1932

Abstract

Transformation is a widespread mechanism of horizontal gene transfer in bacteria. DNA uptake to the periplasmic compartment requires a DNA-uptake pilus and the DNA-binding protein ComEA. In the gram-negative bacteria, DNA is first pulled toward the outer membrane by retraction of the pilus and then taken up by binding to periplasmic ComEA, acting as a Brownian ratchet to prevent backward diffusion. A similar mechanism probably operates in the gram-positive bacteria as well, but these systems have been less well characterized. Transport, defined as movement of a single strand of transforming DNA to the cytosol, requires the channel protein ComEC. Although less is understood about this process, it may be driven by proton symport. In this review we also describe various phenomena that are coordinated with the expression of competence for transformation, such as fratricide, the kin-discriminatory killing of neighboring cells, and competence-mediated growth arrest.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112618-043641
2019-12-03
2024-06-14
Loading full text...

Full text loading...

/deliver/fulltext/genet/53/1/annurev-genet-112618-043641.html?itemId=/content/journals/10.1146/annurev-genet-112618-043641&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adams DW, Stutzmann S, Stoudmann C, Blokesch M 2019. DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction. Nat. Microbiol. 4:1545–-57
    [Google Scholar]
  2. 2. 
    Albano M, Hahn J, Dubnau D 1987. Expression of competence genes in Bacillus subtilis. J. Bacteriol 169:3110–17
    [Google Scholar]
  3. 3. 
    Ambur OH, Frye SA, Tonjum T 2007. New functional identity for the DNA uptake sequence in transformation and its presence in transcriptional terminators. J. Bacteriol. 189:2077–85
    [Google Scholar]
  4. 4. 
    Aravind L. 1999. An evolutionary classification of the metallo-β-lactamase fold proteins. In Silico Biol 1:69–91
    [Google Scholar]
  5. 5. 
    Avery OT, Macleod CM, McCarty M 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. I. Induction of transformation by a deoxyribonucleic acid fraction isolated from Pneumococcus type III. J. Exp. Med. 79:137–58
    [Google Scholar]
  6. 6. 
    Baker JA, Simkovic F, Taylor HM, Rigden DJ 2016. Potential DNA binding and nuclease functions of ComEC domains characterized in silico. Proteins 84:1431–42
    [Google Scholar]
  7. 7. 
    Beaber JW, Hochhut B, Waldor MK 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:72–74
    [Google Scholar]
  8. 8. 
    Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, Henriques-Normark B 2006. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr. Biol. 16:401–7
    [Google Scholar]
  9. 9. 
    Bergé MJ, Kamgoué A, Martin B, Polard P, Campo N, Claverys J-P 2013. Midcell recruitment of the DNA uptake and virulence nuclease, EndA, for pneumococcal transformation. PLOS Pathog 9:e1003596
    [Google Scholar]
  10. 10. 
    Bergé MJ, Mercy C, Mortier-Barrière I, VanNieuwenhze MS, Brun YV et al. 2017. A programmed cell division delay preserves genome integrity during natural genetic transformation in Streptococcus pneumoniae. . Nat. Commun 8:1621
    [Google Scholar]
  11. 11. 
    Berka RM, Hahn J, Albano M, Draskovic I, Persuh M et al. 2002. Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK. Mol. Microbiol. 43:1331–45
    [Google Scholar]
  12. 12. 
    Berry JL, Xu Y, Ward PN, Lea SM, Matthews SJ, Pelicic V 2016. A comparative structure/function analysis of two type IV pilin DNA receptors defines a novel mode of DNA binding. Structure 24:926–34
    [Google Scholar]
  13. 13. 
    Borgeaud S, Metzger LC, Scrignari T, Blokesch M 2015. The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 347:63–67
    [Google Scholar]
  14. 14. 
    Bremer W, Kooistra J, Hellingwerf KJ, Konings WN 1984. Role of the electrochemical proton gradient in genetic transformation of Haemophilus influenzae. J. Bacteriol 157:868–73
    [Google Scholar]
  15. 15. 
    Briley K Jr., Dorsey-Oresto A, Prepiak P, Dias MJ, Mann JM, Dubnau D. 2011. The secretion ATPase ComGA is required for the binding and transport of transforming DNA. Mol. Microbiol. 81:818–30
    [Google Scholar]
  16. 16. 
    Burton B, Dubnau D. 2010. Membrane-associated DNA transport machines. Cold Spring Harb. Perspect. Biol. 2:a000406
    [Google Scholar]
  17. 16a. 
    Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R et al. 2013. Specific DNA recognition mediated by a type IV pillin. PNAS 110:3065–-70
    [Google Scholar]
  18. 17. 
    Chang YW, Rettberg LA, Treuner-Lange A, Iwasa J, Søgaard-Andersen L, Jensen GJ 2016. Architecture of the type IVa pilus machine. Science 351:aad2001
    [Google Scholar]
  19. 18. 
    Charpentier X, Kay E, Schneider D, Shuman HA 2011. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J. Bacteriol 193:1114–21
    [Google Scholar]
  20. 19. 
    Chen I, Christie PJ, Dubnau D 2005. The ins and outs of DNA transfer in bacteria. Science 310:1456–60
    [Google Scholar]
  21. 20. 
    Chen I, Gotschlich EC. 2001. ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J. Bacteriol. 183:3160–68
    [Google Scholar]
  22. 21. 
    Chen I, Provvedi R, Dubnau D 2006. A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. J. Biol. Chem 281:21720–27
    [Google Scholar]
  23. 22. 
    Chung YS, Breidt F, Dubnau D 1998. Cell surface localization and processing of the ComG proteins, required for DNA binding during transformation of Bacillus subtilis. Mol. Microbiol 29:905–13
    [Google Scholar]
  24. 23. 
    Claverys J-P, Martin B, Polard P 2009. The genetic transformation machinery: composition, localization, and mechanism. FEMS Microbiol. Rev. 33:643–56
    [Google Scholar]
  25. 24. 
    Claverys J-P, Prudhomme M, Martin B 2006. Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu. Rev. Microbiol. 60:451–75
    [Google Scholar]
  26. 25. 
    Claverys J-P, Prudhomme M, Mortier-Barrière I, Martin B 2000. Adaptation to the environment: Streptococcus pneumoniae, a paradigm for recombination-mediated genetic plasticity?. Mol. Microbiol. 35:251–59
    [Google Scholar]
  27. 26. 
    Cooper RM, Tsimring L, Hasty J 2017. Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance. eLife 6:e25950
    [Google Scholar]
  28. 27. 
    Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M et al. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 23:651–62
    [Google Scholar]
  29. 28. 
    Diallo A, Foster HR, Gromek KA, Perry TN, Dujeancourt A et al. 2017. Bacterial transformation: ComFA is a DNA-dependent ATPase that forms complexes with ComFC and DprA. Mol. Microbiol. 105:741–54
    [Google Scholar]
  30. 29. 
    Doherty AJ, Serpell LC, Ponting CP 1996. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res 24:2488–97
    [Google Scholar]
  31. 30. 
    Domenech A, Slager J, Veening JW 2018. Antibiotic-induced cell chaining triggers pneumococcal competence by reshaping quorum sensing to autocrine-like signaling. Cell Rep 25:2390–400.e3
    [Google Scholar]
  32. 31. 
    Domingues S, Nielsen KM. 2017. Membrane vesicles and horizontal gene transfer in prokaryotes. Curr. Opin. Microbiol. 38:16–21
    [Google Scholar]
  33. 32. 
    Draskovic I, Dubnau D. 2005. Biogenesis of a putative channel protein, ComEC, required for DNA uptake: membrane topology, oligomerization and formation of disulphide bonds. Mol. Microbiol. 55:881–96
    [Google Scholar]
  34. 33. 
    Dubnau D, Cirigliano C. 1972. Fate of transforming DNA following uptake by competent Bacillus subtilis. III. Formation and properties of products isolated from transformed cells which are derived entirely from donor DNA. J. Mol. Biol. 64:9–29
    [Google Scholar]
  35. 34. 
    Eldholm V, Johnsborg O, Straume D, Ohnstad HS, Berg KH et al. 2010. Pneumococcal CbpD is a murein hydrolase that requires a dual cell envelope binding specificity to kill target cells during fratricide. Mol. Microbiol. 76:905–17
    [Google Scholar]
  36. 35. 
    Ellison CK, Dalia TN, Vidal Ceballos A, Wang JC-Y, Biais N et al. 2018. Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat. Microbiol 3:773–80
    [Google Scholar]
  37. 36. 
    Ellison CK, Kan J, Chlebek JL, Hummels KR, Panis G et al. 2019. A bifunctional ATPase drives tad pilus extension and retraction. bioRxiv 616128. https://doi.org/10.1101/616128
    [Crossref]
  38. 37. 
