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Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering
Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine).ORCID iD: 0000-0002-6367-821X
Indian Institute of Science Education and Research (IISER) Pune, Pune, India.
Umeå University, Faculty of Medicine, Umeå Centre for Microbial Research (UCMR). Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology).ORCID iD: 0000-0003-1510-8324
2023 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 14, no 1, article id 3555Article in journal (Refereed) Published
Abstract [en]

The evolutionary transition from unicellularity to multicellularity was a key innovation in the history of life. Experimental evolution is an important tool to study the formation of undifferentiated cellular clusters, the likely first step of this transition. Although multicellularity first evolved in bacteria, previous experimental evolution research has primarily used eukaryotes. Moreover, it focuses on mutationally driven (and not environmentally induced) phenotypes. Here we show that both Gram-negative and Gram-positive bacteria exhibit phenotypically plastic (i.e., environmentally induced) cell clustering. Under high salinity, they form elongated clusters of ~ 2 cm. However, under habitual salinity, the clusters disintegrate and grow planktonically. We used experimental evolution with Escherichia coli to show that such clustering can be assimilated genetically: the evolved bacteria inherently grow as macroscopic multicellular clusters, even without environmental induction. Highly parallel mutations in genes linked to cell wall assembly formed the genomic basis of assimilated multicellularity. While the wildtype also showed cell shape plasticity across high versus low salinity, it was either assimilated or reversed after evolution. Interestingly, a single mutation could genetically assimilate multicellularity by modulating plasticity at multiple levels of organization. Taken together, we show that phenotypic plasticity can prime bacteria for evolving undifferentiated macroscopic multicellularity.

Place, publisher, year, edition, pages
Springer Nature, 2023. Vol. 14, no 1, article id 3555
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:umu:diva-211144DOI: 10.1038/s41467-023-39320-9ISI: 001026275700029PubMedID: 37322016Scopus ID: 2-s2.0-85162005447OAI: oai:DiVA.org:umu-211144DiVA, id: diva2:1779790
Funder
Wenner-Gren Foundations, UPD2020-0113Wenner-Gren Foundations, UPD2021-0182Available from: 2023-07-04 Created: 2023-07-04 Last updated: 2025-04-24Bibliographically approved

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Chavhan, YashrajLind, Peter A

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Department of Molecular Biology (Faculty of Medicine)Umeå Centre for Microbial Research (UCMR)Department of Molecular Biology (Faculty of Science and Technology)
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