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Integrated mobile genetic elements in Thaumarchaeota.

Mart Krupovic1, Kira S Makarova2, Yuri I Wolf2

  • 1Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, 75015, Paris, France.

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Mobile genetic elements (MGE) in Thaumarchaeota archaea were identified, revealing diverse types including proviruses and novel elements. These elements contribute to host adaptation and engage in gene exchange and antagonistic interactions.

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Area of Science:

  • Microbiology
  • Genomics
  • Molecular Biology

Background:

  • Thaumarchaeota archaea are globally abundant microorganisms involved in key biogeochemical cycles.
  • Mobile genetic elements (MGE) play crucial roles in microbial evolution and adaptation.
  • Understanding MGE diversity in Thaumarchaeota is essential for comprehending their ecological roles.

Purpose of the Study:

  • To investigate the diversity and characteristics of integrated MGE (iMGE) within Thaumarchaeota genomes.
  • To explore the functional implications of iMGE, including gene content and potential interactions.
  • To elucidate the evolutionary relationships and gene-sharing networks among thaumarchaeal MGE.

Main Methods:

  • Bioinformatic analysis of 20 thaumarchaeal genomes to identify integrated MGE.
  • Classification of iMGE into distinct categories based on sequence homology and structural features.
  • Comparative genomics to analyze gene content, identify auxiliary metabolic and stress response genes.
  • Network analysis to study gene sharing and potential interactions between MGE.

Main Results:

  • Identification of 2 Mbp of mobile DNA across 20 thaumarchaeal genomes, comprising five major iMGE classes: proviruses, casposons, insertion sequence-like transposons, integrative-conjugative elements, and cryptic integrated elements.
  • The majority of iMGE were cryptic elements, potentially representing novel viral or plasmid families. Proviruses showed relationships to Caudovirales and tailless icosahedral viruses.
  • Thaumarchaeal iMGE form a gene-sharing network, indicating pervasive gene exchange. They carry auxiliary metabolic genes (e.g., multicopper oxidases, AmoC) and stress response genes (e.g., UspA).
  • Several iMGE harbored type I-B CRISPR-Cas systems with spacers matching other iMGE, suggesting antagonistic interactions and co-evolutionary dynamics.

Conclusions:

  • Integrated MGE are diverse in Thaumarchaeota, encompassing known and potentially novel mobile element types.
  • iMGE contribute significantly to the adaptation and fitness of thaumarchaeal hosts through gene acquisition, including metabolic and stress response genes.
  • The identified gene-sharing network and CRISPR-Cas interactions highlight complex ecological dynamics and co-evolutionary relationships between MGE and their archaeal hosts.