Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes

PLoS Biology

Volumn 13, Issue 6, 2015, Pages 1-30

  Masri, Leila ^a,b,f   Branca, Antoine ^c,g   Sheppard, Anna E ^a,h   Papkou, Andrei ^a   Laehnemann, David ^a,b   Guenther, Patrick S ^b   Prahl, Swantje ^a   Saebelfeld, Manja ^a   Hollensteiner, Jacqueline ^d   Liesegang, Heiko ^d   Brzuszkiewicz, Elzbieta ^d   Daniel, Rolf ^d   Michiels, Nicolaas K ^b   Schulte, Rebecca D ^e   Kurtz, Joachim ^c   Rosenstiel, Philip ^a   Telschow, Arndt ^c   Bornberg Bauer, Erich ^c   Schulenburg, Hinrich ^a,b  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF OSNABRÜCK   (Germany)

^f INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^g UNIVERSITÉ PARIS SUD   (France)

^h UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CRY TOXIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; CRY TOXIN RECEPTORS, BACILLUS THURINGIENSIS;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL GENE; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; COEVOLUTION; EVOLUTIONARY ADAPTATION; GENE DOSAGE; GENOTYPE; HOST PATHOGEN INTERACTION; NONHUMAN; ANIMAL; BACTERIAL GENOME; EVOLUTION; GENETIC SELECTION; GENETICS; GENOMICS; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; VIRULENCE;

ANIMALIA; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; GENOME, BACTERIAL; GENOMICS; GENOTYPE; HOST-PATHOGEN INTERACTIONS; PHENOTYPE; RECEPTORS, CELL SURFACE; SELECTION, GENETIC; VIRULENCE;

EID: 84934767518     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002169     Document Type: Article

References (58)

