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; Mohammad T. Alam; Maria E. Merlo; Jonathan Moore; Walid A M Omara; Edward R. Morrissey; Miguel A. Juarez-Hermosillo; Antonio Rodríguez-García; Merle Nentwich; Louise Thomas; Mudassar Iqbal; Roxane Legaie; William H. Gaze; Gregory L. Challis; 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

doi:10.1186/1471-2164-11-10

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, Mohammad T. Alam, Maria E. Merlo, Jonathan Moore, Walid A M Omara, Edward R. Morrissey, Miguel A. Juarez-Hermosillo, Antonio Rodríguez-García, Merle Nentwich, Louise Thomas, Mudassar Iqbal, Roxane Legaie, William H. Gaze, Gregory L. ChallisRitsert 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 journal › Article › peer-review

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 fermentergrown
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 language	English
Pages (from-to)	1-9
Number of pages	9
Journal	BMC Genomics
Volume	11
Issue number	10
DOIs	https://doi.org/10.1186/1471-2164-11-10
Publication status	Published - 6 Jan 2010

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Nieselt, K., Battke, F., Herbig, A., Bruheim, P., Wentzel, A., Jakobsen, Ø. M., Sletta, H., Alam, M. T., Merlo, M. E., Moore, J., Omara, W. A. M., Morrissey, E. R., Juarez-Hermosillo, M. A., Rodríguez-García, A., Nentwich, M., Thomas, L., Iqbal, M., Legaie, R., Gaze, W. H., ... Wellington, E. M. H. (2010). The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics, 11(10), 1-9. https://doi.org/10.1186/1471-2164-11-10

@article{586bfe0c45d047eaa02fc781e131eb19,

title = "The dynamic architecture of the metabolic switch in Streptomyces coelicolor",

abstract = "Background: During the lifetime of a fermenter culture, the soil bacterium S. coelicolor undergoes a majormetabolic switch from exponential growth to antibiotic production. We have studied gene expression patternsduring this switch, using a specifically designed Affymetrix genechip and a high-resolution time-series of fermentergrownsamples.Results: Surprisingly, we find that the metabolic switch actually consists of multiple finely orchestrated switchingevents. Strongly coherent clusters of genes show drastic changes in gene expression already many hours beforethe classically defined transition phase where the switch from primary to secondary metabolism was expected. Themain switch in gene expression takes only 2 hours, and changes in antibiotic biosynthesis genes are delayedrelative to the metabolic rearrangements. Furthermore, global variation in morphogenesis genes indicates aninvolvement of cell differentiation pathways in the decision phase leading up to the commitment to antibioticbiosynthesis.Conclusions: Our study provides the first detailed insights into the complex sequence of early regulatory eventsduring and preceding the major metabolic switch in S. coelicolor, which will form the starting point for futureattempts at engineering antibiotic production in a biotechnological setting",

author = "Kay Nieselt and Florian Battke and Alexander Herbig and Per Bruheim and Alexander Wentzel and Jakobsen, {{\O}yvind M.} and H{\aa}vard Sletta and Alam, {Mohammad T.} and Merlo, {Maria E.} and Jonathan Moore and Omara, {Walid A M} and Morrissey, {Edward R.} and Juarez-Hermosillo, {Miguel A.} and Antonio Rodr{\'i}guez-Garc{\'i}a and Merle Nentwich and Louise Thomas and Mudassar Iqbal and Roxane Legaie and Gaze, {William H.} and Challis, {Gregory L.} and Jansen, {Ritsert C.} and Lubbert Dijkhuizen and Rand, {David A.} and Wild, {David L.} and Michael Bonin and Jens Reuther and Wolfgang Wohlleben and Smith, {Margaret C M} and Burroughs, {Nigel J.} and Mart{\'i}n, {Juan F.} and Hodgson, {David A.} and Eriko Takano and Rainer Breitling and Ellingsen, {Trond E.} and Wellington, {Elizabeth M H}",

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Nieselt, K, Battke, F, Herbig, A, Bruheim, P, Wentzel, A, Jakobsen, ØM, Sletta, H, Alam, MT, Merlo, ME, Moore, J, Omara, WAM, Morrissey, ER, Juarez-Hermosillo, MA, Rodríguez-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, no. 10, pp. 1-9. https://doi.org/10.1186/1471-2164-11-10

TY - JOUR

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, Mohammad T.

AU - Merlo, Maria E.

AU - Moore, Jonathan

AU - Omara, Walid A M

AU - Morrissey, Edward R.

AU - Juarez-Hermosillo, Miguel A.

AU - Rodríguez-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

Y1 - 2010/1/6

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

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

U2 - 10.1186/1471-2164-11-10

DO - 10.1186/1471-2164-11-10

M3 - Article

SN - 1471-2164

VL - 11

SP - 1

EP - 9

JO - BMC Genomics

JF - BMC Genomics

IS - 10

ER -

The dynamic architecture of the metabolic switch in Streptomyces coelicolor

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