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Nasty Viruses, Costly Plasmids, Population Dynamics, and the Conditions for Establishing and Maintaining CRISPR-Mediated Adaptive Immunity in Bacteria


Clustered, Regularly Interspaced Short Palindromic Repeats (CRISPR) abound in the genomes of almost all archaebacteria and nearly half the eubacteria sequenced. Through a genetic interference mechanism, bacteria with CRISPR regions carrying copies of the DNA of previously encountered phage and plasmids abort the replication of phage and plasmids with these sequences. Thus it would seem that protection against infecting phage and plasmids is the selection pressure responsible for establishing and maintaining CRISPR in bacterial populations. But is it? To address this question and provide a framework and hypotheses for the experimental study of the ecology and evolution of CRISPR, I use mathematical models of the population dynamics of CRISPR-encoding bacteria with lytic phage and conjugative plasmids. The results of the numerical (computer simulation) analysis of the properties of these models with parameters in the ranges estimated for Escherichia coli and its phage and conjugative plasmids indicate: (1) In the presence of lytic phage there are broad conditions where bacteria with CRISPR-mediated immunity will have an advantage in competition with non-CRISPR bacteria with otherwise higher Malthusian fitness. (2) These conditions for the existence of CRISPR are narrower when there is envelope resistance to the phage. (3) While there are situations where CRISPR-mediated immunity can provide bacteria an advantage in competition with higher Malthusian fitness bacteria bearing deleterious conjugative plasmids, the conditions for this to obtain are relatively narrow and the intensity of selection favoring CRISPR weak. The parameters of these models can be independently estimated, the assumption behind their construction validated, and the hypotheses generated from the analysis of their properties tested in experimental populations of bacteria with lytic phage and conjugative plasmids. I suggest protocols for estimating these parameters and outline the design of experiments to evaluate the validity of these models and test these hypotheses.


Vyšlo v časopise: Nasty Viruses, Costly Plasmids, Population Dynamics, and the Conditions for Establishing and Maintaining CRISPR-Mediated Adaptive Immunity in Bacteria. PLoS Genet 6(10): e32767. doi:10.1371/journal.pgen.1001171
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001171

Souhrn

Clustered, Regularly Interspaced Short Palindromic Repeats (CRISPR) abound in the genomes of almost all archaebacteria and nearly half the eubacteria sequenced. Through a genetic interference mechanism, bacteria with CRISPR regions carrying copies of the DNA of previously encountered phage and plasmids abort the replication of phage and plasmids with these sequences. Thus it would seem that protection against infecting phage and plasmids is the selection pressure responsible for establishing and maintaining CRISPR in bacterial populations. But is it? To address this question and provide a framework and hypotheses for the experimental study of the ecology and evolution of CRISPR, I use mathematical models of the population dynamics of CRISPR-encoding bacteria with lytic phage and conjugative plasmids. The results of the numerical (computer simulation) analysis of the properties of these models with parameters in the ranges estimated for Escherichia coli and its phage and conjugative plasmids indicate: (1) In the presence of lytic phage there are broad conditions where bacteria with CRISPR-mediated immunity will have an advantage in competition with non-CRISPR bacteria with otherwise higher Malthusian fitness. (2) These conditions for the existence of CRISPR are narrower when there is envelope resistance to the phage. (3) While there are situations where CRISPR-mediated immunity can provide bacteria an advantage in competition with higher Malthusian fitness bacteria bearing deleterious conjugative plasmids, the conditions for this to obtain are relatively narrow and the intensity of selection favoring CRISPR weak. The parameters of these models can be independently estimated, the assumption behind their construction validated, and the hypotheses generated from the analysis of their properties tested in experimental populations of bacteria with lytic phage and conjugative plasmids. I suggest protocols for estimating these parameters and outline the design of experiments to evaluate the validity of these models and test these hypotheses.


