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

BMC Biol. 2014 May 19;12:36. doi: 10.1186/1741-7007-12-36.

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.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Archaea / genetics
  • Archaea / immunology
  • Archaeal Proteins / chemistry
  • Attachment Sites, Microbiological
  • Bacteria / genetics
  • Bacteria / immunology
  • Bacterial Proteins / chemistry
  • CRISPR-Cas Systems / genetics*
  • DNA Replication
  • DNA Transposable Elements / genetics*
  • DNA-Directed DNA Polymerase / metabolism
  • Genomic Islands / genetics
  • Immunity / genetics*
  • Models, Biological
  • Phylogeny
  • Prokaryotic Cells / immunology*
  • Prokaryotic Cells / metabolism*

Substances

  • Archaeal Proteins
  • Bacterial Proteins
  • DNA Transposable Elements
  • DNA-Directed DNA Polymerase