#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Linking high GC content to the repair of double strand breaks in prokaryotic genomes


Autoři: Jake L. Weissman aff001;  William F. Fagan aff001;  Philip L. F. Johnson aff001
Působiště autorů: Department of Biology, University of Maryland - College Park, College Park, Maryland, United States of America aff001
Vyšlo v časopise: Linking high GC content to the repair of double strand breaks in prokaryotic genomes. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008493
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008493

Souhrn

Genomic GC content varies widely among microbes for reasons unknown. While mutation bias partially explains this variation, prokaryotes near-universally have a higher GC content than predicted solely by this bias. Debate surrounds the relative importance of the remaining explanations of selection versus biased gene conversion favoring GC alleles. Some environments (e.g. soils) are associated with a high genomic GC content of their inhabitants, which implies that either high GC content is a selective adaptation to particular habitats, or that certain habitats favor increased rates of gene conversion. Here, we report a novel association between the presence of the non-homologous end joining DNA double-strand break repair pathway and GC content; this observation suggests that DNA damage may be a fundamental driver of GC content, leading in part to the many environmental patterns observed to-date. We discuss potential mechanisms accounting for the observed association, and provide preliminary evidence that sites experiencing higher rates of double-strand breaks are under selection for increased GC content relative to the genomic background.

Klíčová slova:

Comparative genomics – DNA repair – Genomic databases – Homologous recombination – Phylogenetic analysis – Phylogenetics – Non-homologous end joining – Prokaryotic cells


Zdroje

1. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, et al. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science. 2006;314(5797):267–267. doi: 10.1126/science.1134196 17038615

2. Foerstner KU, von Mering C, Hooper SD, Bork P. Environments shape the nucleotide composition of genomes. EMBO reports. 2005 Dec;6(12):1208–1213. doi: 10.1038/sj.embor.7400538 16200051

3. Reichenberger ER, Rosen G, Hershberg U, Hershberg R. Prokaryotic nucleotide composition is shaped by both phylogeny and the environment. Genome Biology and Evolution. 2015 Apr;7(5):1380–1389. doi: 10.1093/gbe/evv063 25861819

4. Hershberg R, Petrov DA. Evidence That Mutation Is Universally Biased towards AT in Bacteria. PLOS Genetics. 2010 Sep;6(9):e1001115. Available from: http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1001115 20838599

5. Hildebrand F, Meyer A, Eyre-Walker A. Evidence of Selection upon Genomic GC-Content in Bacteria. PLOS Genetics. 2010 Sep;6(9):e1001107. Available from: http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1001107 20838593

6. Long H, Sung W, Kucukyildirim S, Williams E, Miller SF, Guo W, et al. Evolutionary determinants of genome-wide nucleotide composition. Nature Ecology & Evolution. 2018 Feb;2(2):237–240. Available from: https://www.nature.com/articles/s41559-017-0425-y.

7. Lassalle F, Périan S, Bataillon T, Nesme X, Duret L, Daubin V. GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands. PLOS Genetics. 2015 Feb;11(2):e1004941. Available from: http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1004941 25659072

8. Raghavan R, Kelkar YD, Ochman H. A selective force favoring increased G+ C content in bacterial genes. Proceedings of the National Academy of Sciences. 2012;109(36):14504–14507. doi: 10.1073/pnas.1205683109

9. Rocha EPC. Neutral Theory, Microbial Practice: Challenges in Bacterial Population Genetics. Molecular Biology and Evolution. 2018 Jun;35(6):1338–1347. Available from: https://academic.oup.com/mbe/article/35/6/1338/4976545 29684183

10. Bobay LM, Ochman H. Impact of recombination on the base composition of bacteria and archaea. Molecular biology and evolution. 2017;34(10):2627–2636. doi: 10.1093/molbev/msx189 28957503

11. Rocha EPC, Feil EJ. Mutational Patterns Cannot Explain Genome Composition: Are There Any Neutral Sites in the Genomes of Bacteria? PLOS Genetics. 2010 Sep;6(9):e1001104. Available from: http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1001104 20838590

12. Naya H, Romero H, Zavala A, Alvarez B, Musto H. Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. Journal of Molecular Evolution. 2002 Sep;55(3):260–264. doi: 10.1007/s00239-002-2323-3 12187379

13. Romero H, Pereira E, Naya H, Musto H. Oxygen and Guanine—Cytosine Profiles in Marine Environments. Journal of Molecular Evolution. 2009 Aug;69(2):203–206. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2722718/ 19554248

