Distribution and Phasing of Sequence Motifs That Facilitate CRISPR Adaptation

Overview

Journal Curr Biol

Publisher Cell Press

Specialty Biology

Date 2021 Jun 26

PMID 34174210

Citations 14

Authors

Andrew Santiago-Frangos

Murat Buyukyoruk

Tanner Wiegand

Pushya Krishna

Blake Wiedenheft

Affiliations

Soon will be listed here.

Abstract

CRISPR-associated proteins (Cas1 and Cas2) integrate foreign DNA at the "leader" end of CRISPR loci. Several CRISPR leader sequences are reported to contain a binding site for a DNA-bending protein called integration host factor (IHF). IHF-induced DNA bending kinks the leader of type I-E CRISPRs, recruiting an upstream sequence motif that helps dock Cas1-2 onto the first repeat of the CRISPR locus. To determine the prevalence of IHF-directed CRISPR adaptation, we analyzed 15,274 bacterial and archaeal CRISPR leaders. These experiments reveal multiple IHF binding sites and diverse upstream sequence motifs in a subset of the I-C, I-E, I-F, and II-C CRISPR leaders. We identify subtype-specific motifs and show that the phase of these motifs is critical for CRISPR adaptation. Collectively, this work clarifies the prevalence and mechanism(s) of IHF-dependent CRISPR adaptation and suggests that leader sequences and adaptation proteins may coevolve under the selective pressures of foreign genetic elements like plasmids or phages.

Citing Articles

SspA is a transcriptional regulator of CRISPR adaptation in E. coli.

Lopez S, Lee Y, Zhang K, Shipman S Nucleic Acids Res. 2024; 53(4).

PMID: 39727179 PMC: 11879090. DOI: 10.1093/nar/gkae1244.

Structure reveals why genome folding is necessary for site-specific integration of foreign DNA into CRISPR arrays.

Santiago-Frangos A, Henriques W, Wiegand T, Gauvin C, Buyukyoruk M, Graham A Nat Struct Mol Biol. 2023; 30(11):1675-1685.

PMID: 37710013 PMC: 10872659. DOI: 10.1038/s41594-023-01097-2.

Histones direct site-specific CRISPR spacer acquisition in model archaeon.

Watts E, Garrett S, Catchpole R, Clark L, Sanders T, Marshall C Nat Microbiol. 2023; 8(9):1682-1694.

PMID: 37550505 PMC: 10823912. DOI: 10.1038/s41564-023-01446-3.

Widespread CRISPR-derived RNA regulatory elements in CRISPR-Cas systems.

Shmakov S, Barth Z, Makarova K, Wolf Y, Brover V, Peters J Nucleic Acids Res. 2023; 51(15):8150-8168.

PMID: 37283088 PMC: 10450183. DOI: 10.1093/nar/gkad495.

Widespread CRISPR repeat-like RNA regulatory elements in CRISPR-Cas systems.

Shmakov S, Barth Z, Makarova K, Wolf Y, Brover V, Peters J bioRxiv. 2023; .

PMID: 37090614 PMC: 10120712. DOI: 10.1101/2023.03.03.530964.

References

Bolotin A, Quinquis B, Sorokin A, Ehrlich S . Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology (Reading). 2005; 151(Pt 8):2551-2561. DOI: 10.1099/mic.0.28048-0. View

Crooks G, Hon G, Chandonia J, Brenner S . WebLogo: a sequence logo generator. Genome Res. 2004; 14(6):1188-90. PMC: 419797. DOI: 10.1101/gr.849004. View

Mojica F, Diez-Villasenor C, Garcia-Martinez J, Soria E . Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol. 2005; 60(2):174-82. DOI: 10.1007/s00239-004-0046-3. View

Fu L, Niu B, Zhu Z, Wu S, Li W . CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012; 28(23):3150-2. PMC: 3516142. DOI: 10.1093/bioinformatics/bts565. View

Kim S, Loeff L, Colombo S, Jergic S, Brouns S, Joo C . Selective loading and processing of prespacers for precise CRISPR adaptation. Nature. 2020; 579(7797):141-145. DOI: 10.1038/s41586-020-2018-1. View

Li W, Godzik A . Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006; 22(13):1658-9. DOI: 10.1093/bioinformatics/btl158. View

Levo M, Segal E . In pursuit of design principles of regulatory sequences. Nat Rev Genet. 2014; 15(7):453-68. DOI: 10.1038/nrg3684. View

Jansen R, van Embden J, Gaastra W, Schouls L . Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol. 2002; 43(6):1565-75. DOI: 10.1046/j.1365-2958.2002.02839.x. View

Schleif R . DNA looping. Annu Rev Biochem. 1992; 61:199-223. DOI: 10.1146/annurev.bi.61.070192.001215. View

10.

Grant C, Bailey T, Noble W . FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011; 27(7):1017-8. PMC: 3065696. DOI: 10.1093/bioinformatics/btr064. View

11.

Richter C, Gristwood T, Clulow J, Fineran P . In vivo protein interactions and complex formation in the Pectobacterium atrosepticum subtype I-F CRISPR/Cas System. PLoS One. 2012; 7(12):e49549. PMC: 3513311. DOI: 10.1371/journal.pone.0049549. View

12.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

13.

Vorontsova D, Datsenko K, Medvedeva S, Bondy-Denomy J, Savitskaya E, Pougach K . Foreign DNA acquisition by the I-F CRISPR-Cas system requires all components of the interference machinery. Nucleic Acids Res. 2015; 43(22):10848-60. PMC: 4678832. DOI: 10.1093/nar/gkv1261. View

14.

Kobryn K, Naigamwalla D, Chaconas G . Site-specific DNA binding and bending by the Borrelia burgdorferi Hbb protein. Mol Microbiol. 2000; 37(1):145-55. DOI: 10.1046/j.1365-2958.2000.01981.x. View

15.

Wei Y, Chesne M, Terns R, Terns M . Sequences spanning the leader-repeat junction mediate CRISPR adaptation to phage in Streptococcus thermophilus. Nucleic Acids Res. 2015; 43(3):1749-58. PMC: 4330368. DOI: 10.1093/nar/gku1407. View

16.

Peters J, Makarova K, Shmakov S, Koonin E . Recruitment of CRISPR-Cas systems by Tn7-like transposons. Proc Natl Acad Sci U S A. 2017; 114(35):E7358-E7366. PMC: 5584455. DOI: 10.1073/pnas.1709035114. View

17.

Westra E, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski J, Best A . Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense. Curr Biol. 2015; 25(8):1043-9. DOI: 10.1016/j.cub.2015.01.065. View

18.

Petassi M, Hsieh S, Peters J . Guide RNA Categorization Enables Target Site Choice in Tn7-CRISPR-Cas Transposons. Cell. 2020; 183(7):1757-1771.e18. PMC: 7770071. DOI: 10.1016/j.cell.2020.11.005. View

19.

Pourcel C, Salvignol G, Vergnaud G . CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology (Reading). 2005; 151(Pt 3):653-663. DOI: 10.1099/mic.0.27437-0. View

20.

Connolly M, Arra A, Zvoda V, Steinbach P, Rice P, Ansari A . Static Kinks or Flexible Hinges: Multiple Conformations of Bent DNA Bound to Integration Host Factor Revealed by Fluorescence Lifetime Measurements. J Phys Chem B. 2018; 122(49):11519-11534. PMC: 8562321. DOI: 10.1021/acs.jpcb.8b07405. View