Genomic Location of the Major Ribosomal Protein Gene Locus Determines Global Growth and Infectivity

English version České info

Increasing evidence indicates that nucleoid spatiotemporal organization is crucial for bacterial physiology since these microorganism lack compartmentalized nucleus. However, it is still unclear how gene order within the chromosome can influence cell physiology. Here, by systematically relocating ribosomal protein genes to different genomic positions in Vibrio cholerae, we revealed drastic differences in growth rate and infectivity of this isogenic strain set. We show that genomic positioning of ribosomal protein genes is crucial for physiology by providing replication-dependent higher dosage. Therefore it might play a key role in genome evolution of bacterial species. This work will contribute to discover genomic rules governing cell physiology which will be essential in the context of the creation of new artificial life forms.

Vyšlo v časopise: Genomic Location of the Major Ribosomal Protein Gene Locus Determines Global Growth and Infectivity. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005156
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005156

Souhrn

Zdroje

1. Reyes-Lamothe R, Nicolas E, Sherratt DJ. Chromosome replication and segregation in bacteria. Annual review of genetics. 2012;46:121–43. doi: 10.1146/annurev-genet-110711-155421 22934648.

2. Dorman CJ. Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nature reviews Microbiology. 2013;11(5):349–55. doi: 10.1038/nrmicro3007 23549066.

3. Toro E, Shapiro L. Bacterial chromosome organization and segregation. Cold Spring Harbor perspectives in biology. 2010;2(2):a000349. Epub 2010/02/26. doi: 10.1101/cshperspect.a000349 20182613; PubMed Central PMCID: PMCPMC2828278.

4. Sobetzko P, Travers A, Muskhelishvili G. Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(2):E42–50. doi: 10.1073/pnas.1108229109 22184251; PubMed Central PMCID: PMC3258614.

5. Junier I, Herisson J, Kepes F. Genomic organization of evolutionarily correlated genes in bacteria: limits and strategies. Journal of molecular biology. 2012;419(5):369–86. doi: 10.1016/j.jmb.2012.03.009 22446685.

6. Geertz M, Travers A, Mehandziska S, Sobetzko P, Chandra-Janga S, Shimamoto N, et al. Structural coupling between RNA polymerase composition and DNA supercoiling in coordinating transcription: a global role for the omega subunit? mBio. 2011;2(4). doi: 10.1128/mBio.00034-11 21810966; PubMed Central PMCID: PMC3147163.

7. Dryselius R, Izutsu K, Honda T, Iida T. Differential replication dynamics for large and small Vibrio chromosomes affect gene dosage, expression and location. BMC genomics. 2008;9:559. doi: 10.1186/1471-2164-9-559 19032792; PubMed Central PMCID: PMC2612033.

8. Block DH, Hussein R, Liang LW, Lim HN. Regulatory consequences of gene translocation in bacteria. Nucleic acids research. 2012;40(18):8979–92. Epub 2012/07/27. doi: 10.1093/nar/gks694 22833608; PubMed Central PMCID: PMCPMC3467084.

9. Montero Llopis P, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, et al. Spatial organization of the flow of genetic information in bacteria. Nature. 2010;466(7302):77–81. doi: 10.1038/nature09152 20562858; PubMed Central PMCID: PMC2896451.

10. Kuhlman TE, Cox EC. Gene location and DNA density determine transcription factor distributions in Escherichia coli. Molecular systems biology. 2012;8:610. doi: 10.1038/msb.2012.42 22968444; PubMed Central PMCID: PMC3472691.

11. Slager J, Kjos M, Attaiech L, Veening JW. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell. 2014;157(2):395–406. doi: 10.1016/j.cell.2014.01.068 24725406.

12. Rocha EP. The organization of the bacterial genome. Annual review of genetics. 2008;42:211–33. doi: 10.1146/annurev.genet.42.110807.091653 18605898.

13. Kepes F, Jester BC, Lepage T, Rafiei N, Rosu B, Junier I. The layout of a bacterial genome. FEBS letters. 2012;586(15):2043–8. doi: 10.1016/j.febslet.2012.03.051 22483986.

14. Merrikh H, Zhang Y, Grossman AD, Wang JD. Replication-transcription conflicts in bacteria. Nature reviews Microbiology. 2012;10(7):449–58. Epub 2012/06/07. doi: 10.1038/nrmicro2800 22669220; PubMed Central PMCID: PMCPMC3467967.