14. Karanjawala ZE, Murphy N, Hinton DR, Hsieh CL, Lieber MR. Oxygen Metabolism Causes Chromosome Breaks and Is Associated with the Neuronal Apoptosis Observed in DNA Double-Strand Break Repair Mutants. Current Biology. 2002 Mar;12(5):397–402. Available from: http://www.sciencedirect.com/science/article/pii/S096098220200684X 11882291

15. Pitcher RS, Brissett NC, Doherty AJ. Nonhomologous end-joining in bacteria: a microbial perspective. Annual Review of Microbiology. 2007;61:259–282. doi: 10.1146/annurev.micro.61.080706.093354 17506672

16. Charbon G, Bjørn L, Mendoza-Chamizo B, Frimodt-Møller J, Løbner-Olesen A. Oxidative DNA damage is instrumental in hyperreplication stress-induced inviability of Escherichia coli. Nucleic acids research. 2014;42(21):13228–13241. doi: 10.1093/nar/gku1149 25389264

17. Dianov GL, Timehenko TV, Sinitsina OI, Kuzminov AV, Medvedev OA, Salganik RI. Repair of uracil residues closely spaced on the opposite strands of plasmid DNA results in double-strand break and deletion formation. Molecular and General Genetics MGG. 1991;225(3):448–452. doi: 10.1007/bf00261686 2017139

18. Kozmin SG, Sedletska Y, Reynaud-Angelin A, Gasparutto D, Sage E. The formation of double-strand breaks at multiply damaged sites is driven by the kinetics of excision/incision at base damage in eukaryotic cells. Nucleic acids research. 2009;37(6):1767–1777. doi: 10.1093/nar/gkp010 19174565

19. Hong Y, Li L, Luan G, Drlica K, Zhao X. Contribution of reactive oxygen species to thymineless death in Escherichia coli. Nature microbiology. 2017;2(12):1667. doi: 10.1038/s41564-017-0037-y 28970486

20. Henrikus SS, Henry C, McDonald JP, Hellmich Y, Wood EA, Woodgate R, et al. DNA double-strand breaks induced by reactive oxygen species promote DNA polymerase IV activity in Escherichia coli. bioRxiv. 2019; p. 533422.

21. Bonura T, Town CD, Smith KC, Kaplan HS. The influence of oxygen on the yield of DNA double-strand breaks in X-irradiated Escherichia coli K-12. Radiation research. 1975;63(3):567–577. doi: 10.2307/3574108 1099612

22. Tilby MJ, Loverock PS. Measurements of DNA double-strand break yields in E. coli after rapid irradiation and cell inactivation: the effects of inactivation technique and anoxic radiosensitizers. Radiation research. 1983;96(2):309–321. doi: 10.2307/3576214 6359240

23. Van der Schans G, Blok J. The influence of oxygen and sulphhydryl compounds on the production of breaks in bacteriophage DNA by gamma-rays. International Journal of Radiation Biology and Related Studies in Physics, Chemistry and Medicine. 1970;17(1):25–38. doi: 10.1080/09553007014550041

24. Mahaseth T, Kuzminov A. Prompt repair of hydrogen peroxide-induced DNA lesions prevents catastrophic chromosomal fragmentation. DNA repair. 2016;41:42–53. doi: 10.1016/j.dnarep.2016.03.012 27078578

25. Wang HC, Susko E, Roger AJ. On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: Data quality and confounding factors. Biochemical and Biophysical Research Communications. 2006 Apr;342(3):681–684. Available from: http://www.sciencedirect.com/science/article/pii/S0006291X06003214 16499870

26. Pitcher RS, Green AJ, Brzostek A, Korycka-Machala M, Dziadek J, Doherty AJ. NHEJ protects mycobacteria in stationary phase against the harmful effects of desiccation. DNA repair. 2007;6(9):1271–1276. doi: 10.1016/j.dnarep.2007.02.009 17360246

27. Vriezen JA, De Bruijn FJ, Nüsslein K. Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Applied and Environmental Microbiology. 2007;73(11):3451–3459. doi: 10.1128/AEM.02991-06 17400779

28. Dupuy P, Gourion B, Sauviac L, Bruand C. DNA double-strand break repair is involved in desiccation resistance of Sinorhizobium meliloti, but is not essential for its symbiotic interaction with Medicago truncatula. Microbiology. 2017;163(3):333–342. doi: 10.1099/mic.0.000400 27902438

