The dynamic architecture of the metabolic switch in Streptomyces coelicolor

Kay Nieselt, Florian Battke, Alexander Herbig, Per Bruheim, Alexander Wentzel, Øyvind M Jakobsen, Håvard Sletta, M F Alam, Maria E Merlo, Joe Moore, Walid A M Omara, Edward R Morrissey, Miguel A Juarez-Hermosillo, Antonio Rodriguez-García, Merle Nentwich, Louise Thomas, Mudassar Iqbal, Roxane Legaie, William H Gaze, Gregory L Challis & 15 others Ritsert C Jansen, Lubbert Dijkhuizen, David A Rand, David L Wild, Michael Bonin, Jens Reuther, Wolfgang Wohlleben, Margaret C M Smith, Nigel J Burroughs, Juan F Martín, David A Hodgson, Eriko Takano, Rainer Breitling, Trond E Ellingsen, Elizabeth M H Wellington

Research output: Contribution to journalArticle

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Abstract

Background: During the lifetime of a fermenter culture, the soil bacterium S. coelicolor undergoes a major metabolic switch from exponential growth to antibiotic production. We have studied gene expression patterns during this switch, using a specifically designed Affymetrix genechip and a high-resolution time-series of fermenter-grown samples.

Results: Surprisingly, we find that the metabolic switch actually consists of multiple finely orchestrated switching events. Strongly coherent clusters of genes show drastic changes in gene expression already many hours before the classically defined transition phase where the switch from primary to secondary metabolism was expected. The main switch in gene expression takes only 2 hours, and changes in antibiotic biosynthesis genes are delayed relative to the metabolic rearrangements. Furthermore, global variation in morphogenesis genes indicates an involvement of cell differentiation pathways in the decision phase leading up to the commitment to antibiotic biosynthesis.

Conclusions: Our study provides the first detailed insights into the complex sequence of early regulatory events during and preceding the major metabolic switch in S. coelicolor, which will form the starting point for future attempts at engineering antibiotic production in a biotechnological setting.

Original languageEnglish
Article number10
Number of pages9
JournalBMC Genomics
Volume11
DOIs
Publication statusPublished - 6 Jan 2010

Keywords

  • nitrogen-metabolism
  • gene-cluster
  • antibiotic production
  • A3(2)
  • phop
  • expression
  • phase
  • identification
  • sporulation
  • regulator

Cite this

Nieselt, K., Battke, F., Herbig, A., Bruheim, P., Wentzel, A., Jakobsen, Ø. M., ... Wellington, E. M. H. (2010). The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics, 11, [10]. https://doi.org/10.1186/1471-2164-11-10

The dynamic architecture of the metabolic switch in Streptomyces coelicolor. / Nieselt, Kay; Battke, Florian; Herbig, Alexander; Bruheim, Per; Wentzel, Alexander; Jakobsen, Øyvind M; Sletta, Håvard; Alam, M F; Merlo, Maria E; Moore, Joe; Omara, Walid A M; Morrissey, Edward R; Juarez-Hermosillo, Miguel A; Rodriguez-García, Antonio; Nentwich, Merle; Thomas, Louise; Iqbal, Mudassar; Legaie, Roxane; Gaze, William H; Challis, Gregory L; Jansen, Ritsert C; Dijkhuizen, Lubbert; Rand, David A; Wild, David L; Bonin, Michael; Reuther, Jens; Wohlleben, Wolfgang; Smith, Margaret C M; Burroughs, Nigel J; Martín, Juan F; Hodgson, David A; Takano, Eriko; Breitling, Rainer; Ellingsen, Trond E; Wellington, Elizabeth M H.

In: BMC Genomics, Vol. 11, 10, 06.01.2010.