    Fisher RA, Gollan B, Helaine S 2017. Persistent bacterial infections and persister cells. Nat. Rev. Microbiol. 15:453–64
    [Google Scholar]
  39. 38. 
    Fleurie A, Manuse S, Zhao C, Campo N, Cluzel C et al. 2014. Interplay of the serine/threonine-kinase StkP and the paralogs DivIVA and GpsB in pneumococcal cell elongation and division. PLOS Genet 10:e1004275
    [Google Scholar]
  40. 39. 
    Friedrich A, Hartsch T, Averhoff B 2001. Natural transformation in mesophilic and thermophilic bacteria: identification and characterization of novel, closely related competence genes in Acinetobacter sp. strain BD413 and Thermus thermophilus HB27. Appl. Environ. Microbiol. 67:3140–48
    [Google Scholar]
  41. 40. 
    Gangel H, Hepp C, Müller S, Oldewurtel ER, Aas FE et al. 2014. Concerted spatio-temporal dynamics of imported DNA and ComE DNA uptake protein during gonococcal transformation. PLOS Pathog 10:e1004043
    [Google Scholar]
  42. 41. 
    García-Aljaro C, Ballesté E, Muniesa M 2017. Beyond the canonical strategies of horizontal gene transfer in prokaryotes. Curr. Opin. Microbiol. 38:95–105
    [Google Scholar]
  43. 42. 
    Giltner CL, Nguyen Y, Burrows LL 2012. Type IV pilin proteins: versatile molecular modules. Microbiol. Mol. Biol. Rev. 76:740–72
    [Google Scholar]
  44. 43. 
    Gold VA, Salzer R, Averhoff B, Kühlbrandt W 2015. Structure of a type IV pilus machinery in the open and closed state. eLife 4:e07380
    [Google Scholar]
  45. 44. 
    Grangeasse C. 2016. Rewiring the pneumococcal cell cycle with serine/threonine- and tyrosine-kinases. Trends Microbiol 24:713–24
    [Google Scholar]
  46. 45. 
    Griffith F. 1928. The significance of Pneumococcal types. J. Hyg. 27:113–59
    [Google Scholar]
  47. 46. 
    Guerin É, Cambray G, Sanchez-Alberola N, Campoy S, Erill I et al. 2009. The SOS response controls integron recombination. Science 324:1034
    [Google Scholar]
  48. 47. 
    Guiral S, Mitchell TJ, Martin B, Claverys J-P 2005. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. PNAS 102:8710–15
    [Google Scholar]
  49. 48. 
    Hahn J, Albano M, Dubnau D 1987. Isolation and characterization of Tn917lac-generated competence mutants of Bacillus subtilis. J. Bacteriol. 169:3104–9
    [Google Scholar]
  50. 49. 
    Hahn J, Kramer N, Briley K Jr., Dubnau D. 2009. McsA and B mediate the delocalization of competence proteins from the cell poles of Bacillus subtilis. Mol. Microbiol 72:202–15
    [Google Scholar]
  51. 50. 
    Hahn J, Maier B, Haijema BJ, Sheetz M, Dubnau D 2005. Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122:59–71
    [Google Scholar]
  52. 51. 
    Hahn J, Tanner AW, Carabetta VJ, Cristea IM, Dubnau D 2015. ComGA-RelA interaction and persistence in the Bacillus subtilis K-state. Mol. Microbiol. 97:454–71
    [Google Scholar]
  53. 52. 
    Haijema BJ, Hahn J, Haynes J, Dubnau D 2001. A ComGA-dependent checkpoint limits growth during the escape from competence. Mol. Microbiol. 40:52–64
    [Google Scholar]
  54. 53. 
    Håvarstein LS, Martin B, Johnsborg O, Granadel C, Claverys J-P 2006. New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol. Microbiol. 59:1297–307
    [Google Scholar]
  55. 54. 
    Hepp C, Maier B. 2016. Kinetics of DNA uptake during transformation provide evidence for a translocation ratchet mechanism. PNAS 113:12467–72
    [Google Scholar]
  56. 55. 
    Ho BT, Dong TG, Mekalanos JJ 2014. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15:9–21
    [Google Scholar]
  57. 56. 
    Hobbs M, Mattick JS. 1993. Common components in the assembly of type-4 fimbriae, DNA transfer systems, filamentous phage and protein secretion apparatus; a general system for the formation of surface-associated protein complexes. Mol. Microbiol. 10:233–43
    [Google Scholar]
  58. 57. 