29. Slieman TA, Nicholson WL. Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA. Appl Environ Microbiol. 2000;66(1):199–205. doi: 10.1128/aem.66.1.199-205.2000 10618224

30. Singer CE, Ames BN. Sunlight ultraviolet and bacterial DNA base ratios. Science. 1970;170(3960):822–826. doi: 10.1126/science.170.3960.822 5473414

31. Rocha EP, Cornet E, Michel B. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS genetics. 2005;1(2):e15. doi: 10.1371/journal.pgen.0010015 16132081

32. Gong C, Bongiorno P, Martins A, Stephanou NC, Zhu H, Shuman S, et al. Mechanism of nonhomologous end-joining in mycobacteria: a low-fidelity repair system driven by Ku, ligase D and ligase C. Nature structural & molecular biology. 2005;12(4):304. doi: 10.1038/nsmb915

33. Aravind L, Koonin EV. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Research. 2001 Aug;11(8):1365–1374. doi: 10.1101/gr.181001 11483577

34. Doherty Aidan J, Jackson Stephen P, Weller Geoffrey R. Identification of bacterial homologues of the Ku DNA repair proteins. FEBS Letters. 2001 Jul;500(3):186–188. Available from: https://febs.onlinelibrary.wiley.com/doi/full/10.1016/S0014-5793%2801%2902589-3.

35. Mcewan CE, Gatherer D, Mcewan NR. Nitrogen-fixing aerobic bacteria have higher genomic GC content than non-fixing species within the same genus. Hereditas. 1998;128(2):173–178. doi: 10.1111/j.1601-5223.1998.00173.x 9687237

36. Musto H, Naya H, Zavala A, Romero H, Alvarez-Valín F, Bernardi G. Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochemical and biophysical research communications. 2006;347(1):1–3. doi: 10.1016/j.bbrc.2006.06.054 16815305

37. Galtier N, Lobry J. Relationships between genomic G+ C content, RNA secondary structures, and optimal growth temperature in prokaryotes. Journal of molecular evolution. 1997;44(6):632–636. doi: 10.1007/pl00006186 9169555

38. Hurst LD, Merchant AR. High guanine—cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proceedings of the Royal Society of London Series B: Biological Sciences. 2001;268(1466):493–497. doi: 10.1098/rspb.2000.1397 11296861

39. Brbić M, Piškorec M, Vidulin V, Kriško A, Šmuc T, Supek F. The landscape of microbial phenotypic traits and associated genes. Nucleic Acids Research. 2016 Dec;44(21):10074–10090. Available from: https://academic.oup.com/nar/article/44/21/10074/2290929 27915291

40. Tatusova T, Ciufo S, Fedorov B, O’Neill K, Tolstoy I. RefSeq microbial genomes database: new representation and annotation strategy. Nucleic acids research. 2013;42(D1):D553–D559. doi: 10.1093/nar/gkt1274 24316578

41. McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991;351(6328):652. doi: 10.1038/351652a0 1904993

42. Kristensen DM, Wolf YI, Koonin EV. ATGC database and ATGC-COGs: an updated resource for micro-and macro-evolutionary studies of prokaryotic genomes and protein family annotation. Nucleic acids research. 2016; p. gkw934.

43. Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. The ISME journal. 2009;3(2):199. doi: 10.1038/ismej.2008.93 18830278

44. Rendueles O, de~Sousa JAM, Bernheim A, Touchon M, Rocha EP. Genetic exchanges are more frequent in bacteria encoding capsules. PLoS genetics. 2018;14(12):e1007862. doi: 10.1371/journal.pgen.1007862 30576310

45. Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics. 2006;172(4):2665–2681. doi: 10.1534/genetics.105.048975 16489234

46. Yahara K, Didelot X, Jolley KA, Kobayashi I, Maiden MC, Sheppard SK, et al. The landscape of realized homologous recombination in pathogenic bacteria. Molecular biology and evolution. 2015;33(2):456–471. doi: 10.1093/molbev/msv237 26516092

47. González-Torres P, Rodríguez-Mateos F, Antón J, Gabaldón T. Impact of homologous recombination on the evolution of prokaryotic core genomes. mBio. 2019;10(1):e02494–18. doi: 10.1128/mBio.02494-18 30670614

48. Liu H, Huang J, Sun X, Li J, Hu Y, Yu L, et al. Tetrad analysis in plants and fungi finds large differences in gene conversion rates but no GC bias. Nature ecology & evolution. 2018;2(1):164. doi: 10.1038/s41559-017-0372-7

