1887

Abstract

We investigated the co-catabolism of carbohydrate mixtures in QM B1551 using a C-assisted metabolomics profiling approach. Specifically, we monitored the ability of to achieve the simultaneous catabolism of glucose and a common disaccharide – cellobiose, maltose, or sucrose. Growth experiments indicated that each disaccharide alone can serve as a sole carbon source for , in accordance with the genetic analysis of this bacterium, which predicted diverse metabolic capabilities. However, following growth on C-labelled glucose and each unlabelled disaccharide, the labelling patterns of the intracellular metabolites in glycolysis and the pentose phosphate pathway revealed a hierarchy in disaccharide catabolism: (i) complete inhibition of cellobiose catabolism, (ii) minimal catabolism of maltose and (iii) unbiased catabolism of sucrose. The labelling of amino acids confirmed this selective assimilation of each substrate in biomass precursors. This study highlights the fact that exhibits a mixed-carbohydrate utilization that is different from that of the most studied model species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000540
2017-10-01
2024-11-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/10/1509.html?itemId=/content/journal/micro/10.1099/mic.0.000540&mimeType=html&fmt=ahah

References

  1. Stülke J, Hillen W. Regulation of carbon catabolism in Bacillus species. Annu Rev Microbiol 2000; 54:849–880 [View Article][PubMed]
    [Google Scholar]
  2. Fisher SH, Sonenshein AL. Control of carbon and nitrogen metabolism in Bacillus subtilis. Annu Rev Microbiol 1991; 45:107–135 [View Article][PubMed]
    [Google Scholar]
  3. Fuhrer T, Fischer E, Sauer U. Experimental identification and quantification of glucose metabolism in seven bacterial species. J Bacteriol 2005; 187:1581–1590 [View Article][PubMed]
    [Google Scholar]
  4. Vary PS. Prime time for Bacillus megaterium. Microbiology 1994; 140:1001–1013 [View Article][PubMed]
    [Google Scholar]
  5. Ortíz-Castro R, Valencia-Cantero E, López-Bucio J. Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 2008; 3:263–265 [View Article][PubMed]
    [Google Scholar]
  6. Schallmey M, Singh A, Ward OP. Developments in the use of Bacillus species for industrial production. Can J Microbiol 2004; 50:1–17 [View Article][PubMed]
    [Google Scholar]
  7. Vary PS, Biedendieck R, Fuerch T, Meinhardt F, Rohde M et al. Bacillus megaterium–from simple soil bacterium to industrial protein production host. Appl Microbiol Biotechnol 2007; 76:957–967 [View Article][PubMed]
    [Google Scholar]
  8. Tännler S, Decasper S, Sauer U. Maintenance metabolism and carbon fluxes in Bacillus species. Microb Cell Fact 2008; 7:19 [View Article][PubMed]
    [Google Scholar]
  9. Paul EA, Clark FE. Soil Microbiology and Biochemistry, 2nd ed. New York: Academic Press; 1996
    [Google Scholar]
  10. Quentin Y, Fichant G, Denizot F. Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. J Mol Biol 1999; 287:467–484 [View Article][PubMed]
    [Google Scholar]
  11. Schönert S, Seitz S, Krafft H, Feuerbaum EA, Andernach I et al. Maltose and maltodextrin utilization by Bacillus subtilis. J Bacteriol 2006; 188:3911–3922 [View Article][PubMed]
    [Google Scholar]
  12. Steinmetz M, Le Coq D, Aymerich S. Induction of saccharolytic enzymes by sucrose in Bacillus subtilis: evidence for two partially interchangeable regulatory pathways. J Bacteriol 1989; 171:1519–1523 [View Article][PubMed]
    [Google Scholar]
  13. Tangney M, Buchanan CJ, Priest FG, Mitchell WJ. Maltose uptake and its regulation in Bacillus subtilis. FEMS Microbiol Lett 1992; 76:191–196[PubMed]
    [Google Scholar]
  14. Tobisch S, Glaser P, Krüger S, Hecker M. Identification and characterization of a new beta-glucoside utilization system in Bacillus subtilis. J Bacteriol 1997; 179:496–506 [View Article][PubMed]
    [Google Scholar]
  15. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000; 28:27–30 [View Article][PubMed]
    [Google Scholar]
  16. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016; 44:D457–D462 [View Article][PubMed]
    [Google Scholar]
  17. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 2017; 45:D353–D361 [View Article][PubMed]
    [Google Scholar]
  18. Aristilde L. Metabolite labelling reveals hierarchies in Clostridium acetobutylicum that selectively channel carbons from sugar mixtures towards biofuel precursors. Microb Biotechnol 2017; 10:162–174 [View Article][PubMed]
    [Google Scholar]
  19. Aristilde L, Reed ML, Wilkes RA, Youngster T, Kukurugya MA et al. Glyphosate-induced specific and widespread perturbations in the metabolome of soil Pseudomonas species. Front Environ Sci 2017; 5:34 [View Article]
    [Google Scholar]
  20. Sasnow SS, Wei H, Aristilde L. Bypasses in intracellular glucose metabolism in iron-limited Pseudomonas putida. Microbiologyopen 2016; 5:3–20 [View Article][PubMed]
    [Google Scholar]
  21. Buescher JM, Antoniewicz MR, Boros LG, Burgess SC, Brunengraber H et al. A roadmap for interpreting patterns from cells C metabolite labeling. Curr Opin Biotechnol 2015; 34:189–201
    [Google Scholar]
  22. Schönert S, Buder T, Dahl MK. Properties of maltose-inducible α-glucosidase MalL (sucrase-isomaltase-maltase) in Bacillus subtilis: evidence for its contribution to maltodextrin utilization. Res Microbiol 1999; 150:167–177 [View Article][PubMed]
    [Google Scholar]
  23. Deutscher J, Reizer J, Fischer C, Galinier A, Saier MH et al. Loss of protein kinase-catalyzed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J Bacteriol 1994; 176:3336–3344 [View Article][PubMed]
    [Google Scholar]
  24. Débarbouillé M, Martin-Verstraete I, Arnaud M, Klier A, Rapoport G. Positive and negative regulation controlling expression of the sac genes in Bacillus subtilis. Res Microbiol 1991; 142:757–764 [View Article][PubMed]
    [Google Scholar]
  25. Rutberg B. Antitermination of transcription of catabolic operons. Mol Microbiol 1997; 23:413–321 [View Article][PubMed]
    [Google Scholar]
  26. Chambert R, Treboul G, Dedonder R. Kinetic studies of levansucrase of Bacillus subtilis. Eur J Biochem 1974; 41:285–300 [View Article][PubMed]
    [Google Scholar]
  27. Meng G, Fütterer K. Structural framework of fructosyl transfer in Bacillus subtilis levansucrase. Nat Struct Biol 2003; 10:935–941 [View Article][PubMed]
    [Google Scholar]
  28. Biedendieck R, Gamer M, Jaensch L, Meyer S, Rohde M et al. A sucrose-inducible promoter system for the intra- and extracellular protein production in Bacillus megaterium. J Biotechnol 2007; 132:426–430 [View Article][PubMed]
    [Google Scholar]
  29. Homann A, Biedendieck R, Götze S, Jahn D, Seibel J. Insights into polymer versus oligosaccharide synthesis: mutagenesis and mechanistic studies of a novel levansucrase from Bacillus megaterium. Biochem J 2007; 407:189–198 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.000540
Loading
/content/journal/micro/10.1099/mic.0.000540
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error