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One Ring does not rule them all: Linear mtDNA in Metazoa.

Ehsan Kayal1, Dennis V Lavrov1

  • 1Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, USA.

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Summary

Linear mitochondrial genomes (mtDNA) are increasingly discovered in Metazoa, challenging the traditional circular model. This review explores their distribution, origins, and maintenance mechanisms, highlighting the importance of all available mtDNA data.

Keywords:
CnidariaIsopodaLinear mtDNAMitochondrial telomereOrigin linearityPorifera

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Area of Science:

  • Genomics and Molecular Biology
  • Evolutionary Biology
  • Zoology

Background:

  • Genome sequencing advances enable exploration of mitochondrial genome (mtDNA) architecture.
  • Whole genome sequencing provides access to unusual mtDNA organizations previously difficult to obtain.
  • A growing number of complete mtDNA sequences are available, especially for Metazoa.

Purpose of the Study:

  • To review the distribution of linear mtDNA across Metazoa, focusing on isopods, cnidarians, and sponges.
  • To discuss the multiple evolutionary origins of linear mitogenomes in these clades.
  • To summarize knowledge on mechanisms maintaining linear mtDNA integrity and caution against premature definitions of completeness.

Main Methods:

  • Literature review of existing studies on metazoan mitochondrial genomes.
  • Analysis of published data on linear mtDNA distribution and characteristics.
  • Synthesis of findings regarding origins and maintenance of linearity.

Main Results:

  • Linear mtDNA is found in non-bilaterian animals like isopods, cnidarians, and sponges, challenging the circular mtDNA paradigm.
  • Multiple independent origins of linearity are proposed, including plasmid insertion (cnidarians, sponges) and tRNA heteroplasmy (isopods).
  • Terminal repeats likely function as telomeres, maintaining linear mtDNA integrity.

Conclusions:

  • The popular view of metazoan mtDNA as exclusively circular is outdated.
  • Linear mtDNAs have diverse origins and utilize specific mechanisms for stability.
  • All available mtDNA data, including incomplete sequences, are valuable for phylogenetic and genomic studies.