IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-60023-w.html
   My bibliography  Save this article

The latent cis-regulatory potential of mobile DNA in Escherichia coli

Author

Listed:
  • Timothy Fuqua

    (University of Zurich
    Quartier Sorge-Batiment Genopode)

  • Andreas Wagner

    (University of Zurich
    Quartier Sorge-Batiment Genopode
    The Sante Fe Institute)

Abstract

Transposable elements can alter gene regulation in their host genome, either when they integrate into a genome, or when they accrue mutations after integration. However, the extent to which transposons can alter gene expression, as well as the necessary mutational steps, are not well characterized. Here we study the gene regulatory potential of the prominent IS3 family of transposable elements in E.coli. We started with 10 sequences from the ends of 5 IS3 sequences, created 18,537 random mutations in them, and measured their promoter activity using a massively parallel reporter assay. All 10 sequences could evolve de-novo promoter activity from single point mutations. De-novo promoters mostly emerge from existing proto-promoter sequences when mutations create new −10 boxes downstream of preexisting −35 boxes. The ends of IS3s harbor ~1.5 times as many such proto-promoter sequences than the E. coli genome. We also estimate that at least 26% of the 706 characterized IS3s already encode promoters. Our study shows that transposable elements can have a high latent cis-regulatory potential. Our observations can help to explain why mobile DNA may persist in prokaryotic genomes. They also underline the potential use of transposable elements as a substrate for evolving new gene expression.

