1887

Abstract

Transcriptional analysis was performed on with the goal of identifying sugar-specific mechanisms for the transcriptional regulation of transport and metabolism genes. DNA microarrays were used to determine transcript levels from total RNA isolated from cells grown on media containing eleven different carbohydrates, including two pentoses (xylose, arabinose), four hexoses (glucose, mannose, galactose, fructose), four disaccharides (sucrose, lactose, maltose, cellobiose) and one polysaccharide (starch). Sugar-specific induction of many transport and metabolism genes indicates that these processes are regulated at the transcriptional level and are subject to carbon catabolite repression. The results show that utilizes symporters and ATP-binding cassette (ABC) transporters for the uptake of pentose sugars, while disaccharides and hexoses are primarily taken up by phosphotransferase system (PTS) transporters and a gluconate : H (GntP) transporter. The transcription of some transporter genes was induced by specific sugars, while others were induced by a subset of the sugars tested. Sugar-specific transport roles are suggested, based on expression comparisons, for various transporters of the PTS, the ABC superfamily and members of the major facilitator superfamily (MFS), including the GntP symporter family and the glycoside-pentoside-hexuronide (GPH)-cation symporter family. Additionally, updates to the genome annotation are proposed, including the identification of genes likely to encode proteins involved in the metabolism of arabinose and xylose via the pentose phosphate pathway.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.037085-0
2010-11-01
2020-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/11/3478.html?itemId=/content/journal/micro/10.1099/mic.0.037085-0&mimeType=html&fmt=ahah