49. Marsolier-Kergoat MC, Yeramian E. GC content and recombination: reassessing the causal effects for the Saccharomyces cerevisiae genome. Genetics. 2009;183(1):31–38. doi: 10.1534/genetics.109.105049 19546316

50. Brissett NC, Pitcher RS, Juarez R, Picher AJ, Green AJ, Dafforn TR, et al. Structure of a NHEJ polymerase-mediated DNA synaptic complex. Science. 2007;318(5849):456–459. doi: 10.1126/science.1145112 17947582

51. Brissett NC, Doherty AJ. Repairing DNA double-strand breaks by the prokaryotic non-homologous end-joining pathway. Biochemical Society transactions. 2009 Jun;37:539–545. doi: 10.1042/BST0370539 19442248

52. Della M, Palmbos PL, Tseng HM, Tonkin LM, Daley JM, Topper LM, et al. Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science. 2004;306(5696):683–685. doi: 10.1126/science.1099824 15499016

53. Aniukwu J, Glickman MS, Shuman S. The pathways and outcomes of mycobacterial NHEJ depend on the structure of the broken DNA ends. Genes & development. 2008;22(4):512–527. doi: 10.1101/gad.1631908

54. Sfeir A, Symington LS. Microhomology-mediated end joining: a back-up survival mechanism or dedicated pathway? Trends in biochemical sciences. 2015;40(11):701–714. doi: 10.1016/j.tibs.2015.08.006 26439531

55. Sandoval A, Labhart P. High G/C content of cohesive overhangs renders DNA end joining Ku-independent. DNA repair. 2004;3(1):13–21. doi: 10.1016/j.dnarep.2003.08.014 14697755

56. Daley JM, Wilson TE. Rejoining of DNA double-strand breaks as a function of overhang length. Molecular and cellular biology. 2005;25(3):896–906. doi: 10.1128/MCB.25.3.896-906.2005 15657419

57. Pleška M, Qian L, Okura R, Bergmiller T, Wakamoto Y, Kussell E, et al. Bacterial autoimmunity due to a restriction-modification system. Current Biology. 2016;26(3):404–409. doi: 10.1016/j.cub.2015.12.041 26804559

58. Limor-Waisberg K, Carmi A, Scherz A, Pilpel Y, Furman I. Specialization versus adaptation: two strategies employed by cyanophages to enhance their translation efficiencies. Nucleic acids research. 2011;39(14):6016–6028. doi: 10.1093/nar/gkr169 21470965

59. Roberts RJ, Vincze T, Posfai J, Macelis D. REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Research. 2010 Jan;38(suppl_1):D234–D236. Available from: https://academic.oup.com/nar/article/38/suppl_1/D234/3112229 19846593

60. Cox MM, Battista JR. Deinococcus radiodurans-the consummate survivor. Nature Reviews Microbiology. 2005;3(11):882. doi: 10.1038/nrmicro1264 16261171

61. Rohwer F, Azam F. Detection of DNA damage in prokaryotes by terminal deoxyribonucleotide transferase-mediated dUTP nick end labeling. Appl Environ Microbiol. 2000;66(3):1001–1006. doi: 10.1128/aem.66.3.1001-1006.2000 10698764

62. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Research. 2016 Jan;44(Database issue):D733–D745. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4702849/ 26553804

63. Eddy SR. Profile hidden Markov models. Bioinformatics (Oxford, England). 1998;14(9):755–763. doi: 10.1093/bioinformatics/14.9.755

64. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, et al. The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains. Systematic and Applied Microbiology. 2008 Sep;31(4):241–250. Available from: http://www.sciencedirect.com/science/article/pii/S072320200800060X 18692976

65. Weissman JL, Laljani RM, Fagan WF, Johnson PL. Visualization and prediction of CRISPR incidence in microbial trait-space to identify drivers of antiviral immune strategy. The ISME journal. 2019. doi: 10.1038/s41396-019-0411-2 31239539

66. Ho LsT, Ané C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Systematic Biology. 2014 May;63(3):397–408. doi: 10.1093/sysbio/syu005 24500037

67. Beaulieu JM, O’Meara BC, Donoghue MJ. Identifying hidden rate changes in the evolution of a binary morphological character: the evolution of plant habit in campanulid angiosperms. Systematic biology. 2013;62(5):725–737. doi: 10.1093/sysbio/syt034 23676760

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#