Holding a grudge: Persisting anti-phage CRISPR immunity in multiple human gut microbiomes

RNA Biology

Volumn 10, Issue 5, 2013, Pages 900-906

  Mick, Eran ^a   AdiStern, ^b,c   Sorek, Rotem ^d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

CRISPR; Human gut; Human microbiome; Lysogeny; Phages; Prophages

Indexed keywords

ADAPTIVE IMMUNITY; BACTERIAL STRAIN; BACTERIOPHAGE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENOME; HUMAN; IMMUNITY; INTESTINE FLORA; LYSOGENIZATION; METAGENOMICS; MOLECULAR ECOLOGY; NONHUMAN; NOTE; ADULT; ARCHAEON; BACTERIA; FEMALE; GASTROINTESTINAL TRACT; GENE TARGETING; GENETICS; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; PHYSIOLOGY; VIROLOGY;

CRISPR ASSOCIATED PROTEIN; SPACER DNA;

ADULT; ARCHAEA; BACTERIA; BACTERIOPHAGES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; DNA, INTERGENIC; FEMALE; GASTROINTESTINAL TRACT; GENE TARGETING; HUMANS; LYSOGENY; MALE; METAGENOMICS; MICROBIOTA; MIDDLE AGED;

EID: 84879007876     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.23929     Document Type: Note

References (76)

