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Evolvability and hierarchy in rewired bacterial gene networks

Author

Listed:
  • Mark Isalan

    (EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), UPF, 08003 Barcelona, Spain)

  • Caroline Lemerle

    (EMBL, Meyerhofstrasse 1, Heidelberg D-69117, Germany)

  • Konstantinos Michalodimitrakis

    (EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), UPF, 08003 Barcelona, Spain)

  • Carsten Horn

    (EMBL, Meyerhofstrasse 1, Heidelberg D-69117, Germany)

  • Pedro Beltrao

    (EMBL, Meyerhofstrasse 1, Heidelberg D-69117, Germany)

  • Emanuele Raineri

    (EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), UPF, 08003 Barcelona, Spain)

  • Mireia Garriga-Canut

    (EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), UPF, 08003 Barcelona, Spain)

  • Luis Serrano

    (EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), UPF, 08003 Barcelona, Spain)

Abstract

Sequencing DNA from several organisms has revealed that duplication and drift of existing genes have primarily moulded the contents of a given genome. Though the effect of knocking out or overexpressing a particular gene has been studied in many organisms, no study has systematically explored the effect of adding new links in a biological network. To explore network evolvability, we constructed 598 recombinations of promoters (including regulatory regions) with different transcription or σ-factor genes in Escherichia coli, added over a wild-type genetic background. Here we show that ∼95% of new networks are tolerated by the bacteria, that very few alter growth, and that expression level correlates with factor position in the wild-type network hierarchy. Most importantly, we find that certain networks consistently survive over the wild type under various selection pressures. Therefore new links in the network are rarely a barrier for evolution and can even confer a fitness advantage.

Suggested Citation

  • Mark Isalan & Caroline Lemerle & Konstantinos Michalodimitrakis & Carsten Horn & Pedro Beltrao & Emanuele Raineri & Mireia Garriga-Canut & Luis Serrano, 2008. "Evolvability and hierarchy in rewired bacterial gene networks," Nature, Nature, vol. 452(7189), pages 840-845, April.
    • Handle: RePEc:nat:nature:v:452:y:2008:i:7189:d:10.1038_nature06847
    DOI: 10.1038/nature06847
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    Cited by:

    1. Tadamune Kaneko & Macoto Kikuchi, 2022. "Evolution enhances mutational robustness and suppresses the emergence of a new phenotype: A new computational approach for studying evolution," PLOS Computational Biology, Public Library of Science, vol. 18(1), pages 1-20, January.
    2. Javier Santos-Moreno & Eve Tasiudi & Hadiastri Kusumawardhani & Joerg Stelling & Yolanda Schaerli, 2023. "Robustness and innovation in synthetic genotype networks," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Cheemeng Tan & Robert Phillip Smith & Ming-Chi Tsai & Russell Schwartz & Lingchong You, 2014. "Phenotypic Signatures Arising from Unbalanced Bacterial Growth," PLOS Computational Biology, Public Library of Science, vol. 10(8), pages 1-10, August.
    4. Yichao Han & Wanji Li & Alden Filko & Jingyao Li & Fuzhong Zhang, 2023. "Genome-wide promoter responses to CRISPR perturbations of regulators reveal regulatory networks in Escherichia coli," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Payne, Joshua L., 2016. "No tradeoff between versatility and robustness in gene circuit motifs," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 449(C), pages 192-199.
    6. Shintaro Nagata & Macoto Kikuchi, 2020. "Emergence of cooperative bistability and robustness of gene regulatory networks," PLOS Computational Biology, Public Library of Science, vol. 16(6), pages 1-24, June.

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