    Hofreuter D, Odenbreit S, Haas R 2001. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41:379–91
    [Google Scholar]
  59. 58. 
    Humbert O, Prudhomme M, Hakenbeck R, Dowson CG, Claverys J-P 1995. Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. PNAS 92:9052–56
    [Google Scholar]
  60. 59. 
    Inamine GS, Dubnau D. 1995. ComEA, a Bacillus subtilis integral membrane protein required for genetic transformation, is needed for both DNA binding and transport. J. Bacteriol. 177:3045–51
    [Google Scholar]
  61. 60. 
    Jaskólska M, Stutzmann S, Stoudmann C, Blokesch M 2018. QstR-dependent regulation of natural competence and type VI secretion in Vibrio cholerae. Nucleic Acids Res 46:10619–34
    [Google Scholar]
  62. 61. 
    Johnsen PJ, Dubnau D, Levin BR 2009. Episodic selection and the maintenance of competence and natural transformation in Bacillus subtilis. Genetics 181:1521–33
    [Google Scholar]
  63. 62. 
    Johnston C, Martin B, Fichant G, Polard P, Claverys J-P 2014. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat. Rev. Microbiol. 12:181–96
    [Google Scholar]
  64. 63. 
    Johnston C, Martin B, Granadel C, Polard P, Claverys J-P 2013. Programmed protection of foreign DNA from restriction allows pathogenicity island exchange during pneumococcal transformation. PLOS Pathog 9:e1003178
    [Google Scholar]
  65. 64. 
    Kaufenstein M, van der Laan M, Graumann PL 2011. The three-layered DNA uptake machinery at the cell pole in competent Bacillus subtilis cells is a stable complex. J. Bacteriol. 193:1633–42
    [Google Scholar]
  66. 65. 
    Kidane D, Graumann PL. 2005. Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 122:73–84
    [Google Scholar]
  67. 66. 
    Kjos M, Miller E, Slager J, Lake FB, Gericke O et al. 2016. Expression of Streptococcus pneumoniae bacteriocins is induced by antibiotics via regulatory interplay with the competence system. PLOS Pathog 12:e1005422
    [Google Scholar]
  68. 67. 
    Kramer N, Hahn J, Dubnau D 2007. Multiple interactions among the competence proteins of Bacillus subtilis. Mol. Microbiol 65:454–64
    [Google Scholar]
  69. 68. 
    Lacks SA. 1988. Mechanisms of genetic recombination in gram-positive bacteria. Genetic Recombination ed. R Kucherlapti, GR Smith 43–86 Washington, DC: American Society for Microbiology
    [Google Scholar]
  70. 69. 
    Laurenceau R, Péhau-Arnaudet G, Baconnais S, Gault J, Malosse C et al. 2013. A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLOS Pathog 9:e1003473
    [Google Scholar]
  71. 70. 
    Lo Scrudato M, Blokesch M 2012. The regulatory network of natural competence and transformation of Vibrio cholerae. PLOS Genet 8:e1002778
    [Google Scholar]
  72. 71. 
    Londoño-Vallejo JA, Dubnau D. 1994. Membrane association and role in DNA uptake of the Bacillus subtilis PriA analogue ComF1. Mol. Microbiol. 13:197–205
    [Google Scholar]
  73. 72. 
    Londoño-Vallejo JA, Dubnau D. 1994. Mutation of the putative nucleotide binding site of the Bacillus subtilis membrane protein ComFA abolishes the uptake of DNA during transformation. J. Bacteriol. 176:4642–45
    [Google Scholar]
  74. 73. 
    Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S et al. 2014. Structure of a type IV secretion system. Nature 508:550–53
    [Google Scholar]
  75. 74. 
    Maier B, Chen I, Dubnau D, Sheetz MP 2004. DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nat. Struct. Mol. Biol. 11:643–49
    [Google Scholar]
  76. 75. 
    Matias VRF, Beveridge TJ. 2005. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56:240–51
    [Google Scholar]
  77. 76. 
    Matias VRF, Beveridge TJ. 2006. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol 188:1011–21
    [Google Scholar]
  78. 76a. 
    Matthey N, Stutzmann S, Stoudmann C, Guex N, Iseli C, Blokesch M. 2019. Neighbor predation linked to natural competence fosters the transfer of large genomic regions in Vibrio cholerae. . eLife 8:e48212
    [Google Scholar]
  79. 77. 
