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Open Access Highly Accessed Research article

Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity

Mart Krupovic1*, Kira S Makarova2, Patrick Forterre1, David Prangishvili1 and Eugene V Koonin2*

Author Affiliations

1 Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, 25 rue du Docteur Roux, 75015 Paris, France

2 National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD 20894, USA

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BMC Biology 2014, 12:36  doi:10.1186/1741-7007-12-36

Published: 19 May 2014

Abstract

Background

Diverse transposable elements are abundant in genomes of cellular organisms from all three domains of life. Although transposons are often regarded as junk DNA, a growing body of evidence indicates that they are behind some of the major evolutionary innovations. With the growth in the number and diversity of sequenced genomes, previously unnoticed mobile elements continue to be discovered.

Results

We describe a new superfamily of archaeal and bacterial mobile elements which we denote casposons because they encode Cas1 endonuclease, a key enzyme of the CRISPR-Cas adaptive immunity systems of archaea and bacteria. The casposons share several features with self-synthesizing eukaryotic DNA transposons of the Polinton/Maverick class, including terminal inverted repeats and genes for B family DNA polymerases. However, unlike any other known mobile elements, the casposons are predicted to rely on Cas1 for integration and excision, via a mechanism similar to the integration of new spacers into CRISPR loci. We identify three distinct families of casposons that differ in their gene repertoires and evolutionary provenance of the DNA polymerases. Deep branching of the casposon-encoded endonuclease in the Cas1 phylogeny suggests that casposons played a pivotal role in the emergence of CRISPR-Cas immunity.

Conclusions

The casposons are a novel superfamily of mobile elements, the first family of putative self-synthesizing transposons discovered in prokaryotes. The likely contribution of capsosons to the evolution of CRISPR-Cas parallels the involvement of the RAG1 transposase in vertebrate immunoglobulin gene rearrangement, suggesting that recruitment of endonucleases from mobile elements as ready-made tools for genome manipulation is a general route of evolution of adaptive immunity.

Keywords:
Mobile genetic elements; CRISPR-Cas system; Adaptive immunity; Transposons; Archaea; DNA polymerases