References

  1. Abranches J., Chen Y. Y., Burne R. A.. 2003; Characterization of Streptococcus mutans strains deficient in EIIAB Man of the sugar phosphotransferase system. Appl Environ Microbiol69:4760–4769
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410
    [Google Scholar]
  3. Amster-Choder O., Wright A.. 1997; BglG, the response regulator of the Escherichia coli bgl operon, is phosphorylated on a histidine residue. J Bacteriol179:5621–5624
    [Google Scholar]
  4. Behrens S., Mitchell W., Bahl H.. 2001; Molecular analysis of the mannitol operon of Clostridium acetobutylicum encoding a phosphotransferase system and a putative PTS-modulated regulator. Microbiology147:75–86
    [Google Scholar]
  5. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S.. 2004; Improved prediction of signal peptides: SignalP 3.0. J Mol Biol340:783–795
    [Google Scholar]
  6. Bolstad B. M., Irizarry R. A., Astrand M., Speed T. P.. 2003; A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics19:185–193
    [Google Scholar]
  7. Brückner R., Titgemeyer F.. 2002; Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett209:141–148
    [Google Scholar]
  8. Casjens S.. 2003; Prophages and bacterial genomics: what have we learned so far?. Mol Microbiol49:277–300
    [Google Scholar]
  9. Deutscher J., Francke C., Postma P. W.. 2006; How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev70:939–1031
    [Google Scholar]
  10. Ezeji T., Blaschek H. P.. 2008; Fermentation of dried distillers' grains and solubles (DDGS) hydrolysates to solvents and value-added products by solventogenic clostridia. Bioresour Technol99:5232–5242
    [Google Scholar]
  11. Gapes J. R.. 2000; The economics of acetone-butanol fermentation: theoretical and market considerations. J Mol Microbiol Biotechnol2:27–32
    [Google Scholar]
  12. Gu Y., Ding Y., Ren C., Sun Z., Rodionov D. A., Zhang W., Yang S., Yang C., Jiang W.. 2010; Reconstruction of xylose utilization pathway and regulons in Fermicutes. BMC Genomics11:255 (in press). doi: 10.1186/1471-2164-11-255
    [Google Scholar]
  13. Gutierrez N. A., Maddox I. S.. 1996; Galactose transport in Clostridium acetobutylicum p262. Lett Appl Microbiol23:97–100
    [Google Scholar]
  14. Irizarry R. A., Bolstad B. M., Collin F., Cope L. M., Hobbs B., Speed T. P.. 2003; Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res31:e15
    [Google Scholar]
  15. Jones D. T., Woods D. R.. 1986; Acetone-butanol fermentation revisited. Microbiol Rev50:484–524
    [Google Scholar]
  16. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K. F., Itoh M., Kawashima S., Katayama T., Araki M., Hirakawa M.. 2006; From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res34:D354–D357
    [Google Scholar]
  17. Karp P. D., Ouzounis C. A., Moore-Kochlacs C., Goldovsky L., Kaipa P., Ahren D., Tsoka S., Darzentas N., Kunin V., Lopez-Bigas N.. 2005; Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res33:6083–6089
    [Google Scholar]
  18. Li Y. K., Yao H. J., Cho Y.. 2000; Effective induction, purification and characterization of Trichoderma koningii G-39 β-xylosidase with high transferase activity. Biotechnol Appl Biochem31:119–125
    [Google Scholar]
  19. Liberman E. S., Bleiweis A. S.. 1984; Transport of glucose and mannose by a common phosphoenolpyruvate-dependent phosphotransferase system in Streptococcus mutans GS5. Infect Immun43:1106–1109
    [Google Scholar]
  20. Mitchell W. J., Tangney M.. 2005; Carbohydrate uptake by the phosphotransferase system and other mechanisms. In Handbook on Clostridia pp155–176 Edited by Durre P.. Boca Raton, FL: CRC Press;
    [Google Scholar]
  21. Mitchell W. J., Shaw J. E., Andrews L.. 1991; Properties of the glucose phosphotransferase system of Clostridium acetobutylicum NCIB 8052. Appl Environ Microbiol57:2534–2539
    [Google Scholar]
  22. Nölling J. G., Breton M. V., Omelchenko K. S., Makarova Q., Zeng R., Gibson H. M., Lee J., Dubois D., Qiu J.. other authors 2001; Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol183:4823–4838
    [Google Scholar]
  23. Novichkov P. S., Laikova O. N., Novichkova E. S., Gelfand M. S., Arkin A. P., Dubchak I., Rodionov D. A.. 2010; RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res38:D111–D118
    [Google Scholar]
  24. Paquet V., Croux C., Goma G., Soucaille P.. 1991; Purification and characterization of the extracellular alpha-amylase from Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol57:212–218
    [Google Scholar]
  25. Paredes C. J., Rigoutsos I., Papoutsakis E. T.. 2004; Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res32:1973–1981
    [Google Scholar]
  26. Pfaffl M. W.. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res29:e45
    [Google Scholar]
  27. Poolman B., Knol J., van der Does C., Henderson P. J., Liang W. J., Leblanc G., Pourcher T., Mus-Veteau I.. 1996; Cation and sugar selectivity determinants in a novel family of transport proteins. Mol Microbiol19:911–922