1. Chibani-Chennoufi S, Bruttin A, Dillmann ML, Brüssow H. Phage-host interaction: an ecological perspective. J Bacteriol 2004; 186:3677-86; PMID:15175280; http://dx.doi.org/10.1128/JB.186.12.3677-3686.2004.
2. Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasić L, Thingstad TF, Rohwer F, et al. Explaining microbial population genomics through phage predation. Nat Rev Microbiol 2009; 7:828-36; PMID:19834481; http://dx.doi. org/10.1038/nrmicro2235.
3. Weinbauer MG, Rassoulzadegan F. Are viruses driving microbial diversification and diversity? Environ Microbiol 2004; 6:1-11; PMID:14686936; http://dx.doi.org/10.1046/j.1462-2920.2003.00539.x.
4. Stern A, Sorek R. The phage-host arms race: shaping the evolution of microbes. Bioessays 2011; 33:43-51; PMID:20979102; http://dx.doi.org/10.1002/ bies.201000071.
5. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315:1709-12; PMID:17379808; http://dx.doi.org/10.1126/science.1138140.
6. Sorek R, Kunin V, Hugenholtz P. CRISPR - a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 2008; 6:181-6; PMID:18157154; http:// dx.doi.org/10.1038/nrmicro1793.
7. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 2009; 34:401-7; PMID:19646880; http://dx.doi.org/10.1016/j.tibs.2009.05.002.
8. Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science 2010; 327:167-70; PMID:20056882; http://dx.doi.org/10.1126/ science.1179555.
9. Karginov FV, Hannon GJ. The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol Cell 2010; 37:7-19; PMID:20129051; http://dx.doi.org/10.1016/j.molcel.2009.12.033.
10. Marraffini LA, Sontheimer EJ. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 2010; 11:181-90; PMID:20125085; http://dx.doi.org/10.1038/nrg2749.
11. Deveau H, Garneau JE, Moineau S. CRISPR/ Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 2010; 64:475-93; PMID:20528693; http://dx.doi.org/10.1146/annurev.micro.112408.134123.
12. Levin BR. Nasty viruses, costly plasmids, population dynamics, and the conditions for establishing and maintaining CRISPR-mediated adaptive immunity in bacteria. PLoS Genet 2010; 6:e1001171; PMID:21060859; http://dx.doi.org/10. 1371/journal.pgen.1001171.
13. Childs LM, Held NL, Young MJ, Whitaker RJ, Weitz JS. Multiscale model of CRISPR-induced coevolutionary dynamics: diversification at the interface of Lamarck and Darwin. Evolution 2012; 66:2015-29; PMID:22759281; http://dx.doi.org/10.1111/j.1558-5646.2012.01595.x.
14. Weinberger AD, Wolf YI, Lobkovsky AE, Gilmore MS, Koonin EV. Viral diversity threshold for adaptive immunity in prokaryotes. MBio 2012; 3:e00456-12; PMID:23221803; http://dx.doi.org/10.1128/mBio.00456-12.
15. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004; 304:66-74; PMID:15001713; http://dx.doi.org/10.1126/science.1093857.
16. Tringe SG, Rubin EM. Metagenomics: DNA sequencing of environmental samples. Nat Rev Genet 2005; 6:805-14; PMID:16304596; http://dx.doi.org/10.1038/ nrg1709.
17. Rohwer F. Global phage diversity. Cell 2003; 113:141; PMID:12705861; http://dx.doi.org/10.1016/S0092-8674(03)00276-9.
18. Hatfull GF, Hendrix RW. Bacteriophages and their genomes. Curr Opin Virol 2011; 1:298-303; PMID:22034588; http://dx.doi.org/10.1016/j.coviro.2011.06.009.
19. Rosario K, Breitbart M. Exploring the viral world through metagenomics. Curr Opin Virol 2011; 1:289-97; PMID:22440785; http://dx.doi.org/10.1016/j. coviro.2011.06.004.
20. Tadmor AD, Ottesen EA, Leadbetter JR, Phillips R. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 2011; 333:58-62; PMID:21719670; http://dx.doi.org/10.1126/science.1200758.
21. Andersson AF, Banfield JF. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 2008; 320:1047-50; PMID:18497291; http://dx.doi.org/10.1126/science.1157358.
22. Sorokin VA, Gelfand MS, Artamonova II. Evolutionary dynamics of clustered irregularly interspaced short palindromic repeat systems in the ocean metagenome. Appl Environ Microbiol 2010; 76:2136-44; PMID:20118362; http://dx.doi.org/10.1128/AEM.01985-09.
23. Anderson RE, Brazelton WJ, Baross JA. Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol Ecol 2011; 77:120-33; PMID:21410492; http://dx.doi.org/10.1111/j.1574-6941.2011.01090.x.
24. Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D. Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS One 2009; 4:e4169; PMID:19132092; http://dx.doi.org/10. 1371/journal.pone.0004169.
25. Held NL, Whitaker RJ. Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ Microbiol 2009; 11:457-66; PMID:19196276; http://dx.doi.org/10.1111/j.1462-2920.2008.01784.x.