1. Woolhouse ME, Webster JP, Domingo E, Charlesworth B, Levin BR. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet. 2002; 32: 569-577. PMID: 12457190
2. Schmid-Hempel P. Evolutionary parasitology. Oxford, UK: Oxford University Press; 2011.
3. Dybdahl MF, Jenkins CE, Nuismer SL. Identifying the molecular basis of host-parasite coevolution: merging models and mechanisms. Am Nat. 2014; 184: 1-13. doi: 10. 1086/676591 PMID: 24921596
4. Zaman L, Meyer JR, Devangam S, Bryson DM, Lenski RE, Ofria C. Coevolution Drives the Emergence of Complex Traits and Promotes Evolvability. Keller L, editor. PLoS Biol. 2014; 12: e1002023. doi: 10. 1371/journal. pbio. 1002023 PMID: 25514332
5. Weitz JS, Hartman H, Levin SA. Coevolutionary arms races between bacteria and bacteriophage. Proc Nat Acad Sci U S A. 2005; 102: 9535-9540. PMID: 15976021
6. Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev. 2014
7. Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010; 11: 539-548. doi: 10. 1038/nrg2812 PMID: 20585331
8. Karasov TL, Horton MW, Bergelson J. Genomic variability as a driver of plant-pathogen coevolution? Curr Opin Plant Biol. 2014; 18: 24-30. doi: 10. 1016/j. pbi. 2013. 12. 003 PMID: 24491596
9. Jousimo J, Tack AJM, Ovaskainen O, Mononen T, Susi H, Tollenaere C, et al. Disease ecology. Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science. 2014; 344: 1289-1293. doi: 10. 1126/science. 1253621 PMID: 24926021
10. Ebert D. Host-parasite coevolution: Insights from the Daphnia-parasite model system. Curr Opin Microbiol. 2008; 11: 290-301. doi: 10. 1016/j. mib. 2008. 05. 012 PMID: 18556238
11. King KC, Delph LF, Jokela J, Lively CM. The geographic mosaic of sex and the Red Queen. Curr Biol. 2009; 19: 1438-1441. doi: 10. 1016/j. cub. 2009. 06. 062 PMID: 19631541
12. Dupas S, Dubuffet A, Carton Y, Poirie M. Local, geographic and phylogenetic scales of coevolution in Drosophila-parasitoid interactions. Adv Parasitol. 2009; 70: 281-295. doi: 10. 1016/S0065-308X(09) 70011-9 PMID: 19773075
13. Morran LT, Schmidt OG, Gelarden IA, Parrish RC, Lively CM. Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex. Science. 2011; 333: 216-218. doi: 10. 1126/science. 1206360 PMID: 21737739
14. Kerr PJ. Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antiviral Res. 2012; 93: 387-415. doi: 10. 1016/j. antiviral. 2012. 01. 009 PMID: 22333483
15. Brockhurst MA, Koskella B. Experimental coevolution of species interactions. Trends Ecol Evol. 2013; 28: 367-375. doi: 10. 1016/j. tree. 2013. 02. 009 PMID: 23523051
16. Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, et al. Antagonistic coevolution accelerates molecular evolution. Nature. 2010; 464: 275-278. doi: 10. 1038/nature08798 PMID: 20182425
17. Kashiwagi A, Yomo T. Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Qb and Escherichia coli. PLoS Genet. 2011; 7: e1002188. doi: 10. 1371/journal. pgen. 1002188 PMID: 21829387
18. Scanlan PD, Hall AR, Lopez-Pascua LD, Buckling A. Genetic basis of infectivity evolution in a bacteriophage. Mol Ecol. 2011; 20: 981-989. doi: 10. 1111/j. 1365-294X. 2010. 04903. x PMID: 21073584
19. Poullain V, Gandon S, Brockhurst MA, Buckling A, Hochberg ME. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution. 2008; 62: 1-11. PMID: 18005153
20. Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, Lenski RE. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science. 2012; 335: 428-432. doi: 10. 1126/science. 1214449 PMID: 22282803
21. Schulte RD, Makus C, Hasert B, Michiels NK, Schulenburg H. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc Natl Acad Sci U S A. 2010; 107: 7359-7364. doi: 10. 1073/pnas. 1003113107 PMID: 20368449
22. Griffitts JS, Aroian RV. Many roads to resistance: how invertebrates adapt to Bt toxins. Bioessays. 2005; 27: 614-624. PMID: 15892110
23. Nielsen-LeRoux C, Gaudriault S, Ramarao N, Lereclus D, Givaudan A. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Curr Opin Microbiol. 2012; 15: 220-231. doi: 10. 1016/j. mib. 2012. 04. 006 PMID: 22633889
24. Schulte RD, Makus C, Hasert B, Michiels NK, Schulenburg H. Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proc Biol Sci. 2011; 278: 2832-2839. doi: 10. 1098/rspb. 2011. 0019 PMID: 21307053
25. Schulte RD, Hasert B, Makus C, Michiels NK, Schulenburg H. Increased responsiveness in feeding behaviour of Caenorhabditis elegans after experimental coevolution with its microparasite Bacillus thuringiensis. Biol Lett. 2012; 8: 234-236. doi: 10. 1098/rsbl. 2011. 0684 PMID: 21880622
26. Schulte RD, Makus C, Schulenburg H. Host-parasite coevolution favours parasite genetic diversity and horizontal gene transfer. J Evol Biol. 2013; 26: 1836-1840. doi: 10. 1111/jeb. 12174 PMID: 23865952
27. Masri L, Schulte RD, Timmermeyer N, Thanisch S, Crummenerl LL, Jansen G, et al. Sex differences in host defence interfere with parasite-mediated selection for outcrossing during host-parasite coevolution. Ecol Lett. 2013; 16: 461-468. doi: 10. 1111/ele. 12068 PMID: 23301667
28. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995; 57: 289-300.
29. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. Sticking together: building a biofilm the Bacillus subtilis way. Nature Reviews Microbiology. 2013; 11: 157-168. doi: 10. 1038/nrmicro2960 PMID: 23353768
