CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome

Genome Research

Volumn 22, Issue 10, 2012, Pages 1985-1994

  Stern, Adi ^a,c,d   Mick, Eran ^a,b   Tirosh, Itay ^a   Sagy, Or ^a   Sorek, Rotem ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE DNA; CONTIG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL IMMUNITY; BACTERIOPHAGE; CONTROLLED STUDY; CRISPR GENE; DNA STRUCTURE; ECOLOGICAL NICHE; FECES ANALYSIS; GENE CONSTRUCT; GENE LOCUS; GENE SEQUENCE; GENE TARGETING; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; INTESTINE FLORA; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL;

BACTERIA; BACTERIOPHAGES; GENOMICS; HUMANS; INTESTINES; METAGENOME;

BACTERIA (MICROORGANISMS);

EID: 84865169354     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.138297.112     Document Type: Article

References (40)

1. Andersson AF, Banfield JF. 2008. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320: 1047-1050. (Pubitemid 351929541)
2. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.
3. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. 2011. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474: 604-608.
4. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712. (Pubitemid 46515624)
5. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F. 2003. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185: 6220-6223. (Pubitemid 37248478)
6. Bryant DW Jr, Wong WK, Mockler TC. 2009. QSRA-a quality-value guided de novo short read assembler. BMC Bioinformatics 10: 69. doi: 10.1186/1471-2105-10- 69.
7. Chibani-Chennoufi S, Bruttin A, Dillmann ML, Brussow H. 2004. Phage-host interaction: An ecological perspective. J Bacteriol 186: 3677-3686. (Pubitemid 38746042)
8. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. 2006. Toward automatic reconstruction of a highly resolved tree of life. Science 311: 1283-1287. (Pubitemid 43334717)
9. Dethlefsen L, McFall-Ngai M, Relman DA. 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449: 811-818. (Pubitemid 47598621)
10. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science 308: 1635-1638. (Pubitemid 40807514)
11. Edgar RC. 2007. PILER-CR: Fast and accurate identification of CRISPR repeats. BMC Bioinformatics 8: 18. doi: 10.1186/1471-2105-8-18.
12. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
13. Edgar R, Qimron U. 2010. The Escherichia coli CRISPR system protects from λ lysogenization, lysogens, and prophage induction. J Bacteriol 192: 6291-6294.
14. Fouts DE. 2006. Phage-Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34: 5839-5851. (Pubitemid 44941163)
15. Hooper LV, Midtvedt T, Gordon JI. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22: 283-307. (Pubitemid 35221463)
16. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.
17. Karginov FV, Hannon GJ. 2010. The CRISPR system: Small RNA-guided defense in bacteria and archaea. Mol Cell 37: 7-19.
18. Krupovic M, Forterre P. 2011. Microviridae goes temperate: Microvirus-related proviruses reside in the genomes of Bacteroidetes. PLoS ONE 6: e19893. doi: 10.1371/journal.pone.0019893.
19. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, et al. 2007. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169-181.
20. Letarov A, Kulikov E. 2009. The bacteriophages in human- and animal body-associated microbial communities. J Appl Microbiol 107: 1-13.
21. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, et al. 2011. CDD: A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
22. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843.
23. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11: 181-190.
24. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. 2011. The human gut virome: Inter-individual variation and dynamic response to diet. Genome Res 21: 1616-1625.
25. Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, Banfield JF, Relman DA. 2011. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21: 126-136.
26. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
27. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. 2010. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466: 334-338.
28. Rohwer F. 2003. Global phage diversity. Cell 113: 141. (Pubitemid 36514964)
29. Salzberg SL, Delcher AL, Kasif S, White O. 1998. Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26: 544-548. (Pubitemid 28291582)
30. Snyder JC, Bateson MM, Lavin M, Young MJ. 2010. Use of cellular CRISPR (clusters of regularly interspaced short palindromic repeats) spacer-based microarrays for detection of viruses in environmental samples. Appl Environ Microbiol 76: 7251-7258.
31. Sorek R, Kunin V, Hugenholtz P. 2008. CRISPR - a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6: 181-186. (Pubitemid 351256313)
32. Stern A, Sorek R. 2011. The phage-host arms race: Shaping the evolution of microbes. Bioessays 33: 43-51.
33. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. 2010. Self-targeting by CRISPR: Gene regulation or autoimmunity? Trends Genet 26: 335-340.
34. Tadmor AD, Ottesen EA, Leadbetter JR, Phillips R. 2011. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333: 58-62.
35. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. 2007. The human microbiome project. Nature 449: 804-810. (Pubitemid 47598620)
36. Tyson GW, Banfield JF. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200-207.
37. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ. 2009. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34: 401-407.
38. Walter J, Ley RE. 2011. The human gut microbiome: Ecology and recent evolutionary changes. Annu Rev Microbiol. 65: 411-429.
39. Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, Sturino JM, Wood TK. 2010. Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1: 147. doi: 10.1038/ncomms1146.
40. Zhang T, Breitbart M, Lee WH, Run JQ, Wei CL, Soh SW, Hibberd ML, Liu ET, Rohwer F, Ruan Y. 2006. RNA viral community in human feces: Prevalence of plant pathogenic viruses. PLoS Biol 4: e3. doi: 10.1371/journal.pbio.0040003.