Zdroje

1. OchmanH

LawrenceJG

GroismanEA

2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405 299 304

2. KooninEV

MakarovaKS

AravindL

2001 Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55 709 742

3. HallRM

1997 Mobile gene cassettes and integrons: moving antibiotic resistance genes in gram-negative bacteria. Ciba Foundation Symposium 207 192 202; discussion 202–195

4. HallRM

1998 The role of gene cassettes and integrons in the horizontal transfer of genes in Gram-negative bacteria.

KadoMSaCI

Horizontral Gene Transfer New York Chapman & Hall 53 62

5. MazelD

DaviesJ

1999 Gene capture in : Response. Trends Microbiol 7 95

6. Rowe-MagnusDA

GueroutAM

PloncardP

DychincoB

DaviesJ

2001 The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc Natl Acad Sci U S A 98 652 657

7. BennettPM

1999 Integrons and gene cassettes: a genetic construction kit for bacteria. J Antimicrob Chemother 43 1 4

8. LevinBR

1980 Conditions for the existence of R-plasmids in bacterial populations Berln, Prague Aviceum, Springer 197 202

9. DahlbergC

ChaoL

2003 Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165 1641 1649

10. LindP

CTobin

BergO

KurlandC

AnderssonD

2010 Compensatory gene amplification restores fitness after inter-species gene replacements. Molecular Microbiology doi:10.1111/j.1365-2958.2009.07030.x

11. JohnsenPJ

LevinBR

2010 Adjusting to alien genes. Molecular Microbiology doi:10.1111/j.1365-2958.2010.07075.x

12. ThomasCM

NielsenKM

2005 Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3 711 721

13. BickleTA

KrugerDH

1993 Biology of DNA restriction. Microbiological Reviews 57 434 450

14. WilsonGG

MurrayNE

1991 Restriction and modification systems. Annual Review of Genetics 25 585 627

15. HorvathP

BarrangouR

2010 CRISPR/Cas, the immune system of bacteria and archaea. Science 327 167 170

16. MarraffiniLA

SontheimerEJ

2010 CRISPR interference RNA-directed adaptive immunity in bacteria and archea. Nature Reviews Genetics 11 181 190

17. BarrangouR

FremauxC

DeveauH

RichardsM

BoyavalP

2007 CRISPR provides acquired resistance against viruses in prokaryotes. Science 315 1709 1712

18. MarraffiniLA

SontheimerEJ

2008 CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322 1843 1845

19. van der OostJ

JoreMM

WestraER

LundgrenM

BrounsSJ

2009 CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34 401 407

20. SorokinVA

GelfandMS

ArtamonovaII

2010 Evolutionary dynamics of CRISPR systems in the Ocean metagenome. Appl Environ Microbiol

21. HeidelbergJF

NelsonWC

SchoenfeldT

BhayaD

2009 Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS One 4 e4169 doi:10.1371/journal.pone.0004169

22. AnderssonAF

BanfieldJF

2008 Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320 1047 1050

23. TysonGW

BanfieldJF

2008 Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10 200 207

24. ValePF

LittleTJ

2010 CRISPR-mediated phage resistance and the ghost of coevolution past. Proc Biol Sci

25. KooninEV

WolfYI

2009 Is evolution Darwinian or/and Lamarckian? Biol Direct 4 42

26. MonodJ

1949 The growth of bacterial cultures. Annual Review of Microbiology 3 371 394

27. StewartFM

LevinBR

1973 Resource partitioning and the outcome of interspecific competition: a model and some general considerations. American Naturalist 107 171 198

28. LevinBR

StewartFM

ChaoL

1977 Resource - limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. American Naturalist 977 3 24

29. StewartFM

LevinBR

1977 The population biology of bacterial plasmids: a priori conditions for the existence of conjugationally transmitted factors. Genetics 87 209 228

30. SchragS

MittlerJE

1996 Host parasite coexistence: the role of spatial refuges in stabilizing bacteria-phage interactions. American Naturalist 148 438 377