    Meima R, Eschevins C, Fillinger S, Bolhuis A, Hamoen LW et al. 2002. The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development. J. Biol. Chem. 277:6994–7001
    [Google Scholar]
  80. 78. 
    Mejean V, Claverys J-P. 1993. DNA processing during entry in transformation of Streptococcus pneumoniae. J. Biol. Chem 268:5594–99
    [Google Scholar]
  81. 79. 
    Mell JC, Hall IM, Redfield RJ 2012. Defining the DNA uptake specificity of naturally competent Haemophilus influenzae cells. Nucleic Acids Res 40:8536–49
    [Google Scholar]
  82. 80. 
    Melville S, Craig L. 2013. Type IV pili in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 77:323–41
    [Google Scholar]
  83. 81. 
    Metzger LC, Blokesch M. 2016. Regulation of competence-mediated horizontal gene transfer in the natural habitat of Vibrio cholerae. Curr. Opin. Microbiol 30:1–7
    [Google Scholar]
  84. 82. 
    Metzger LC, Matthey N, Stoudmann C, Collas EJ, Blokesch M 2019. Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species. Environ. Microbiol. 21:2231–47
    [Google Scholar]
  85. 83. 
    Mirouze N, Dubnau D. 2013. Chance and necessity in Bacillus subtilis development. Microbiol. Spectr. 1: https://doi.org/10.1128/microbiolspectrum.TBS-0004-2012
    [Crossref] [Google Scholar]
  86. 84. 
    Mirouze N, Ferret C, Cornilleau C, Carballido-López R 2018. Antibiotic sensitivity reveals that wall teichoic acids mediate DNA binding during competence in Bacillus subtilis. Nat. Commun 9:5072
    [Google Scholar]
  87. 85. 
    Mirouze N, Ferret C, Yao Z, Chastanet A, Carballido-López R 2015. MreB-dependent inhibition of cell elongation during the escape from competence in Bacillus subtilis. PLOS Genet 11:e1005299
    [Google Scholar]
  88. 86. 
    Moreno-Gámez S, Sorg RA, Domenech A, Kjos M, Weissing FJ et al. 2017. Quorum sensing integrates environmental cues, cell density and cell history to control bacterial competence. Nat. Commun. 8:854
    [Google Scholar]
  89. 87. 
    Nester EW, Stocker BAD. 1963. Biosynthetic latency in early stages of deoxyribonucleic acid transformation in Bacillus subtilis. J. Bacteriol 86:785–96
    [Google Scholar]
  90. 88. 
    Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D 2007. Release and persistence of extracellular DNA in the environment. Environ. Biosafety Res. 6:37–53
    [Google Scholar]
  91. 89. 
    Overballe-Petersen S, Harms K, Orlando LA, Mayar JV, Rasmussen S et al. 2013. Bacterial natural transformation by highly fragmented and damaged DNA. PNAS 110:19860–65
    [Google Scholar]
  92. 90. 
    Pimentel ZT, Zhang Y. 2018. Evolution of the natural transformation protein, ComEC, in bacteria. Front. Microbiol. 9:2980
    [Google Scholar]
  93. 91. 
    Provvedi R, Chen I, Dubnau D 2001. NucA is required for DNA cleavage during transformation of Bacillus subtilis. Mol. Microbiol 40:634–44
    [Google Scholar]
  94. 92. 
    Provvedi R, Dubnau D. 1999. ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Mol. Microbiol 31:271–80
    [Google Scholar]
  95. 93. 
    Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys J-P 2006. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313:89–92
    [Google Scholar]
  96. 94. 
    Prudhomme M, Berge M, Martin B, Polard P 2016. Pneumococcal competence coordination relies on a cell-contact sensing mechanism. PLOS Genet 12:e1006113
    [Google Scholar]
  97. 95. 
    Puyet A, Greenberg B, Lacks SA 1990. Genetic and structural characterization of EndA. A membrane-bound nuclease required for transformation of Streptococcus pneumoniae. J. Mol. Biol 213:727–38
    [Google Scholar]
  98. 96. 
    Redfield RJ. 1988. Evolution of bacterial transformation: Is sex with dead cells ever better than no sex at all?. Genetics 119:213–21
    [Google Scholar]
  99. 97. 
    Ringel PD, Hu D, Basler M 2017. The role of type VI secretion system effectors in target cell lysis and subsequent horizontal gene transfer. Cell Rep 21:3927–40
    [Google Scholar]
  100. 98. 
