Abstract
CRISPR-Cas is a genetic adaptive immune system unique to prokaryotic cells used to combat phage and plasmid threats. The host cell adapts by incorporating DNA sequences from invading phages or plasmids into its CRISPR locus as spacers. These spacers are expressed as mobile surveillance RNAs that direct CRISPR-associated (Cas) proteins to protect against subsequent attack by the same phages or plasmids. The threat from mobile genetic elements inevitably shapes the CRISPR loci of archaea and bacteria, and simultaneously the CRISPR-Cas immune system drives evolution of these invaders. Here, we highlight our recent work, as well as that of others, that seeks to understand phage mechanisms of CRISPR-Cas evasion and conditions for population coexistence of phages with CRISPR-protected prokaryotes.
This is a preview of subscription content, access via your institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DBT, Shmakov S, Makarova KS, Semenova E, Minakhin L, Severinov K, Regev A, Lander ES, Koonin EV, Zhang F (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353(6299):aaf5573
Al-Attar S, Westra ER, van der Oost J, Brouns SJ (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs): The hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol Chem 392(4):277–289
Andersson AF, Banfield Jillian F (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320(5879):1047–1050
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(5819):1709–1712
Berezovskaya FS, Wolf YI, Koonin EV, Karev GP (2014) Pseudo-chaotic oscillations in CRISPR-virus coevolution predicted by bifurcation analysis. Biol Direct 9(1):1–17
Berezovsky IN, Shakhnovich EI (2005) Physics and evolution of thermophilic adaptation. Proc Natl Acad Sci USA 102(36):12742–12747
Bhaya D, Davison M, Barrangou Rodolphe (2011) CRISPR-Cas systems in bacteria and archaea: Versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45:273–297
Bolotin A, Quinquis B, Sorokin A, Dusko Ehrlich S (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(8):2551–2561
Briner AE, Barrangou R (2016) Deciphering and shaping bacterial diversity through CRISPR. Curr Opin Microbiol 31:101–108
Childs LM, Held NL, Young MJ, Whitaker RJ, Weitz JS (2012) Multiscale model of CRISPR-induced coevolutionary dynamics: Diversification at the interface of Lamarck and Darwin. Evolution 66(7):2015–2029
Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau Sylvain (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190(4):1390–1400
Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475–493
Emerson JB, Andrade K, Thomas BC, Norman A, Allen EE, Heidelberg KB, Banfield JF (2013) Virus-host and CRISPR dynamics in archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea, 2013, p 370871
Haerter JO, Trusina A, Sneppen K (2011) Targeted bacterial immunity buffers phage diversity. J Virol 85(20):10554–10560
Han P, Deem MW (2017) Non-classical phase diagram for virus bacterial coevolution mediated by clustered regularly interspaced short palindromic repeats. J R Soc Interface 14(127):20160905
Han P, Niestemski LR, Barrick JE, Deem MW (2013) Physical model of the immune response of bacteria against bacteriophage through the adaptive CRISPR-Cas immune system. Phys Biol 10(2):025004
He J, Deem MW (2010) Heterogeneous diversity of spacers within CRISPR (clustered regularly interspaced short palindromic repeats). Phys Rev Lett 105(12):128102
Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D (2009) Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4(1):e4169
Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962):167–170
Horvath P, Coûté-Monvoisin A-C, Romero DA, Boyaval P, Fremaux C, Barrangou R (2009) Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 131(1):62–70
Howe A, Ringus DL, Williams RJ, Choo Z-N, Greenwald SM, Owens SM, Coleman ML, Meyer F, Chang EB (2015) Divergent responses of viral and bacterial communities in the gut microbiome to dietary disturbances in mice. ISME J 10:1217–1227
Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278
Iranzo J, Lobkovsky AE, Wolf YI, Koonin EV (2013) Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context. J Bacteriol 195(17):3834–3844
Jiang W, Maniv I, Arain F, Wang Y, Levin BR, Marraffini LA (2013) Dealing with the evolutionary downside of CRISPR immunity: bacteria and beneficial plasmids. PLoS Genet 9(9):e1003844
Koonin EV, Wolf YI (2015) Evolution of the CRISPR-Cas adaptive immunity systems in prokaryotes: Models and observations on virus-host coevolution. Mol BioSyst 11:20–27
Lander ES (2016) The heroes of CRISPR. Cell 164(1–2):18–28
Levin BR, Moineau S, Bushman M, Barrangou R (2013) The population and evolutionary dynamics of phage and bacteria with CRISPR—mediated immunity. PLoS Genet 9(3):e1003312
Lillestøl R, Redder P, Garrett RA, Brügger KIM (2006) A putative viral defence mechanism in archaeal cells. Archaea 2(1):59–72
Mahony J, van Sinderen D (2015) Novel strategies to prevent or exploit phages in fermentations, insights from phage–host interactions. Curr Opin Biotechnol 32:8–13
Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJM, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13(11):722–736
Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11(3):181–190
Maxwell KL (2016) Phages fight back: inactivation of the CRISPR-Cas bacterial immune system by anti-CRISPR proteins. PLoS Pathog 12(1):e1005282
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(10):1616–1625
Mojica FJM, Garca-Martnez J, Soria E, Diez-Villasenor C (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60(2):174–182
Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC, Barrangou R, Banfield JF (2015) CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. mBio 6(2):e00262-15
Pennisi E (2013) The CRISPR craze. Science 341(6148):833–836
Peters JM, Silvis MR, Zhao D, Hawkins JS, Gross CA, Qi LS (2015) Bacterial CRISPR: accomplishments and prospects. Curr Opin Microbiol 27:121–126
Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151(3):653–663
Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39(21):9275–9282
Scarpellini E, Ianiro G, Attili F, Bassanelli C, De Santis A, Gasbarrini A (2015) The human gut microbiota and virome: potential therapeutic implications. Dig Liver Dis 47(12):1007–1012
Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H et al (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38(7):779–786
Seed KD, Lazinski DW, Calderwood SB, Camilli A (2013) A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494(7438):489–491
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(3):181–186
Sorek R, Lawrence CM, Wiedenheft B (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Ann Rev Biochem 82:237–266
Sun CL, Barrangou R, Thomas BC, Horvath P, Fremaux C, Banfield JF (2013) Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol 15(2):463–470
Tyson GW, Banfield JF (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10(1):200–207
Weinberger AD, Wolf YI, Lobkovsky AE, Gilmore MS, Koonin EV (2012) Viral diversity threshold for adaptive immunity in prokaryotes. MBio 3(6):e00456–12
Yosef I, Manor M, Kiro R, Qimron U (2015) Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc Natl Acad Sci USA 112(23):7267–7272
Acknowledgements
This work was partially supported by the Center for Theoretical Biological Physics at Rice University, Houston, TX 77005, USA.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Bonomo, M.E., Deem, M.W. (2017). How the Other Half Lives: CRISPR-Cas’s Influence on Bacteriophages. In: Pontarotti, P. (eds) Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts. Springer, Cham. https://doi.org/10.1007/978-3-319-61569-1_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-61569-1_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-61568-4
Online ISBN: 978-3-319-61569-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)