Comprehensive profiling of integrative conjugative elements (ICEs) in Mollicutes: distinct catalysts of gene flow and genome shaping

Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elu...

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Published inNAR genomics and bioinformatics Vol. 7; no. 2; p. lqaf083
Main Authors Chai, Zili, Guo, Zhiyun, Chen, Xinxin, Yang, Zilong, Wang, Xia, Zhang, Fengwei, Kang, Fuqiang, Liu, Wenting, Liang, Shuang, Ren, Hongguang, Yue, Junjie, Jin, Yuan
Format Journal Article
LanguageEnglish
Published England Oxford University Press 01.06.2025
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ISSN2631-9268
2631-9268
DOI10.1093/nargab/lqaf083

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Abstract Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, P = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that Ureaplasma ICE facilitates genetic exchange and the spread of antibiotic resistance gene tet(M) among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.
AbstractList Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, P = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that Ureaplasma ICE facilitates genetic exchange and the spread of antibiotic resistance gene tet(M) among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.
Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that ICE facilitates genetic exchange and the spread of antibiotic resistance gene among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.
Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, P = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that Ureaplasma ICE facilitates genetic exchange and the spread of antibiotic resistance gene tet(M) among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.
Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, P = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that Ureaplasma ICE facilitates genetic exchange and the spread of antibiotic resistance gene tet(M) among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have highlighted their rapid evolutionary capabilities and genetic exchange within individual genomes; however, their evolutionary trajectory remains elusive. By comprehensive screening 1433 available Mollicutes genomes, we revealed widespread horizontal gene transfer (HGT) in 83.9% of investigated species. These genes involve type IV secretion systems and DNA integration, inferring the unique role of integrative conjugative elements (ICEs) or integrative and mobilizable elements (IMEs) as self-transmissible genetic elements. We systematically identified 263 ICEs/IMEs across most Mollicutes genera, being intact or fragmented, showing a strong correlation with HGT frequency (cor 0.573, P = .002). Their transfer tendency was highlighted across species sharing ecological niches, notably in livestock-associated mycoplasmas and insect-vectored spiroplasmas. ICEs/IMEs not only act as gene shuttles ferrying various phenotypic genes, but also promote increased large-scale chromosomal transfer events, shaping the host genomes profoundly. Additionally, we provided novel evidence that Ureaplasma ICE facilitates genetic exchange and the spread of antibiotic resistance gene tet(M) among other pathogens. These findings suggest that, despite the gene-loss pressure associated with the compact genomes of Mollicutes, ICEs/IMEs play a crucial role by introducing substantial genetic resources, providing essential opportunities for evolutionary adaptation.
Author Kang, Fuqiang
Liang, Shuang
Chai, Zili
Guo, Zhiyun
Yue, Junjie
Wang, Xia
Zhang, Fengwei
Chen, Xinxin
Yang, Zilong
Liu, Wenting
Ren, Hongguang
Jin, Yuan
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Zili Chai, Zhiyun Guo and Xinxin Chen should be regarded as Joint First Authors.
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  ident: 2025062820064953400_B18
  article-title: Chromosomal gene transfer in Spiroplasma citri
  publication-title: Science
  doi: 10.1126/science.3261453
– volume: 44
  start-page: 6614
  year: 2016
  ident: 2025062820064953400_B44
  article-title: NCBI prokaryotic genome annotation pipeline
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkw569
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Snippet Mollicutes, known as the simplest bacteria with streamlined genomes, were traditionally thought to evolve mainly through gene loss. Recent studies have...
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SubjectTerms Conjugation, Genetic
Evolution, Molecular
Gene Flow
Gene Transfer, Horizontal
Genome, Bacterial
Phylogeny
Tenericutes - genetics
Title Comprehensive profiling of integrative conjugative elements (ICEs) in Mollicutes: distinct catalysts of gene flow and genome shaping
URI https://www.ncbi.nlm.nih.gov/pubmed/40585299
https://www.proquest.com/docview/3225872130
https://pubmed.ncbi.nlm.nih.gov/PMC12205969
Volume 7
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