    Rosenthal AZ, Qi Y, Hormoz S, Park J, Li SHJ, Elowitz MB 2018. Metabolic interactions between dynamic bacterial subpopulations. eLife 7:e3309
    [Google Scholar]
  101. 99. 
    Seitz P, Blokesch M. 2013. Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental gram-negative bacteria. FEMS Microbiol. Rev. 37:336–63
    [Google Scholar]
  102. 100. 
    Seitz P, Blokesch M. 2013. DNA-uptake machinery of naturally competent Vibrio cholerae. PNAS 110:17987–92
    [Google Scholar]
  103. 101. 
    Seitz P, Blokesch M. 2014. DNA transport across the outer and inner membranes of naturally transformable Vibrio cholerae is spatially but not temporally coupled. mBio 5:e01409–14
    [Google Scholar]
  104. 102. 
    Seitz P, Pezeshgi Modarres H, Borgeaud S, Bulushev RD, Steinbock LJ et al. 2014. ComEA is essential for the transfer of external DNA into the periplasm in naturally transformable Vibrio cholerae cells. PLOS Genet 10:e1004066
    [Google Scholar]
  105. 103. 
    Slager J, Kjos M, Attaiech L, Veening JW 2014. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 157:395–406
    [Google Scholar]
  106. 104. 
    Smith H, Wiersma K, Bron S, Venema G 1983. Transformation in Bacillus subtilis: purification and partial characterization of a membrane-bound DNA-binding protein. J. Bacteriol. 156:101–8
    [Google Scholar]
  107. 105. 
    Smith SB, Finzi L, Bustamante C 1992. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258:1122–26
    [Google Scholar]
  108. 106. 
    Steinmoen H, Knutsen E, Håvarstein LS 2002. Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. PNAS 99:7681–86
    [Google Scholar]
  109. 107. 
    Stevens KE, Chang D, Zwack EE, Sebert ME 2011. Competence in Streptococcus pneumoniae is regulated by the rate of ribosomal decoding errors. mBio 2:e00071–11
    [Google Scholar]
  110. 108. 
    Stingl K, Müller S, Scheidgen-Kleyboldt G, Clausen M, Maier B 2010. Composite system mediates two-step DNA uptake into Helicobacter pylori. PNAS 107:1184–89
    [Google Scholar]
  111. 109. 
    Straume D, Stamsås GA, Salehian Z, Håvarstein LS 2017. Overexpression of the fratricide immunity protein ComM leads to growth inhibition and morphological abnormalities in Streptococcus pneumoniae. Microbiology 163:9–21
    [Google Scholar]
  112. 110. 
    Touchon M, Moura de Sousa JA, Rocha EP 2017. Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr. Opin. Microbiol. 38:66–73
    [Google Scholar]
  113. 111. 
    Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A 2015. The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res 43:W401–7
    [Google Scholar]
  114. 112. 
    van Nieuwenhoven MH, Hellingwerf KJ, Venema G, Konings WN 1982. Role of proton motive force in genetic transformation of Bacillus subtilis. J. Bacteriol 151:771–76
    [Google Scholar]
  115. 113. 
    Veening JW, Blokesch M. 2017. Interbacterial predation as a strategy for DNA acquisition in naturally competent bacteria. Nat. Rev. Microbiol. 15:621–29
    [Google Scholar]
  116. 114. 
    Wang CY, Patel N, Wholey W-Y, Dawid S 2018. ABC transporter content diversity in Streptococcus pneumoniae impacts competence regulation and bacteriocin production. PNAS 115:E5776–85
    [Google Scholar]
  117. 115. 
    Wholey W-Y, Kochan TJ, Storck DN, Dawid S 2016. Coordinated bacteriocin expression and competence in Streptococcus pneumoniae contributes to genetic adaptation through neighbor predation. PLOS Pathog 12:e1005413
    [Google Scholar]
  118. 116. 
    Wiesner RS, Hendrixson DR, DiRita VJ 2003. Natural transformation of Campylobacter jejuni requires components of a type II secretion system. J. Bacteriol. 185:5408–18
    [Google Scholar]
  119. 117. 
    Zöllner R, Cronenberg T, Maier B 2019. Motor properties of PilT-independent type 4 pilus retraction in gonococci. J. Bacteriol. 201:e00778–18
    [Google Scholar]
/content/journals/10.1146/annurev-genet-112618-043641
Loading
/content/journals/10.1146/annurev-genet-112618-043641
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error