Research output: Contribution to journalArticle

Nieselt, K, Battke, F, Herbig, A, Bruheim, P, Wentzel, A, Jakobsen, ØM, Sletta, H, Alam, MF, Merlo, ME, Moore, J, Omara, WAM, Morrissey, ER, Juarez-Hermosillo, MA, Rodriguez-García, A, Nentwich, M, Thomas, L, Iqbal, M, Legaie, R, Gaze, WH, Challis, GL, Jansen, RC, Dijkhuizen, L, Rand, DA, Wild, DL, Bonin, M, Reuther, J, Wohlleben, W, Smith, MCM, Burroughs, NJ, Martín, JF, Hodgson, DA, Takano, E, Breitling, R, Ellingsen, TE & Wellington, EMH 2010, 'The dynamic architecture of the metabolic switch in Streptomyces coelicolor' BMC Genomics, vol. 11, 10. https://doi.org/10.1186/1471-2164-11-10
Nieselt K, Battke F, Herbig A, Bruheim P, Wentzel A, Jakobsen ØM et al. The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics. 2010 Jan 6;11. 10. https://doi.org/10.1186/1471-2164-11-10
Nieselt, Kay ; Battke, Florian ; Herbig, Alexander ; Bruheim, Per ; Wentzel, Alexander ; Jakobsen, Øyvind M ; Sletta, Håvard ; Alam, M F ; Merlo, Maria E ; Moore, Joe ; Omara, Walid A M ; Morrissey, Edward R ; Juarez-Hermosillo, Miguel A ; Rodriguez-García, Antonio ; Nentwich, Merle ; Thomas, Louise ; Iqbal, Mudassar ; Legaie, Roxane ; Gaze, William H ; Challis, Gregory L ; Jansen, Ritsert C ; Dijkhuizen, Lubbert ; Rand, David A ; Wild, David L ; Bonin, Michael ; Reuther, Jens ; Wohlleben, Wolfgang ; Smith, Margaret C M ; Burroughs, Nigel J ; Martín, Juan F ; Hodgson, David A ; Takano, Eriko ; Breitling, Rainer ; Ellingsen, Trond E ; Wellington, Elizabeth M H. / The dynamic architecture of the metabolic switch in Streptomyces coelicolor. In: BMC Genomics. 2010 ; Vol. 11.
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T1 - The dynamic architecture of the metabolic switch in Streptomyces coelicolor

AU - Nieselt, Kay

AU - Battke, Florian

AU - Herbig, Alexander

AU - Bruheim, Per

AU - Wentzel, Alexander

AU - Jakobsen, Øyvind M

AU - Sletta, Håvard

AU - Alam, M F

AU - Merlo, Maria E

AU - Moore, Joe

AU - Omara, Walid A M

AU - Morrissey, Edward R

AU - Juarez-Hermosillo, Miguel A

AU - Rodriguez-García, Antonio

AU - Nentwich, Merle

AU - Thomas, Louise

AU - Iqbal, Mudassar

AU - Legaie, Roxane

AU - Gaze, William H

AU - Challis, Gregory L

AU - Jansen, Ritsert C

AU - Dijkhuizen, Lubbert

AU - Rand, David A

AU - Wild, David L

AU - Bonin, Michael

AU - Reuther, Jens

AU - Wohlleben, Wolfgang

AU - Smith, Margaret C M

AU - Burroughs, Nigel J

AU - Martín, Juan F

AU - Hodgson, David A

AU - Takano, Eriko

AU - Breitling, Rainer

AU - Ellingsen, Trond E

AU - Wellington, Elizabeth M H

PY - 2010/1/6

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N2 - Background: During the lifetime of a fermenter culture, the soil bacterium S. coelicolor undergoes a major metabolic switch from exponential growth to antibiotic production. We have studied gene expression patterns during this switch, using a specifically designed Affymetrix genechip and a high-resolution time-series of fermenter-grown samples.Results: Surprisingly, we find that the metabolic switch actually consists of multiple finely orchestrated switching events. Strongly coherent clusters of genes show drastic changes in gene expression already many hours before the classically defined transition phase where the switch from primary to secondary metabolism was expected. The main switch in gene expression takes only 2 hours, and changes in antibiotic biosynthesis genes are delayed relative to the metabolic rearrangements. Furthermore, global variation in morphogenesis genes indicates an involvement of cell differentiation pathways in the decision phase leading up to the commitment to antibiotic biosynthesis.Conclusions: Our study provides the first detailed insights into the complex sequence of early regulatory events during and preceding the major metabolic switch in S. coelicolor, which will form the starting point for future attempts at engineering antibiotic production in a biotechnological setting.

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KW - nitrogen-metabolism

KW - gene-cluster

KW - antibiotic production

KW - A3(2)

KW - phop

KW - expression

KW - phase

KW - identification

KW - sporulation

KW - regulator

U2 - 10.1186/1471-2164-11-10

DO - 10.1186/1471-2164-11-10

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JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

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ER -