Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering
Abstract 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 firs...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-06-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-39320-9 |
| _version_ | 1797801360601645056 |
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| author | Yashraj Chavhan Sutirth Dey Peter A. Lind |
| author_facet | Yashraj Chavhan Sutirth Dey Peter A. Lind |
| author_sort | Yashraj Chavhan |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-03-13T04:49:17Z |
| format | Article |
| id | doaj.art-3572edbb367c46478f9549b96fe3fe53 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-13T04:49:17Z |
| publishDate | 2023-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-3572edbb367c46478f9549b96fe3fe532023-06-18T11:18:48ZengNature PortfolioNature Communications2041-17232023-06-0114111210.1038/s41467-023-39320-9Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clusteringYashraj Chavhan0Sutirth Dey1Peter A. Lind2Department of Molecular Biology, Umeå UniversityIndian Institute of Science Education and Research (IISER) PuneDepartment of Molecular Biology, Umeå UniversityAbstract 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.https://doi.org/10.1038/s41467-023-39320-9 |
| spellingShingle | Yashraj Chavhan Sutirth Dey Peter A. Lind Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering Nature Communications |
| title | Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| title_full | Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| title_fullStr | Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| title_full_unstemmed | Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| title_short | Bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| title_sort | bacteria evolve macroscopic multicellularity by the genetic assimilation of phenotypically plastic cell clustering |
| url | https://doi.org/10.1038/s41467-023-39320-9 |
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