30. Lopez D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harb Perspect Biol. 2010; 2: a000398. doi: 10. 1101/cshperspect. a000398 PMID: 20519345
31. Agaisse H, Lereclus D. How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol. 1995; 177: 6027-6032. PMID: 7592363
32. Sniegowski PD, Gerrish PJ. Beneficial mutations and the dynamics of adaptation in asexual populations. Philos Trans R Soc Lond B Biol Sci. 2010; 365: 1255-1263. doi: 10. 1098/rstb. 2009. 0290 PMID: 20308101
33. Morgan AD, Gandon S, Buckling A. The effect of migration on local adaptation in a coevolving host-parasite system. Nature. 2005; 437: 253-256. PMID: 16148933
34. Tellier A, Brown JK. Spatial heterogeneity, frequency-dependent selection and polymorphism in hostparasite interactions. BMC Evol Biol. 2011; 11: 319. doi: 10. 1186/1471-2148-11-319 PMID: 22044632
35. Wang J, Nakad R, Schulenburg H. Activation of the Caenorhabditis elegans FOXO family transcription factor DAF-16 by pathogenic Bacillus thuringiensis. Dev Comp Immunol. 2012; 37: 193-201. doi: 10. 1016/j. dci. 2011. 08. 016 PMID: 21945834
36. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW, et al. Population genomics: wholegenome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 2007; 5: e310. PMID: 17988176
37. Carsiotis M, Stocker BA, Weinstein DL, O'Brien AD. A Salmonella typhimurium virulence gene linked to flg. Infect Immun. 1989; 57: 3276-3280. PMID: 2680969
38. Ling JM, Moore RA, Surette MG, Woods DE. The mviN homolog in Burkholderia pseudomallei is essential for viability and virulence. Can J Microbiol. 2006; 52: 831-842. PMID: 17110975
39. Ulland TK, Buchan BW, Ketterer MR, Fernandes-Alnemri T, Meyerholz DK, Apicella MA, et al. Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence. J Immunol. 2010; 185: 2670-2674. doi: 10. 4049/ jimmunol. 1001610 PMID: 20679532
40. Wei JZ, Hale K, Carta L, Platzer E, Wong C, Fang SC, et al. Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A. 2003; 100: 2760-2765. PMID: 12598644
41. Bravo A, Gómez I, Porta H, García-Gómez BI, Rodriguez-Almazan C, Pardo L, et al. Evolution of Bacillus thuringiensis Cry toxins insecticidal activity: Evolution of Bt toxins. Microbial Biotechnology. 2013; 6: 17-26. doi: 10. 1111/j. 1751-7915. 2012. 00342. x PMID: 22463726
42. Crickmore N. The diversity of Bacillus thuringiensis d-endotoxins. In: Charles J, Delécluse A, Nielsen- LeRoux C, editors. Entomopathogenic bacteria: From laboratory to field application. Dordrecht: Kluwer Academic Publishers; 2000. pp. 65-79.
43. Teotonio H, Carvalho S, Manoel D, Roque M, Chelo IM. Evolution of outcrossing in experimental populations of Caenorhabditis elegans. PLoS ONE. 2012; 7: e35811. doi: 10. 1371/journal. pone. 0035811 PMID: 22540006
44. Stiernagle T. Maintenance of C. elegans. In: The C. elegans Research Community, editor. WormBook. 2006. p.
45. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature. 2008; 456: 53-59. doi: 10. 1038/nature07517 PMID: 18987734
46. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10: R25. doi: 10. 1186/gb-2009-10-3-r25 PMID: 19261174
47. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25: 1754-1760. doi: 10. 1093/bioinformatics/btp324 PMID: 19451168
48. Lee W-P, Stromberg MP, Ward A, Stewart C, Garrison EP, Marth GT. MOSAIK: A hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS ONE. 2014; 9: e90581. doi: 10. 1371/journal. pone. 0090581 PMID: 24599324
49. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics. 2008; 24: 713-714. doi: 10. 1093/bioinformatics/btn025 PMID: 18227114
50. Wu TD, Nacu S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010; 26: 873-881. doi: 10. 1093/bioinformatics/btq057 PMID: 20147302
51. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE. 2010; 5: e11147. doi: 10. 1371/journal. pone. 0011147 PMID: 20593022
52. Wei Z, Wang W, Hu P, Lyon GJ, Hakonarson H. SNVer: a statistical tool for variant calling in analysis of pooled or individual next-generation sequencing data. Nucleic Acids Res. 2011; 39: e132. doi: 10. 1093/nar/gkr599 PMID: 21813454
53. Team R. R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria; 2010.
54. Kim SY, Lohmueller KE, Albrechtsen A, Li Y, Korneliussen T, Tian G, et al. Estimation of allele frequency and association mapping using next-generation sequencing data. BMC Bioinformatics. 2011; 12: 231. doi: 10. 1186/1471-2105-12-231 PMID: 21663684
55. Ye K, Schulz MH, Long Q, Apweiler R, Ning Z. Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics. 2009; 25: 2865-28671. doi: 10. 1093/bioinformatics/btp394 PMID: 19561018
56. Abyzov A, Urban AE, Snyder M, Gerstein M. CNVnator: an approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing. Genome Res. 2011; 21: 974-984. doi: 10. 1101/gr. 114876. 110 PMID: 21324876
57. Yoon S, Xuan Z, Makarov V, Ye K, Sebat J. Sensitive and accurate detection of copy number variants using read depth of coverage. Genome Res. 2009; 19: 1586-1592. doi: 10. 1101/gr. 092981. 109 PMID: 19657104
58. Peng D, Luo Y, Guo S, Zeng H, Ju S, Yu Z, et al. Elaboration of an electroporation protocol for large plasmids and wild-type strains of Bacillus thuringiensis. J Appl Microbiol. 2009; 106: 1849-1858. doi: 10. 1111/j. 1365-2672. 2009. 04151. x PMID: 19291242