26. Snyder JC, Bateson MM, Lavin M, Young MJ. Use of cellular CRISPR (clusters of regularly interspaced short palindromic repeats) spacer-based microarrays for detection of viruses in environmental samples. Appl Environ Microbiol 2010; 76:7251-8; PMID:20851987; http://dx.doi.org/10.1128/AEM.01109- 10.
27. Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, et al. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 2011; 21:126-36; PMID:21149389; http://dx.doi.org/10.1101/gr.111732.110.
28. Stern A, Mick E, Tirosh I, Sagy O, Sorek R. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res 2012; 22:1985-94; PMID:22732228; http://dx.doi.org/10.1101/gr.138297.112.
29. Rho M, Wu YW, Tang H, Doak TG, Ye Y. Diverse CRISPRs evolving in human microbiomes. PLoS Genet 2012; 8:e1002441; PMID:22719260; http://dx.doi.org/10. 1371/journal.pgen.1002441.
30. Pride DT, Salzman J, Relman DA. Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ Microbiol 2012; 14:2564-76; PMID:22583485; http://dx.doi.org/10.1111/j.1462-2920.2012.02775.x.
31. 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 2005; 151:653-63; PMID:15758212; http://dx.doi.org/10.1099/mic.0.27437-0.
32. Lillestøl RK, Redder P, Garrett RA, Brügger K. A putative viral defence mechanism in archaeal cells. Archaea 2006; 2:59-72; PMID:16877322; http://dx.doi.org/10.1155/2006/542818.
33. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 2008; 190:1390-400; PMID:18065545; http://dx.doi.org/10.1128/JB.01412-07.
34. Erdmann S, Garrett RA. Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol Microbiol 2012; 85:1044-56; PMID:22834906; http://dx.doi.org/10.1111/j.1365- 2958.2012.08171.x.
35. Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H, Moineau S, et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 2008; 190:1401-12; PMID:18065539; http://dx.doi.org/10.1128/JB.01415-07.
36. Held NL, Herrera A, Cadillo-Quiroz H, Whitaker RJ. CRISPR associated diversity within a population of Sulfolobus islandicus. PLoS One 2010; 5:e12988; PMID:20927396; http://dx.doi.org/10.1371/journal.pone.0012988.
37. Tyson GW, Banfield JF. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 2008; 10:200-7; PMID:17894817.
38. Díez-Villaseñor C, Almendros C, García- Martínez J, Mojica FJ. Diversity of CRISPR loci in Escherichia coli. Microbiology 2010; 156:1351-61; PMID:20133361; http://dx.doi.org/10.1099/mic.0. 036046-0.
39. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, et al. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 2012; 85:1057-71; PMID:22834929; http://dx.doi.org/10.1111/j.1365-2958.2012.08172.x.
40. Blumberg R, Powrie F. Microbiota, disease, and back to health: a metastable journey. Sci Transl Med 2012; 4:rv7; PMID:22674557; http://dx.doi.org/10.1126/scitranslmed.3004184.
41. Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci USA 2012; 109:594-9; PMID:22184244; http://dx.doi.org/10.1073/pnas.1116053109.
42. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490:55- 60; PMID:23023125; http://dx.doi.org/10.1038/nature11450.
43. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 2007; 449:804-10; PMID:17943116; http://dx.doi.org/10.1038/nature06244.
44. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al.; MetaHIT Consortium. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464:59-65; PMID:20203603; http://dx.doi.org/10.1038/nature08821.
45. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature 2012; 486:222-7; PMID:22699611.
46. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 2011; 108(Suppl 1):4578-85; PMID:20668239; http://dx.doi.org/10.1073/pnas.1000081107.
47. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 2013; 23:111-20; PMID:22936250; http://dx.doi.org/10.1101/gr.142315.112.
48. Schloissnig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, et al. Genomic variation landscape of the human gut microbiome. Nature 2013; 493:45-50; PMID:23222524; http://dx.doi.org/10.1038/nature11711.
49. Kuo CH, Ochman H. Deletional bias across the three domains of life. Genome Biol Evol 2009; 1:145-52; PMID:20333185; http://dx.doi.org/10.1093/gbe/ evp016.
50. Jansen R, Embden JD, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 2002; 43:1565-75; PMID:11952905; http://dx.doi.org/10.1046/j.1365-2958.2002.02839.x.
51. Touchon M, Rocha EP. The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS One 2010; 5:e11126; PMID:20559554; http://dx.doi.org/10.1371/journal.pone.0011126.
52. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science 2005; 308:1635-8; PMID:15831718; http://dx.doi.org/10.1126/science.1110591.