15. Wang JD, Levin PA. Metabolism, cell growth and the bacterial cell cycle. Nature reviews Microbiology. 2009;7(11):822–7. doi: 10.1038/nrmicro2202 19806155; PubMed Central PMCID: PMC2887316.

16. Couturier E, Rocha EP. Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Molecular microbiology. 2006;59(5):1506–18. Epub 2006/02/14. doi: 10.1111/j.1365-2958.2006.05046.x 16468991.

17. Bremer H, Dennis PP. Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella: cellular and molecular biology. 1996;2:1553–69.

18. Kaczanowska M, Ryden-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiology and molecular biology reviews: MMBR. 2007;71(3):477–94. doi: 10.1128/MMBR.00013-07 17804668; PubMed Central PMCID: PMC2168646.

19. Allen T, Shen P, Samsel L, Liu R, Lindahl L, Zengel JM. Phylogenetic analysis of L4-mediated autogenous control of the S10 ribosomal protein operon. Journal of bacteriology. 1999;181(19):6124–32. Epub 1999/09/28. 10498727; PubMed Central PMCID: PMCPMC103642.

20. Khayrullina GA, Raabe CA, Hoe CH, Becker K, Reinhardt R, Tang TH, et al. Transcription analysis and small non-protein coding RNAs associated with bacterial ribosomal protein operons. Current medicinal chemistry. 2012;19(30):5187–98. Epub 2012/06/12. 22680642.

21. Schlax PJ, Xavier KA, Gluick TC, Draper DE. Translational repression of the Escherichia coli alpha operon mRNA: importance of an mRNA conformational switch and a ternary entrapment complex. The Journal of biological chemistry. 2001;276(42):38494–501. doi: 10.1074/jbc.M106934200 11504736.

22. Fu Y, Deiorio-Haggar K, Anthony J, Meyer MM. Most RNAs regulating ribosomal protein biosynthesis in Escherichia coli are narrowly distributed to Gammaproteobacteria. Nucleic acids research. 2013;41(6):3491–503. Epub 2013/02/12. doi: 10.1093/nar/gkt055 23396277; PubMed Central PMCID: PMCPMC3616713.

23. Lemke JJ, Sanchez-Vazquez P, Burgos HL, Hedberg G, Ross W, Gourse RL. Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(14):5712–7. doi: 10.1073/pnas.1019383108 21402902; PubMed Central PMCID: PMC3078377.

24. Allen TD, Watkins T, Lindahl L, Zengel JM. Regulation of ribosomal protein synthesis in Vibrio cholerae. Journal of bacteriology. 2004;186(17):5933–7. Epub 2004/08/20. doi: 10.1128/jb.186.17.5933-5937.2004 15317799; PubMed Central PMCID: PMCPMC516831.

25. Bryant JA, Sellars LE, Busby SJ, Lee DJ. Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic acids research. 2015;42(18):11383–92. doi: 10.1093/nar/gku828 25209233.

26. Spitzer J. From water and ions to crowded biomacromolecules: in vivo structuring of a prokaryotic cell. Microbiology and molecular biology reviews: MMBR. 2011;75(3):491–506, second page of table of contents. doi: 10.1128/MMBR.00010-11 21885682; PubMed Central PMCID: PMC3165543.

27. Campos M, Jacobs-Wagner C. Cellular organization of the transfer of genetic information. Current opinion in microbiology. 2013;16(2):171–6. doi: 10.1016/j.mib.2013.01.007 23395479; PubMed Central PMCID: PMC3646911.

28. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature. 2000;406(6795):477–83. doi: 10.1038/35020000 10952301.

29. Rasmussen T, Jensen RB, Skovgaard O. The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. The EMBO journal. 2007;26(13):3124–31. Epub 2007/06/09. doi: 10.1038/sj.emboj.7601747 17557077; PubMed Central PMCID: PMCPMC1914095.

30. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell host & microbe. 2011;10(2):165–74. doi: 10.1016/j.chom.2011.07.007 21843873; PubMed Central PMCID: PMC3166260.

31. DeVito JA. Recombineering with tolC as a selectable/counter-selectable marker: remodeling the rRNA operons of Escherichia coli. Nucleic acids research. 2008;36(1):e4. doi: 10.1093/nar/gkm1084 18084036; PubMed Central PMCID: PMC2248734.

32. Merrikh H, Machon C, Grainger WH, Grossman AD, Soultanas P. Co-directional replication-transcription conflicts lead to replication restart. Nature. 2011;470(7335):554–7. doi: 10.1038/nature09758 21350489; PubMed Central PMCID: PMC3059490.