    [Google Scholar]
  28. Qureshi N., Li X. L., Hughes S., Saha B. C., Cotta M. A.. 2006; Butanol production from corn fiber xylan using Clostridium acetobutylicum. Biotechnol Prog22:673–680
    [Google Scholar]
  29. Reid S. J.. 2005; Genetic organization and regulation of hexose and pentose utilization in the clostridia. Handbook on Clostridia pp133–153 Edited by Durre P.. Boca Raton, FL: CRC Press;
    [Google Scholar]
  30. Reid S. J., Rafudeen M. S., Leat N. G.. 1999; The genes controlling sucrose utilization in Clostridium beijerinckii NCIMB 8052 constitute an operon. Microbiology145:1461–1472
    [Google Scholar]
  31. Rodionov D. A., Mironov A. A., Gelfand M. S.. 2001; Transcriptional regulation of pentose utilisation systems in the Bacillus/ Clostridium group of bacteria. FEMS Microbiol Lett205:305–314
    [Google Scholar]
  32. Rosen S., Skaletsky H. J.. 2000; Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology pp365–386 Edited by Krawetz S., Misener S.. Totowa, NJ: Humana Press;
    [Google Scholar]
  33. Ryttersgaard C., Le Nours J., Lo Leggio L., Jørgensen C. T., Christensen L. L., Bjørnvad M., Larsen S. 2004; The structure of endo-beta-1,4-galactanase from Bacillus licheniformis in complex with two oligosaccharide products. J Mol Biol341:107–117
    [Google Scholar]
  34. Saier M. H. Jr, Reizer J.. 1992; Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoenolpyruvate : sugar phosphotransferase system. J Bacteriol174:1433–1438
    [Google Scholar]
  35. Saier M. H. Jr, Chauvaux S., Cook G. M., Deutscher J., Paulsen I. T., Reizer J., Ye J. J.. 1996; Catabolite repression and inducer control in Gram-positive bacteria. Microbiology142:217–230
    [Google Scholar]
  36. Saurin W., Dassa E.. 1994; Sequence relationships between integral inner-membrane proteins of binding protein-dependent transport systems: evolution by recurrent gene duplications. Protein Sci3:325–344
    [Google Scholar]
  37. Singh K. D., Schmalisch M. H., Stülke J., Görke B.. 2008; Carbon catabolite repression in Bacillus subtilis: quantitative analysis of repression exerted by different carbon sources. J Bacteriol190:7275–7284
    [Google Scholar]
  38. Smyth G. K.. 2004; Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol3: Article 3. doi:10.2202/1544-6115.1027
    [Google Scholar]
  39. Sutrina S. L., Reddy P., Saier M. H. Jr, Reizer J.. 1990; The glucose permease of Bacillus subtilis is a single polypeptide chain that functions to energize the sucrose permease. J Biol Chem265:18581–18589
    [Google Scholar]
  40. Tam R., Saier M. H. Jr. 1993; Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev57:320–346
    [Google Scholar]
  41. Tangney M., Mitchell W. J.. 2000; Analysis of a catabolic operon for sucrose transport and metabolism in Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biotechnol2:71–80
    [Google Scholar]
  42. Tangney M., Mitchell W. J.. 2007; Characterisation of a glucose phosphotransferase system in Clostridium acetobutylicum ATCC 824. Appl Microbiol Biotechnol74:398–405
    [Google Scholar]
  43. Tangney M., Brehm J. K., Minton N. P., Mitchell W. J.. 1998a; A gene system for glucitol transport and metabolism in Clostridium beijerinckii NCIMB 8052. Appl Environ Microbiol64:1612–1619
    [Google Scholar]
  44. Tangney M., Rousse C., Yazdanian M., Mitchell W. J.. 1998b; Note: sucrose transport and metabolism in Clostridium beijerinckii NCIMB 8052. J Appl Microbiol84:914–919
    [Google Scholar]
  45. Tangney M., Winters G. T., Mitchell W. J.. 2001; Characterization of a maltose transport system in Clostridium acetobutylicum ATCC 824. J Ind Microbiol Biotechnol27:298–306
    [Google Scholar]
  46. Tangney M., Galinier A., Deutscher J., Mitchell W. J.. 2003; Analysis of the elements of catabolite repression in Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biotechnol6:6–11
    [Google Scholar]
  47. Tatusov R. L., Koonin E. V., Lipman D. J.. 1997; A genomic perspective on protein families. Science278:631–637
    [Google Scholar]
  48. Thompson J., Hess S., Pikis A.. 2004; Genes malh and pagl of Clostridium acetobutylicum ATCC 824 encode NAD+- and Mn2+-dependent phospho-α-glucosidase(s. J Biol Chem279:1553–1561
    [Google Scholar]
  49. Wiesenborn D. P., Rudolph F. B., Papoutsakis E. T.. 1988; Thiolase from Clostridium acetobutylicum ATCC 824 and its role in the synthesis of acids and solvents. Appl Environ Microbiol54:2717–2722
    [Google Scholar]
  50. Yu Y., Tangney M., Aass H. C., Mitchell W. J.. 2007; Analysis of the mechanism and regulation of lactose transport and metabolism in Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol73:1842–1850
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.037085-0
Loading
/content/journal/micro/10.1099/mic.0.037085-0
Loading

Data & Media loading...

Most cited this month

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