The evolutionary landscape of prokaryotic chromosome/plasmid balance

Abstract The balance between chromosomal and plasmid DNAs determines the genomic plasticity of prokaryotes. Natural selections, acting on the level of organisms or plasmids, shape the abundances of plasmid DNAs in prokaryotic genomes. Despite the importance of plasmids in health and engineering, the...

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Main Authors: Wenzhi Xue, Juken Hong, Teng Wang
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07167-5
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author Wenzhi Xue
Juken Hong
Teng Wang
author_facet Wenzhi Xue
Juken Hong
Teng Wang
author_sort Wenzhi Xue
collection DOAJ
description Abstract The balance between chromosomal and plasmid DNAs determines the genomic plasticity of prokaryotes. Natural selections, acting on the level of organisms or plasmids, shape the abundances of plasmid DNAs in prokaryotic genomes. Despite the importance of plasmids in health and engineering, there have been rare systematic attempts to quantitatively model and predict the determinants underlying the strength of different selection forces. Here, we develop a metabolic flux model that describes the intracellular resource competition between chromosomal and plasmid-encoded reactions. By coarse graining, this model predicts a landscape of natural selections on chromosome/plasmid balance, which is featured by the tradeoff between phenotypic and non-phenotypic selection pressures. This landscape is further validated by the observed pattern of plasmid distributions in the vast collection of prokaryotic genomes retrieved from the NCBI database. Our results establish a universal paradigm to understand the prokaryotic chromosome/plasmid interplay and provide insights into the evolutionary origin of plasmid diversity.
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spelling doaj-art-e8a8cb7457e34039b074fb44ab711f642025-08-20T02:50:04ZengNature PortfolioCommunications Biology2399-36422024-11-017111010.1038/s42003-024-07167-5The evolutionary landscape of prokaryotic chromosome/plasmid balanceWenzhi Xue0Juken Hong1Teng Wang2Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of SciencesKey Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of SciencesKey Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of SciencesAbstract The balance between chromosomal and plasmid DNAs determines the genomic plasticity of prokaryotes. Natural selections, acting on the level of organisms or plasmids, shape the abundances of plasmid DNAs in prokaryotic genomes. Despite the importance of plasmids in health and engineering, there have been rare systematic attempts to quantitatively model and predict the determinants underlying the strength of different selection forces. Here, we develop a metabolic flux model that describes the intracellular resource competition between chromosomal and plasmid-encoded reactions. By coarse graining, this model predicts a landscape of natural selections on chromosome/plasmid balance, which is featured by the tradeoff between phenotypic and non-phenotypic selection pressures. This landscape is further validated by the observed pattern of plasmid distributions in the vast collection of prokaryotic genomes retrieved from the NCBI database. Our results establish a universal paradigm to understand the prokaryotic chromosome/plasmid interplay and provide insights into the evolutionary origin of plasmid diversity.https://doi.org/10.1038/s42003-024-07167-5
spellingShingle Wenzhi Xue
Juken Hong
Teng Wang
The evolutionary landscape of prokaryotic chromosome/plasmid balance
Communications Biology
title The evolutionary landscape of prokaryotic chromosome/plasmid balance
title_full The evolutionary landscape of prokaryotic chromosome/plasmid balance
title_fullStr The evolutionary landscape of prokaryotic chromosome/plasmid balance
title_full_unstemmed The evolutionary landscape of prokaryotic chromosome/plasmid balance
title_short The evolutionary landscape of prokaryotic chromosome/plasmid balance
title_sort evolutionary landscape of prokaryotic chromosome plasmid balance
url https://doi.org/10.1038/s42003-024-07167-5
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