Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment

S.J.J. Brouns, J. Walther, A.P. Snijders, H.J.G. van de Werken, H.L.D.M. Willemen, P. Worm, M.G. de Vos, A. Andersson, M. Lundgren, H.F. Mazon, R.H.H. van den Heuvel, P. Nilsson, L. Salmon, W.M. de Vos, P.C. Wright, R. Bernander, J. van der Oost

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Abstract

The pentose metabolism of Archaea is largely unknown. Here, we have employed an integrated genomics approach including DNA microarray and proteomics analyses to elucidate the catabolic pathway for D-arabinose in Sulfolobus solfataricus. During growth on this sugar, a small set of genes appeared to be differentially expressed compared with growth on D-glucose. These genes were heterologously overexpressed in Escherichia coli, and the recombinant proteins were purified and biochemically studied. This showed that D-arabinose is oxidized to 2-oxoglutarate by the consecutive action of a number of previously uncharacterized enzymes, including a D-arabinose dehydrogenase, a D-arabinonate dehydratase, a novel 2-keto-3-deoxy-D-arabinonate dehydratase, and a 2,5-dioxopentanoate dehydrogenase. Promoter analysis of these genes revealed a palindromic sequence upstream of the TATA box, which is likely to be involved in their concerted transcriptional control. Integration of the obtained biochemical data with genomic context analysis strongly suggests the occurrence of pentose oxidation pathways in both Archaea and Bacteria, and predicts the involvement of additional enzyme components. Moreover, it revealed striking genetic similarities between the catabolic pathways for pentoses, hexaric acids, and hydroxyproline degradation, which support the theory of metabolic pathway genesis by enzyme recruitment
Original languageEnglish
Pages (from-to)27378-27388
JournalJournal of Biological Chemistry
Volume281
Issue number37
DOIs
Publication statusPublished - 2006

Fingerprint

Pentoses
Hydro-Lyases
Arabinose
D-arabinose dehydrogenase
Genes
Archaea
Oxidation
Enzymes
Sulfolobus solfataricus
TATA Box
Escherichia coli Proteins
Hydroxyproline
Microarray Analysis
Microarrays
Growth
Genomics
Metabolic Networks and Pathways
Oligonucleotide Array Sequence Analysis
Recombinant Proteins
Metabolism

Keywords

  • l-arabinose metabolism
  • archaeon sulfolobus-solfataricus
  • entner-doudoroff pathway
  • escherichia-coli
  • crystal-structure
  • thermoacidophilic crenarchaeon
  • fumarylacetoacetate hydrolase
  • pseudomonas-saccharophila
  • glutamate-dehydrogenase
  • caulobacter-crescen

Cite this

Brouns, S. J. J., Walther, J., Snijders, A. P., van de Werken, H. J. G., Willemen, H. L. D. M., Worm, P., ... van der Oost, J. (2006). Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment. Journal of Biological Chemistry, 281(37), 27378-27388. https://doi.org/10.1074/jbc.M605549200
Brouns, S.J.J. ; Walther, J. ; Snijders, A.P. ; van de Werken, H.J.G. ; Willemen, H.L.D.M. ; Worm, P. ; de Vos, M.G. ; Andersson, A. ; Lundgren, M. ; Mazon, H.F. ; van den Heuvel, R.H.H. ; Nilsson, P. ; Salmon, L. ; de Vos, W.M. ; Wright, P.C. ; Bernander, R. ; van der Oost, J. / Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment. In: Journal of Biological Chemistry. 2006 ; Vol. 281, No. 37. pp. 27378-27388.
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abstract = "The pentose metabolism of Archaea is largely unknown. Here, we have employed an integrated genomics approach including DNA microarray and proteomics analyses to elucidate the catabolic pathway for D-arabinose in Sulfolobus solfataricus. During growth on this sugar, a small set of genes appeared to be differentially expressed compared with growth on D-glucose. These genes were heterologously overexpressed in Escherichia coli, and the recombinant proteins were purified and biochemically studied. This showed that D-arabinose is oxidized to 2-oxoglutarate by the consecutive action of a number of previously uncharacterized enzymes, including a D-arabinose dehydrogenase, a D-arabinonate dehydratase, a novel 2-keto-3-deoxy-D-arabinonate dehydratase, and a 2,5-dioxopentanoate dehydrogenase. Promoter analysis of these genes revealed a palindromic sequence upstream of the TATA box, which is likely to be involved in their concerted transcriptional control. Integration of the obtained biochemical data with genomic context analysis strongly suggests the occurrence of pentose oxidation pathways in both Archaea and Bacteria, and predicts the involvement of additional enzyme components. Moreover, it revealed striking genetic similarities between the catabolic pathways for pentoses, hexaric acids, and hydroxyproline degradation, which support the theory of metabolic pathway genesis by enzyme recruitment",
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Brouns, SJJ, Walther, J, Snijders, AP, van de Werken, HJG, Willemen, HLDM, Worm, P, de Vos, MG, Andersson, A, Lundgren, M, Mazon, HF, van den Heuvel, RHH, Nilsson, P, Salmon, L, de Vos, WM, Wright, PC, Bernander, R & van der Oost, J 2006, 'Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment' Journal of Biological Chemistry, vol. 281, no. 37, pp. 27378-27388. https://doi.org/10.1074/jbc.M605549200

Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment. / Brouns, S.J.J.; Walther, J.; Snijders, A.P.; van de Werken, H.J.G.; Willemen, H.L.D.M.; Worm, P.; de Vos, M.G.; Andersson, A.; Lundgren, M.; Mazon, H.F.; van den Heuvel, R.H.H.; Nilsson, P.; Salmon, L.; de Vos, W.M.; Wright, P.C.; Bernander, R.; van der Oost, J.

In: Journal of Biological Chemistry, Vol. 281, No. 37, 2006, p. 27378-27388.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment

AU - Brouns, S.J.J.

AU - Walther, J.

AU - Snijders, A.P.

AU - van de Werken, H.J.G.

AU - Willemen, H.L.D.M.

AU - Worm, P.

AU - de Vos, M.G.

AU - Andersson, A.

AU - Lundgren, M.

AU - Mazon, H.F.

AU - van den Heuvel, R.H.H.

AU - Nilsson, P.

AU - Salmon, L.

AU - de Vos, W.M.

AU - Wright, P.C.

AU - Bernander, R.

AU - van der Oost, J.

PY - 2006

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KW - l-arabinose metabolism

KW - archaeon sulfolobus-solfataricus

KW - entner-doudoroff pathway

KW - escherichia-coli

KW - crystal-structure

KW - thermoacidophilic crenarchaeon

KW - fumarylacetoacetate hydrolase

KW - pseudomonas-saccharophila

KW - glutamate-dehydrogenase

KW - caulobacter-crescen

U2 - 10.1074/jbc.M605549200

DO - 10.1074/jbc.M605549200

M3 - Article

VL - 281

SP - 27378

EP - 27388

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 37

ER -