CRISPR loci reveal networks of gene exchange in archaea

Abstract

Background: CRISPR (Clustered, Regularly, Interspaced, Short, Palindromic Repeats) loci provide prokaryotes with an adaptive immunity against viruses and other mobile genetic elements. CRISPR arrays can be transcribed and processed into small crRNA molecules, which are then used by the cell to target the foreign nucleic acid. Since spacers are accumulated by active CRISPR/Cas systems, the sequences of these spacers provide a record of the past "infection history" of the organism.

Results: Here we analyzed all currently known spacers present in archaeal genomes and identified their source by DNA similarity. While nearly 50% of archaeal spacers matched mobile genetic elements, such as plasmids or viruses, several others matched chromosomal genes of other organisms, primarily other archaea. Thus, networks of gene exchange between archaeal species were revealed by the spacer analysis, including many cases of inter-genus and inter-species gene transfer events. Spacers that recognize viral sequences tend to be located further away from the leader sequence, implying that there exists a selective pressure for their retention.

Conclusions: CRISPR spacers provide direct evidence for extensive gene exchange in archaea, especially within genera, and support the current dogma where the primary role of the CRISPR/Cas system is anti-viral and anti-plasmid defense.

Open peer review: This article was reviewed by: Profs. W. Ford Doolittle, John van der Oost, Christa Schleper (nominated by board member Prof. J Peter Gogarten).

Figure 1

Average number of CRISPR spacers per phylum, normalized by the number of spacer-containing genomes. Error bars represent standard error of the mean.

Figure 2

The function distribution of the filtered hits according to the target gene, where the target is a coding sequence, or the gene closest to the sequence match.

Figure 3

A schematic phylogenetic tree of organisms that have contributed spacer sequences to archaea. The direction of arrows points from the spacer towards its match. Red arrows, within genus matches; purple arrow, between genera matches; black arrows- matches between families, classes or domains; blue arrows, the match is to a virus known to infect that species (not including provirus sequences within genomes of cellular organisms). Boxes denote number of spacer hits between two organisms, absence of a box denoting a single match. "@", "#" equal best hits. Within species matches are not shown.

Figure 4

Distribution of the fractions of between-species (light blue) and within species (dark blue) spacer hits according to their location in the CRISPR array.

Figure 5

The distribution of the normalized number of hits according to the location in the CRISPR array. Light - viral hits; dark non-viral hits. Each result was normalized, dividing by the number of matches in each location bin.