31. ChaoL

LevinBR

StewartFM

1977 A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58 369 378

32. EcLF Website 2010 www.eclf.net/chemostat

33. LabrieSJ

SamsonJE

MoineauS

2010 Bacteriophage resistance mechanisms. Nat Rev Microbiol 8 317 327

34. StewartFM

LevinBR

1977 The Population Biology of Bacterial Plasmids: A PRIORI Conditions for the Existence of Conjugationally Transmitted Factors. Genetics 87 209 228

35. JansenR

EmbdenJD

GaastraW

SchoulsLM

2002 Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43 1565 1575

36. WeiY

OcampoP

LevinBR

(Under Review) An Experimental Study of the Population and Evolutionary Dynamics of Vibrio cholerae O1 and the Bacteriophage JSF4. Proc Royal Soc, B

37. LevinBR

Conditions for the existence of R-plasmids in bacterial populations.

SM

LR

KrcmeryV

1980; Smolenice, Czechoslovakia. Springer Verlag 197 202

38. LevinBR

StewartFM

RiceVA

1979 The kinetics of conjugative plasmid transmission: fit of a simple mass action model. Plasmid 2 247 260

39. SimonsenL

1990 Dynamics of plasmid transfer on surfaces. J Gen Microbiol 136 ( Pt 6) 1001 1007

40. BergstromCT

LipsitchM

LevinBR

2000 Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155 1505 1519

41. LundquistPD

LevinBR

1986 Transitory derepression and the maintenance of conjugative plasmids. Genetics 113 483 497

42. LevinBR

RiceVA

1980 The kinetics of transfer of nonconjugative plasmids by mobilizing conjugative factors. Genetical Research 35 241 259

43. SimonsenL

GordonDM

StewartFM

LevinBR

1990 Estimating the rate of plasmid transfer: an end-point method. Journal of General Microbiology 136 2319 2325

44. LuriaSE

DelbruckM

1943 Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics 28 491 511

45. JonesME

ThomasSM

RogersA

1994 Luria-Delbruck fluctuation experiments: design and analysis. Genetics 136 1209 1216

46. LenskiRE

LevinBR

1985 Constraints on the coevolution of bacteria and virulent phage : a model, some experiments, and predictions for natural communities. American Naturalist 125 585 602

47. KoronaR

LevinBR

1993 Phage-mediated selection and the evolution and maintenance of restriction-modification. Evolution 47 556 575

48. WeigleJJ

DelbrückM

1952 Mutual exclusion by an infecting phage and a carried phage. J Bacteriology 62

49. LevinSA

UdovicJD

1977 A mathematical model of coevolving populations. American Naturalist 111 657 675

50. BohannanBJM

LenskiRE

2000 Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3 362 377

51. BucklingA

RaineyPB

2002 Antagonistic coevolution between a bacterium and a bacteriophage. Proc R Soc Lond B Biol Sci 269 931 936

52. WeitzJS

HartmanH

LevinSA

2005 Coevolutionary arms races between bacteria and bacteriophage. Proc Natl Acad Sci U S A 102 9535 9540

53. FordeSE

BeardmoreRE

GudeljI

ArkinSS

ThompsonJN

2008 Understanding the limits to generalizability of experimental evolutionary models. Nature 455 220 223

54. SummersWC

2001 Bacteriophage therapy. Annu Rev Microbiol 55 437 451

55. FaruqueSM

NaserIB

IslamMJ

FaruqueAS

GhoshAN

2005 Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci U S A 102 1702 1707

56. FaruqueSM

IslamMJ

AhmadQS

FaruqueAS

SackDA

2005 Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage. Proc Natl Acad Sci U S A 102 6119 6124

57. LevinBR

BullJJ

2004 Population and evolutionary biology of phage therapy. Nature Review Microbiology 2 166 173

58. JensenMA

FaruqueSM

MekalanosJJ

LevinBR

2006 Modeling the role of bacteriophage in the control of cholera outbreaks. Proc Natl Acad Sci U S A 103 4652 4657

59. AbedonST

2009 Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog Dis 6 807 815

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