Jure Tica, Martina Oliver Huidobro, Tong Zhu, Georg K A Wachter, Roozbeh H Pazuki, Dario G Bazzoli, Natalie S Scholes, Elisa Tonello, Heike Siebert, Michael P H Stumpf, Robert G Endres, Mark Isalan
{"title":"A three-node Turing gene circuit forms periodic spatial patterns in bacteria.","authors":"Jure Tica, Martina Oliver Huidobro, Tong Zhu, Georg K A Wachter, Roozbeh H Pazuki, Dario G Bazzoli, Natalie S Scholes, Elisa Tonello, Heike Siebert, Michael P H Stumpf, Robert G Endres, Mark Isalan","doi":"10.1016/j.cels.2024.11.002","DOIUrl":null,"url":null,"abstract":"<p><p>Turing patterns are self-organizing systems that can form spots, stripes, or labyrinths. Proposed examples in tissue organization include zebrafish pigmentation, digit spacing, and many others. The theory of Turing patterns in biology has been debated because of their stringent fine-tuning requirements, where patterns only occur within a small subset of parameters. This has complicated the engineering of synthetic Turing gene circuits from first principles, although natural genetic Turing networks have been identified. Here, we engineered a synthetic genetic reaction-diffusion system where three nodes interact according to a non-classical Turing network with improved parametric robustness. The system reproducibly generated stationary, periodic, concentric stripe patterns in growing E. coli colonies. A partial differential equation model reproduced the patterns, with a Turing parameter regime obtained by fitting to experimental data. Our synthetic Turing system can contribute to nanotechnologies, such as patterned biomaterial deposition, and provide insights into developmental patterning programs. A record of this paper's transparent peer review process is included in the supplemental information.</p>","PeriodicalId":93929,"journal":{"name":"Cell systems","volume":" ","pages":"1123-1132.e3"},"PeriodicalIF":0.0000,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cell systems","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1016/j.cels.2024.11.002","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/12/2 0:00:00","PubModel":"Epub","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Turing patterns are self-organizing systems that can form spots, stripes, or labyrinths. Proposed examples in tissue organization include zebrafish pigmentation, digit spacing, and many others. The theory of Turing patterns in biology has been debated because of their stringent fine-tuning requirements, where patterns only occur within a small subset of parameters. This has complicated the engineering of synthetic Turing gene circuits from first principles, although natural genetic Turing networks have been identified. Here, we engineered a synthetic genetic reaction-diffusion system where three nodes interact according to a non-classical Turing network with improved parametric robustness. The system reproducibly generated stationary, periodic, concentric stripe patterns in growing E. coli colonies. A partial differential equation model reproduced the patterns, with a Turing parameter regime obtained by fitting to experimental data. Our synthetic Turing system can contribute to nanotechnologies, such as patterned biomaterial deposition, and provide insights into developmental patterning programs. A record of this paper's transparent peer review process is included in the supplemental information.