53. Weinberger AD, Sun CL, Pluciński MM, Denef VJ, Thomas BC, Horvath P, et al. Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput Biol 2012; 8:e1002475; PMID:22532794; http://dx.doi.org/10.1371/journal. pcbi.1002475.
54. Brodt A, Lurie-Weinberger MN, Gophna U. CRISPR loci reveal networks of gene exchange in archaea. Biol Direct 2011; 6:65; PMID:22188759; http://dx.doi.org/10.1186/1745-6150-6-65.
55. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010; 466:334-8; PMID:20631792; http://dx.doi.org/10.1038/nature09199.
56. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 2011; 21:1616-25; PMID:21880779; http://dx.doi.org/10.1101/gr.122705.111.
57. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, et al. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 2003; 185:6220-3; PMID:14526037; http://dx.doi. org/10.1128/JB.185.20. 6220-6223.2003.
58. Kim MS, Park EJ, Roh SW, Bae JW. Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol 2011; 77:8062-70; PMID:21948823; http://dx.doi.org/10.1128/AEM.06331-11.
59. Fineran PC, Charpentier E. Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 2012; 434:202-9; PMID:23123013; http://dx.doi.org/10.1016/j.virol.2012.10.003.
60. Sun CL, Barrangou R, Thomas BC, Horvath P, Fremaux C, Banfield JF. Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol 2013; 15:463-70; PMID:23057534; http://dx.doi.org/10.1111/j. 1462-2920.2012.02879.x.
61. Edgar R, Qimron U. The Escherichia coli CRISPR system protects from ë lysogenization, lysogens, and prophage induction. J Bacteriol 2010; 192:6291-4; PMID:20889749; http://dx.doi.org/10.1128/JB.00644-10.
62. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet 2010; 26:335-40; PMID:20598393; http://dx.doi.org/10.1016/j.tig.2010.05.008.
63. Gudbergsdottir S, Deng L, Chen Z, Jensen JVK, Jensen LR, She Q, et al. Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol Microbiol 2011; 79:35-49; PMID:21166892; http://dx.doi.org/10.1111/j.1365-2958. 2010.07452.x.
64. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. Genomic island variability facilitates Prochlorococcusvirus coexistence. Nature 2011; 474:604-8; PMID:21720364; http://dx.doi.org/10.1038/nature10172.
65. Young JC, Dill BD, Pan C, Hettich RL, Banfield JF, Shah M, et al. Phage-induced expression of CRISPR-associated proteins is revealed by shotgun proteomics in Streptococcus thermophilus. PLoS One 2012; 7:e38077; PMID:22666452; http://dx.doi.org/10.1371/journal.pone.0038077.
66. Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, Shinkai A. Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J Mol Biol 2010; 395:270-81; PMID:19891975; http://dx.doi.org/10. 1016/j.jmb.2009.10.057.
67. Deng L, Garrett RA, Shah SA, Peng X, She Q. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus . Mol Microbiol 2013; In press; PMID:23320564; http://dx.doi.org/10.1111/mmi.12152.
68. Makarova KS, Anantharaman V, Aravind L, Koonin EV. Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes. Biol Direct 2012; 7:40; PMID:23151069; http://dx.doi.org/10.1186/ 1745-6150-7-40.
69. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 2013; 493:429-32; PMID:23242138; http://dx.doi.org/10.1038/nature11723.
70. Skennerton CT, Angly FE, Breitbart M, Bragg L, He S, McMahon KD, et al. Phage encoded H-NS: a potential achilles heel in the bacterial defence system. PLoS One 2011; 6:e20095; PMID:21625595; http://dx.doi.org/10.1371/journal.pone. 0020095.
71. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 2009; 155:733-40; PMID:19246744; http://dx.doi.org/10.1099/mic.0.023960-0.
72. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli . Nucleic Acids Res 2011; 39:9275-82; PMID:21813460; http://dx.doi.org/10.1093/nar/gkr606.
73. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J Bacteriol 2009; 191:210-9; PMID:18952788; http://dx.doi.org/10.1128/JB.00797-08.
74. Cady KC, White AS, Hammond JH, Abendroth MD, Karthikeyan RS, Lalitha P, et al. Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 2011; 157:430-7; PMID:21081758; http://dx.doi.org/10.1099/mic.0. 045732-0.
75. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J Bacteriol 2012; 194:5728-38; PMID:22885297; http://dx.doi.org/10.1128/JB.01184-12.
76. Li M, Liu H, Han J, Liu J, Wang R, Zhao D, et al. Characterization of CRISPR RNA biogenesis and Cas6-cleavage mediated inhibition of a provirus in the haloarchaeon Haloferax mediterranei. J Bacteriol 2013; 195:867-75; PMID:23243301; http://dx.doi.org/10.1128/JB.01688-12.