Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex

Abstract Background Numerous studies in the past have expanded our understanding of the genetic differences of global distributed cyanobacteria that originated around billions of years ago, however, unraveling how gene gain and loss drive the genetic evolution of cyanobacterial species, and the trad...

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Main Authors: Xian Zhang, Lijun Xiao, Jiahui Liu, Qibai Tian, Jiaqi Xie
Format: Article
Language:English
Published: BMC 2023-08-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09555-3
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author Xian Zhang
Lijun Xiao
Jiahui Liu
Qibai Tian
Jiaqi Xie
author_facet Xian Zhang
Lijun Xiao
Jiahui Liu
Qibai Tian
Jiaqi Xie
author_sort Xian Zhang
collection DOAJ
description Abstract Background Numerous studies in the past have expanded our understanding of the genetic differences of global distributed cyanobacteria that originated around billions of years ago, however, unraveling how gene gain and loss drive the genetic evolution of cyanobacterial species, and the trade-off of these evolutionary forces are still the central but poorly understood issues. Results To delineate the contribution of gene flow in mediating the hereditary differentiation and shaping the microbial evolution, a global genome-wide study of bloom-forming cyanobacterium, Microcystis aeruginosa species complex, provided robust evidence for genetic diversity, reflected by enormous variation in gene repertoire among various strains. Mathematical extrapolation showed an ‘open’ microbial pan-genome of M. aeruginosa species, since novel genes were predicted to be introduced after new genomes were sequenced. Identification of numerous horizontal gene transfer’s signatures in genome regions of interest suggested that genome expansion via transformation and phage-mediated transduction across bacterial lineage as an evolutionary route may contribute to the differentiation of Microcystis functions (e.g., carbohydrate metabolism, amino acid metabolism, and energy metabolism). Meanwhile, the selective loss of some dispensable genes at the cost of metabolic versatility is as a mean of adaptive evolution that has the potential to increase the biological fitness. Conclusions Now that the recruitment of novel genes was accompanied by a parallel loss of some other ones, a trade-off in gene content may drive the divergent differentiation of M. aeruginosa genomes. Our study provides a genetic framework for the evolution of M. aeruginosa species and illustrates their possible evolutionary patterns.
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spelling doaj.art-7eb8e6cf4d344aaebb50a733b219c6b02023-11-19T12:27:15ZengBMCBMC Genomics1471-21642023-08-0124111610.1186/s12864-023-09555-3Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complexXian Zhang0Lijun Xiao1Jiahui Liu2Qibai Tian3Jiaqi Xie4Department of Occupational and Environmental Health, Xiangya School of Public Health, Central South UniversityGuangdong Corps Hospital of Chinese People’s Armed Police ForcesDepartment of Occupational and Environmental Health, Xiangya School of Public Health, Central South UniversityDepartment of Occupational and Environmental Health, Xiangya School of Public Health, Central South UniversityHunan Food and Drug Vocational CollegeAbstract Background Numerous studies in the past have expanded our understanding of the genetic differences of global distributed cyanobacteria that originated around billions of years ago, however, unraveling how gene gain and loss drive the genetic evolution of cyanobacterial species, and the trade-off of these evolutionary forces are still the central but poorly understood issues. Results To delineate the contribution of gene flow in mediating the hereditary differentiation and shaping the microbial evolution, a global genome-wide study of bloom-forming cyanobacterium, Microcystis aeruginosa species complex, provided robust evidence for genetic diversity, reflected by enormous variation in gene repertoire among various strains. Mathematical extrapolation showed an ‘open’ microbial pan-genome of M. aeruginosa species, since novel genes were predicted to be introduced after new genomes were sequenced. Identification of numerous horizontal gene transfer’s signatures in genome regions of interest suggested that genome expansion via transformation and phage-mediated transduction across bacterial lineage as an evolutionary route may contribute to the differentiation of Microcystis functions (e.g., carbohydrate metabolism, amino acid metabolism, and energy metabolism). Meanwhile, the selective loss of some dispensable genes at the cost of metabolic versatility is as a mean of adaptive evolution that has the potential to increase the biological fitness. Conclusions Now that the recruitment of novel genes was accompanied by a parallel loss of some other ones, a trade-off in gene content may drive the divergent differentiation of M. aeruginosa genomes. Our study provides a genetic framework for the evolution of M. aeruginosa species and illustrates their possible evolutionary patterns.https://doi.org/10.1186/s12864-023-09555-3Microcystis aeruginosaGene flowHereditary differentiationAdaptive evolutionTrade-off
spellingShingle Xian Zhang
Lijun Xiao
Jiahui Liu
Qibai Tian
Jiaqi Xie
Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
BMC Genomics
Microcystis aeruginosa
Gene flow
Hereditary differentiation
Adaptive evolution
Trade-off
title Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
title_full Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
title_fullStr Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
title_full_unstemmed Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
title_short Trade-off in genome turnover events leading to adaptive evolution of Microcystis aeruginosa species complex
title_sort trade off in genome turnover events leading to adaptive evolution of microcystis aeruginosa species complex
topic Microcystis aeruginosa
Gene flow
Hereditary differentiation
Adaptive evolution
Trade-off
url https://doi.org/10.1186/s12864-023-09555-3
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AT jiahuiliu tradeoffingenometurnovereventsleadingtoadaptiveevolutionofmicrocystisaeruginosaspeciescomplex
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