33. Stevenson BS, Schmidt TM. Life history implications of rRNA gene copy number in Escherichia coli. Applied and environmental microbiology. 2004;70(11):6670–7. doi: 10.1128/AEM.70.11.6670-6677.2004 15528533; PubMed Central PMCID: PMC525164.

34. Condon C, Liveris D, Squires C, Schwartz I, Squires CL. rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. Journal of bacteriology. 1995;177(14):4152–6. 7608093; PubMed Central PMCID: PMC177152.

35. De Septenville AL, Duigou S, Boubakri H, Michel B. Replication fork reversal after replication-transcription collision. PLoS genetics. 2012;8(4):e1002622. doi: 10.1371/journal.pgen.1002622 22496668; PubMed Central PMCID: PMC3320595.

36. Gyorfy Z, Draskovits G, Vernyik V, Blattner FF, Gaal T, Posfai G. Engineered ribosomal RNA operon copy-number variants of E. coli reveal the evolutionary trade-offs shaping rRNA operon number. Nucleic acids research. 2015;43(3):1783–94. doi: 10.1093/nar/gkv040 25618851.

37. Coenye T, Vandamme P. Organisation of the S10, spc and alpha ribosomal protein gene clusters in prokaryotic genomes. FEMS microbiology letters. 2005;242(1):117–26. doi: 10.1016/j.femsle.2004.10.050 15621428.

38. Stoebe B, Kowallik KV. Gene-cluster analysis in chloroplast genomics. Trends in genetics: TIG. 1999;15(9):344–7. 10461201.

39. Chao MC, Pritchard JR, Zhang YJ, Rubin EJ, Livny J, Davis BM, et al. High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model-based analyses of transposon-insertion sequencing data. Nucleic acids research. 2013;41(19):9033–48. doi: 10.1093/nar/gkt654 23901011; PubMed Central PMCID: PMC3799429.

40. Thiel A, Valens M, Vallet-Gely I, Espeli O, Boccard F. Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain. PLoS genetics. 2012;8(4):e1002672. doi: 10.1371/journal.pgen.1002672 22532809; PubMed Central PMCID: PMC3330122.

41. Val ME, Skovgaard O, Ducos-Galand M, Bland MJ, Mazel D. Genome engineering in Vibrio cholerae: a feasible approach to address biological issues. PLoS genetics. 2012;8(1):e1002472. Epub 2012/01/19. doi: 10.1371/journal.pgen.1002472 22253612; PubMed Central PMCID: PMCPMC3257285.

42. De Souza Silva O, Blokesch M. Genetic manipulation of Vibrio cholerae by combining natural transformation with FLP recombination. Plasmid. 2010;64(3):186–95. Epub 2010/08/17. doi: 10.1016/j.plasmid.2010.08.001 20709100.

43. Nagaraja R, Weisberg RA. Specificity determinants in the attachment sites of bacteriophages HK022 and lambda. Journal of bacteriology. 1990;172(11):6540–50. 2146253; PubMed Central PMCID: PMC526843.

44. Stokke C, Waldminghaus T, Skarstad K. Replication patterns and organization of replication forks in Vibrio cholerae. Microbiology. 2011;157(Pt 3):695–708. doi: 10.1099/mic.0.045112-0 21163839.

45. Purdy AE, Watnick PI. Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(49):19737–42. Epub 2011/11/23. doi: 10.1073/pnas.1111530108 22106284; PubMed Central PMCID: PMCPMC3241763.

46. Blow NS, Salomon RN, Garrity K, Reveillaud I, Kopin A, Jackson FR, et al. Vibrio cholerae infection of Drosophila melanogaster mimics the human disease cholera. PLoS pathogens. 2005;1(1):e8. Epub 2005/10/05. doi: 10.1371/journal.ppat.0010008 16201020; PubMed Central PMCID: PMCPMC1238743.

47. Broza M, Gancz H, Kashi Y. The association between non-biting midges and Vibrio cholerae. Environmental microbiology. 2008;10(12):3193–200. Epub 2008/11/26. doi: 10.1111/j.1462-2920.2008.01714.x 19025555.

48. Pruzzo C, Vezzulli L, Colwell RR. Global impact of Vibrio cholerae interactions with chitin. Environmental microbiology. 2008;10(6):1400–10. Epub 2008/03/04. doi: 10.1111/j.1462-2920.2007.01559.x 18312392.

