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Evolvability and hierarchy in rewired bacterial gene networks
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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 sigma-factor genes in Escherichia coli, added over a wild-type genetic background. Here we show that approximately 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.
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“Microbial cells have an intrinsic capacity to balance self preservation (stress protection) and nutritional competence (SPANC).”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [158]
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“This SPANC balance was intensively studied in E. coli and is governed by strict control of processes such as stress and stringent response [158,159].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [158]
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BackgroundChimeric Protein Complexes in Hybrid Species Generate Novel Phenotypes
Piatkowska, E. M., Naseeb, S., Knight, D., & Delneri, D. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003836 · Cited by 48
Yus, E., Lloréns‐Rico, V., Martínez, S., Gallo, C., Eilers, H., Blötz, C., Stülke, J., Lluch‐Senar, M., & Serrano, L. G. (2019) · Cell Systems · doi:10.1016/j.cels.2019.07.001 · Cited by 51
Self-citationEngineering prokaryotic gene circuits
Michalodimitrakis, K., & Isalan, M. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00139.x · Cited by 46
“Another combinatorial strategy that illustrated how flexible bacterial gene networks can be – and their intrinsic capacity to evolve – came from our own laboratory’s work on rewiring bacterial transcription promoters in E. coli (Isalan et al., 2008).”
BackgroundSelf-citationWhat are genes “for” or where are traits “from”? What is the question?
Buchanan, A. V., Sholtis, S. J., Richtsmeier, J. T., & Weiss, K. M. (2009) · BioEssays · doi:10.1002/bies.200800133 · Cited by 46
“’’ Post-transcriptional regulatory mechanisms also play a significant role in genetic function.((38,39))”
BackgroundEngineering transcription factors with novel DNA-binding specificity using comparative genomics
Desai, T. A., Rodionov, D. A., Gelfand, M. S., Alm, E. J., & Rao, C. V. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp079 · Cited by 45
Eng, T., Banerjee, D., Lau, A. K., Bowden, E., Herbert, R. A., Trinh, J., Prahl, J.-P., Deutschbauer, A., Tanjore, D., & Mukhopadhyay, A. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.04.015 · Cited by 50
“…include the use of double or triple mutant RB-TnSeq libraries, or gene overexpression pools with native or heterologous gene libraries (Dunlop et al., 2011; Isalan et al., 2008; Mutalik et al., 2019) drawing novel gene candidates identified from pan-genome assemblies (Norsigian et al., 2020).”
Evolution of Intra-specific Regulatory Networks in a Multipartite Bacterial Genome
Galardini, M., Brilli, M., Spini, G., Rossi, M., Roncaglia, B., Bani, A., Manuela, C., Moretto, M., Engelen, K., Bacci, G., et al. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004478 · Cited by 43
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The dawn of evolutionary genome engineering
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On the basic computational structure of gene regulatory networks
Rodríguez‐Caso, C., Corominas‐Murtra, B., & Solé, R. V. (2009) · Molecular BioSystems · doi:10.1039/b904960f · Cited by 38
Synthetic Biology: Engineering Living Systems from Biophysical Principles
Bartley, B., Kim, K., Medley, K., & Sauro, H. M. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.02.013 · Cited by 41
Regulatory exaptation of the catabolite repression protein (Crp)–cAMP system in Pseudomonas putida
Milanesio, P. A., Arce‐Rodríguez, A., Muñoz, A., Calles, B., & de Lorenzo, V. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02331.x · Cited by 39
Transhydrogenase Promotes the Robustness and Evolvability of E. coli Deficient in NADPH Production
Chou, H.-H. D., Marx, C. J., & Sauer, U. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005007 · Cited by 41
“This phenotypic robustness allows organisms to traverse fitness-inferior states (so-called fitness valleys), similar to the effect of a robust protein fold to tolerate function-innovating but structure-destabilizing mutations [56,57], the flexibility of gene networks to adopt new regulation without compromising pre-ex…”
BackgroundEvolutionary potential of transcription factors for gene regulatory rewiring
Igler, C., Lagator, M., Tkačik, G., Bollback, J. P., & Guet, C. C. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0651-y · Cited by 35
Agarwala, A., & Fisher, D. S. (2018) · Theoretical Population Biology · doi:10.1016/j.tpb.2019.09.011 · Cited by 41
A quantitative method for proteome reallocation using minimal regulatory interventions
Lastiri-Pancardo, G., Mercado-Hernández, J. S., Kim, J., Jiménez, J. I., & Utrilla, J. (2020) · Nature Chemical Biology · doi:10.1038/s41589-020-0593-y · Cited by 38
Hu, T., Payne, J. L., Banzhaf, W., & Moore, J. H. (2012) · Genetic Programming and Evolvable Machines · doi:10.1007/s10710-012-9159-4 · Cited by 35
“However, in biological systems these relationships have been the focus of numerous theoretical [6, 10, 22, 30, 34, 35, 51, 52, 54, 55] and empirical [4, 13, 19, 23] analyses.”
Background
Metadata
- Authors
- Isalan, M., Lemerle, C., Michalodimitrakis, K., Horn, C., Beltrao, P., Raineri, E., Garriga-Canut, M., & Serrano, L.
- Affiliations
- European Molecular Biology Laboratory (ES)
- European Molecular Biology Laboratory (DE)
- Centre for Genomic Regulation (ES)
- Corresponding author
- Isalan, Mark
- Venue
- Nature
- Published
- 2008-04
- Volume
- 452
- Issue
- 7189
- Pages
- 840-845
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2666274
- OpenAlex
- W2159993062
- Cited by
- 307
- References
- 46
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 9 · 2023: 8 · 2022: 11 · 2021: 7 · 2020: 8 · 2019: 12 · 2018: 13 · 2017: 9 · 2016: 13 · 2015: 19 · 2014: 18 · 2013: 29 · 2012: 27
- FWCI
- 16.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Wellcome Trust (066543, WT066543)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- gene regulatory network rewiring, Escherichia coli, transcription factors, sigma factor, network hierarchy, synthetic gene networks, genome rearrangement, bacterial fitness
- MeSH terms
- Escherichia coli, Genes, Bacterial, Genetic Engineering, Promoter Regions, Genetic, Selection, Genetic, Serial Passage, Sigma Factor, Transcription Factors, Gene Expression Regulation, Bacterial, Open Reading Frames, Heat-Shock Response, Evolution, Molecular, Oligonucleotide Array Sequence Analysis, Escherichia coli Proteins, Gene Regulatory Networks
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