  15. Mori K, Niinuma K, Fujita M, Kamimura N, Masai E. DdvK, a novel major facilitator superfamily transporter essential for 5,5’-dehydrodivanillate uptake by Sphingobium sp. strain SYK-6. Appl Environ Microbiol 2018; 84:1–16 [View Article]
    [Google Scholar]
  16. Fukuhara Y, Kamimura N, Nakajima M, Hishiyama S, Hara H et al. Discovery of pinoresinol reductase genes in sphingomonads. Enzyme Microb Technol 2013; 52:38–43 [View Article] [PubMed]
    [Google Scholar]
  17. Takahashi K, Kamimura N, Hishiyama S, Hara H, Kasai D et al. Characterization of the catabolic pathway for a phenylcoumaran-type lignin-derived biaryl in Sphingobium sp. strain SYK-6. Biodegradation 2014; 25:735–745 [View Article] [PubMed]
    [Google Scholar]
  18. Kasai D, Masai E, Miyauchi K, Katayama Y, Fukuda M. Characterization of the 3-O-methylgallate dioxygenase gene and evidence of multiple 3-O-methylgallate catabolic pathways in Sphingomonas paucimobilis SYK-6. J Bacteriol 2004; 186:4951–4959 [View Article] [PubMed]
    [Google Scholar]
  19. Kasai D, Masai E, Miyauchi K, Katayama Y, Fukuda M. Characterization of the gallate dioxygenase gene: three distinct ring cleavage dioxygenases are involved in syringate degradation by Sphingomonas paucimobilis SYK-6. J Bacteriol 2005; 187:5067–5074 [View Article] [PubMed]
    [Google Scholar]
  20. Abe T, Masai E, Miyauchi K, Katayama Y, Fukuda M. A tetrahydrofolate-dependent O-demethylase, LigM, is crucial for catabolism of vanillate and syringate in Sphingomonas paucimobilis SYK-6. J Bacteriol 2005; 187:2030–2037 [View Article] [PubMed]
    [Google Scholar]
  21. Araki T, Tanatani K, Kamimura N, Otsuka Y, Yamaguchi M et al. The syringate O-demethylase gene of Sphingobium sp. strain SYK-6 is regulated by desX, while other vanillate and syringate catabolism genes are regulated by desR. Appl Environ Microbiol 2020; 86:1–16 [View Article]
    [Google Scholar]
  22. Masai E, Sasaki M, Minakawa Y, Abe T, Sonoki T et al. A novel tetrahydrofolate-dependent O-demethylase gene is essential for growth of Sphingomonas paucimobilis SYK-6 with syringate. J Bacteriol 2004; 186:2757–2765 [View Article] [PubMed]
    [Google Scholar]
  23. Kasai D, Kamimura N, Tani K, Umeda S, Abe T et al. Characterization of FerC, a MarR-type transcriptional regulator, involved in transcriptional regulation of the ferulate catabolic operon in Sphingobium sp. strain SYK-6. FEMS Microbiol Lett 2012; 332:68–75 [View Article]
    [Google Scholar]
  24. Masai E, Harada K, Peng X, Kitayama H, Katayama Y et al. Cloning and characterization of the ferulic acid catabolic genes of Sphingomonas paucimobilis SYK-6. Appl Environ Microbiol 2002; 68:4416–4424 [View Article] [PubMed]
    [Google Scholar]
  25. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article] [PubMed]
    [Google Scholar]
  26. Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E et al. IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 2012; 40:D115–22 [View Article]
    [Google Scholar]
  27. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article]
    [Google Scholar]
  28. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: the United States department of energy systems biology knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article]
    [Google Scholar]
  29. Kamimura N, Aoyama T, Yoshida R, Takahashi K, Kasai D et al. Characterization of the protocatechuate 4,5-cleavage pathway operon in Comamonas sp. strain E6 and discovery of a novel pathway gene. Appl Environ Microbiol 2010; 76:8093–8101 [View Article] [PubMed]
    [Google Scholar]
  30. Hara H, Masai E, Miyauchi K, Katayama Y, Fukuda M. Characterization of the 4-carboxy-4-hydroxy-2-oxoadipate aldolase gene and operon structure of the protocatechuate 4,5-cleavage pathway genes in Sphingomonas paucimobilis SYK-6. J Bacteriol 2003; 185:41–50 [View Article] [PubMed]
    [Google Scholar]
  31. Hara H, Masai E, Katayama Y, Fukuda M. The 4-oxalomesaconate hydratase gene, involved in the protocatechuate 4,5-cleavage pathway, is essential to vanillate and syringate degradation in Sphingomonas paucimobilis SYK-6. J Bacteriol 2000; 182:6950–6957 [View Article] [PubMed]
    [Google Scholar]
  32. Masai E, Momose K, Hara H, Nishikawa S, Katayama Y et al. Genetic and biochemical characterization of 4-carboxy-2-hydroxymuconate-6-semialdehyde dehydrogenase and its role in the protocatechuate 4,5-cleavage pathway in Sphingomonas paucimobilis SYK-6. J Bacteriol 2000; 182:6651–6658 [View Article] [PubMed]
    [Google Scholar]
  33. Araki T, Umeda S, Kamimura N, Kasai D, Kumano S et al. Regulation of vanillate and syringate catabolism by a MarR-type transcriptional regulator DesR in Sphingobium sp. SYK-6. Sci Rep 2019; 9:1–15 [View Article]
    [Google Scholar]
  34. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee MC et al. Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. PLoS One 2013; 8:e62957 [View Article]
    [Google Scholar]
  35. Varman AM, He L, Follenfant R, Wu W, Wemmer S et al. Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization. Proc Natl Acad Sci 2016; 113:E5802–E5811 [View Article]
    [Google Scholar]
  36. Sonoki T, Otsuka Y, Ikeda S, Masai E, Kajita 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 2002; 48:434–439 [View Article]
    [Google Scholar]
  37. Sonoki T, Masai E, Sato K, Kajita S, Katayama Y. Methoxyl groups of lignin are essential carbon donors in C1 metabolism of Sphingobium sp. SYK-6. J Basic Microbiol 2009; 49 Suppl 1:S98–102 [View Article]
    [Google Scholar]
  38. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article]
    [Google Scholar]
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