49. Fotedar R. Vector potential of houseflies (Musca domestica) in the transmission of Vibrio cholerae in India. Acta tropica. 2001;78(1):31–4. 11164748.

50. Evertts AG, Coller HA. Back to the origin: reconsidering replication, transcription, epigenetics, and cell cycle control. Genes & cancer. 2012;3(11–12):678–96. Epub 2013/05/02. doi: 10.1177/1947601912474891 23634256; PubMed Central PMCID: PMCPMC3636748.

51. Sclafani RA, Holzen TM. Cell cycle regulation of DNA replication. Annual review of genetics. 2007;41:237–80. doi: 10.1146/annurev.genet.41.110306.130308 17630848; PubMed Central PMCID: PMC2292467.

52. Mott ML, Berger JM. DNA replication initiation: mechanisms and regulation in bacteria. Nature reviews Microbiology. 2007;5(5):343–54. doi: 10.1038/nrmicro1640 17435790.

53. Robinson NP, Bell SD. Origins of DNA replication in the three domains of life. The FEBS journal. 2005;272(15):3757–66. doi: 10.1111/j.1742-4658.2005.04768.x 16045748.

54. Sousa C, de Lorenzo V, Cebolla A. Modulation of gene expression through chromosomal positioning in Escherichia coli. Microbiology. 1997;143 (Pt 6):2071–8. 9202482.

55. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, et al. Phenotypic landscape of a bacterial cell. Cell. 2011;144(1):143–56. doi: 10.1016/j.cell.2010.11.052 21185072; PubMed Central PMCID: PMC3060659.

56. Vieira-Silva S, Rocha EP. The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS genetics. 2010;6(1):e1000808. doi: 10.1371/journal.pgen.1000808 20090831; PubMed Central PMCID: PMC2797632.

57. Nomura M, Gourse R, Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annual review of biochemistry. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451 6206783.

58. Paul BJ, Ross W, Gaal T, Gourse RL. rRNA transcription in Escherichia coli. Annual review of genetics. 2004;38:749–70. doi: 10.1146/annurev.genet.38.072902.091347 15568992.

59. Murray H, Koh A. Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in Bacillus subtilis. PLoS genetics. 2014;10(10):e1004731. doi: 10.1371/journal.pgen.1004731 25340815; PubMed Central PMCID: PMC4207641.

60. Dez C, Tollervey D. Ribosome synthesis meets the cell cycle. Current opinion in microbiology. 2004;7(6):631–7. doi: 10.1016/j.mib.2004.10.007 15556036.

61. Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer cell. 2009;16(5):369–77. doi: 10.1016/j.ccr.2009.09.024 19878869.

62. Berthon J, Fujikane R, Forterre P. When DNA replication and protein synthesis come together. Trends in biochemical sciences. 2009;34(9):429–34. doi: 10.1016/j.tibs.2009.05.004 19729310.

63. Val ME, Soler-Bistue A, Bland MJ, Mazel D. Management of multipartite genomes: the Vibrio cholerae model. Current opinion in microbiology. 2014;22C:120–6. doi: 10.1016/j.mib.2014.10.003 25460805.

64. Egan ES, Fogel MA, Waldor MK. Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Molecular microbiology. 2005;56(5):1129–38. doi: 10.1111/j.1365-2958.2005.04622.x 15882408.

65. Cooper VS, Vohr SH, Wrocklage SC, Hatcher PJ. Why genes evolve faster on secondary chromosomes in bacteria. PLoS computational biology. 2010;6(4):e1000732. doi: 10.1371/journal.pcbi.1000732 20369015; PubMed Central PMCID: PMC2848543.

66. Karr JR, Sanghvi JC, Macklin DN, Gutschow MV, Jacobs JM, Bolival B Jr., et al. A whole-cell computational model predicts phenotype from genotype. Cell. 2012;150(2):389–401. doi: 10.1016/j.cell.2012.05.044 22817898; PubMed Central PMCID: PMC3413483.

67. Scott M, Hwa T. Bacterial growth laws and their applications. Current opinion in biotechnology. 2011;22(4):559–65. doi: 10.1016/j.copbio.2011.04.014 21592775; PubMed Central PMCID: PMC3152618.

68. Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G. Interactive microbial genome visualization with GView. Bioinformatics. 2010;26(24):3125–6. doi: 10.1093/bioinformatics/btq588 20956244; PubMed Central PMCID: PMC2995121.