Suggested Citation

  • Timothy Fuqua & Andreas Wagner, 2025. "The latent cis-regulatory potential of mobile DNA in Escherichia coli," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60023-w
    DOI: 10.1038/s41467-025-60023-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-60023-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-60023-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jessika Consuegra & Joël Gaffé & Richard E. Lenski & Thomas Hindré & Jeffrey E. Barrick & Olivier Tenaillon & Dominique Schneider, 2021. "Insertion-sequence-mediated mutations both promote and constrain evolvability during a long-term experiment with bacteria," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Feng Yue & Yong Cheng & Alessandra Breschi & Jeff Vierstra & Weisheng Wu & Tyrone Ryba & Richard Sandstrom & Zhihai Ma & Carrie Davis & Benjamin D. Pope & Yin Shen & Dmitri D. Pervouchine & Sarah Djeb, 2014. "A comparative encyclopedia of DNA elements in the mouse genome," Nature, Nature, vol. 515(7527), pages 355-364, November.
    3. Avihu H. Yona & Eric J. Alm & Jeff Gore, 2018. "Random sequences rapidly evolve into de novo promoters," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    4. Zachary D. Blount & Jeffrey E. Barrick & Carla J. Davidson & Richard E. Lenski, 2012. "Genomic analysis of a key innovation in an experimental Escherichia coli population," Nature, Nature, vol. 489(7417), pages 513-518, September.
    5. Gill Bejerano & Craig B. Lowe & Nadav Ahituv & Bryan King & Adam Siepel & Sofie R. Salama & Edward M. Rubin & W. James Kent & David Haussler, 2006. "A distal enhancer and an ultraconserved exon are derived from a novel retroposon," Nature, Nature, vol. 441(7089), pages 87-90, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Liang-Yu Fu & Tao Zhu & Xinkai Zhou & Ranran Yu & Zhaohui He & Peijing Zhang & Zhigui Wu & Ming Chen & Kerstin Kaufmann & Dijun Chen, 2022. "ChIP-Hub provides an integrative platform for exploring plant regulome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Xin Zhang & Yi-Peng Gao & Wen-Sheng Dong & Kang Li & Yu-Xin Hu & Yun-Jia Ye & Can Hu, 2024. "FNDC4 alleviates cardiac ischemia/reperfusion injury through facilitating HIF1α-dependent cardiomyocyte survival and angiogenesis in male mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Jin Woo Oh & Michael A. Beer, 2024. "Gapped-kmer sequence modeling robustly identifies regulatory vocabularies and distal enhancers conserved between evolutionarily distant mammals," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Shabnam Zaman & Birgit Lengerer & Joris Lindt & Indra Saenen & Giorgio Russo & Laura Bossaer & Sebastien Carpentier & Peter Tompa & Patrick Flammang & Kim Roelants, 2024. "Recurrent evolution of adhesive defence systems in amphibians by parallel shifts in gene expression," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Ryo Mizuuchi & Taro Furubayashi & Norikazu Ichihashi, 2022. "Evolutionary transition from a single RNA replicator to a multiple replicator network," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    6. Simeon D. Castle & Michiel Stock & Thomas E. Gorochowski, 2024. "Engineering is evolution: a perspective on design processes to engineer biology," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    7. Tulsi Patel & Jennifer Hammelman & Siaresh Aziz & Sumin Jang & Michael Closser & Theodore L. Michaels & Jacob A. Blum & David K. Gifford & Hynek Wichterle, 2022. "Transcriptional dynamics of murine motor neuron maturation in vivo and in vitro," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    8. Nicholas Leiby & Christopher J Marx, 2014. "Metabolic Erosion Primarily Through Mutation Accumulation, and Not Tradeoffs, Drives Limited Evolution of Substrate Specificity in Escherichia coli," PLOS Biology, Public Library of Science, vol. 12(2), pages 1-10, February.
    9. Hongchun Lin & Hui Peng & Yuxiang Sun & Meijun Si & Jiao Wu & Yanlin Wang & Sandhya S. Thomas & Zheng Sun & Zhaoyong Hu, 2023. "Reprogramming of cis-regulatory networks during skeletal muscle atrophy in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Jiacheng Wu & Xiaoqing Xu & Jiaqi Duan & Yangyang Chai & Jiaying Song & Dongsheng Gong & Bingjing Wang & Ye Hu & Taotao Han & Yuanyuan Ding & Yin Liu & Jingnan Li & Xuetao Cao, 2024. "EFHD2 suppresses intestinal inflammation by blocking intestinal epithelial cell TNFR1 internalization and cell death," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Noah Dukler & Mehreen R. Mughal & Ritika Ramani & Yi-Fei Huang & Adam Siepel, 2022. "Extreme purifying selection against point mutations in the human genome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. James S. Horton & Louise M. Flanagan & Robert W. Jackson & Nicholas K. Priest & Tiffany B. Taylor, 2021. "A mutational hotspot that determines highly repeatable evolution can be built and broken by silent genetic changes," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    13. Ravneet Jaura & Ssu-Yu Yeh & Kaitlin N. Montanera & Alyssa Ialongo & Zobia Anwar & Yiming Lu & Kavindu Puwakdandawa & Ho Sung Rhee, 2022. "Extended intergenic DNA contributes to neuron-specific expression of neighboring genes in the mammalian nervous system," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    14. Orshay Gabay & Yoav Shoshan & Eli Kopel & Udi Ben-Zvi & Tomer D. Mann & Noam Bressler & Roni Cohen‐Fultheim & Amos A. Schaffer & Shalom Hillel Roth & Ziv Tzur & Erez Y. Levanon & Eli Eisenberg, 2022. "Landscape of adenosine-to-inosine RNA recoding across human tissues," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. Rok Grah & Tamar Friedlander, 2020. "The relation between crosstalk and gene regulation form revisited," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-24, February.
    16. Yue Yuan & Qiang Huo & Ziru Zhang & Qun Wang & Juanxia Wang & Shuaikang Chang & Peng Cai & Karen M. Song & David W. Galbraith & Weixiao Zhang & Long Huang & Rentao Song & Zeyang Ma, 2024. "Decoding the gene regulatory network of endosperm differentiation in maize," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Richard E. Lenski & Terence C. Burnham, 2018. "Experimental evolution of bacteria across 60,000 generations, and what it might mean for economics and human decision-making," Journal of Bioeconomics, Springer, vol. 20(1), pages 107-124, April.
    18. Joern Pezoldt & Carolin Wiechers & Mangge Zou & Maria Litovchenko & Marjan Biocanin & Michael Beckstette & Katarzyna Sitnik & Martina Palatella & Guido Mierlo & Wanze Chen & Vincent Gardeux & Stefan F, 2022. "Postnatal expansion of mesenteric lymph node stromal cells towards reticular and CD34+ stromal cell subsets," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Travis L. LaFleur & Ayaan Hossain & Howard M. Salis, 2022. "Automated model-predictive design of synthetic promoters to control transcriptional profiles in bacteria," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. Tomoyuki Ohno & Taichi Akase & Shunya Kono & Hikaru Kurasawa & Takuto Takashima & Shinya Kaneko & Yasunori Aizawa, 2022. "Biallelic and gene-wide genomic substitution for endogenous intron and retroelement mutagenesis in human cells," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60023-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.