Beyond the canonical strategies of horizontal gene transfer in prokaryotes

Current Opinion in Microbiology

Volumn 38, Issue , 2017, Pages 95-105

  García Aljaro, Cristina ^a   Ballesté, Elisenda ^a   Muniesa, Maite ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; NANOTUBE;

AUTOLYSIS; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; CED SYSTEM; DNA STRUCTURE; HORIZONTAL GENE TRANSFER; INTEGRATING CONJUGATIVE ELEMENT; MEMBRANE VESICLE; MOBILIZATION; NON REPLICATING BACTEROIDES UNIT; NONHUMAN; PHAGE INDUCIBLE ELEMENT; PROKARYOTE; REVIEW; BACTERIUM; GENETICS; INTERSPERSED REPEAT; PROKARYOTIC CELL;

BACTERIA; GENE TRANSFER, HORIZONTAL; INTERSPERSED REPETITIVE SEQUENCES; PROKARYOTIC CELLS;

EID: 85020281945     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2017.04.011     Document Type: Review

References (101)

1. Darmon, E., Leach, D.R.F., Bacterial genome instability. Microbiol. Mol. Biol. Rev. 78 (2014), 1–39.
2. Vos, M., Hesselman, M.C., te Beek, T.A., van Passel, M.W.J., Eyre-Walker, A., Rates of lateral gene transfer in prokaryotes: high but why?. Trends Microbiol. 23 (2015), 598–605.
3. Keeling, P.J., Palmer, J.D., Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9 (2008), 605–618.
4. Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.L., Brüssow, H., Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6 (2003), 417–424.
5. Forterre, P., Prangishvili, D., The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3 (2013), 558–565.
6. Marrs, B., Genetic recombination in Rhodopseudomonas capsulata. Proc. Natl. Acad. Sci. U. S. A. 71 (1974), 971–973.
7. Solioz, M., Yen, H.C., Marris, B., Release and uptake of gene transfer agent by Rhodopseudomonas capsulata. J. Bacteriol. 123 (1975), 651–657.
8. 8•• Lang, A.S., Zhaxybayeva, O., Beatty, J.T., Gene transfer agents: phage-like elements of genetic exchange. Nat. Rev. Microbiol. 10 (2012), 472–482 In this review, authors provide the most relevant characteristics of the GTAs identified, along with potential functions for these agents and the possible evolutionary forces that act on the genes involved in their production.
9. Lang, A.S., Beatty, J.T., Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol. 15 (2007), 54–62.
10. McDaniel, L.D., Young, E., Delaney, J., Ruhnau, F., Ritchie, K.B., Paul, J.H., High frequency of horizontal gene transfer in the oceans. Science, 330, 2010, 50.
11. Penadés, J.R., Chen, J., Quiles-Puchalt, N., Carpena, N., Novick, R.P., Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23 (2014), 171–178.
12. Zhan, Y., Huang, S., Voget, S., Simon, M., Chen, F., A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents. Sci. Rep., 6, 2016, 30372.
13. Huang, S., Zhang, Y., Chen, F., Jiao, N., Complete genome sequence of a marine roseophage provides evidence into the evolution of gene transfer agents in alphaproteobacteria. Virol. J., 8, 2011, 124.
14. Hynes, A.P., Mercer, R.G., Watton, D.E., Buckley, C.B., Lang, A.S., DNA packaging bias and differential expression of gene transfer agent genes within a population during production and release of the Rhodobacter capsulatus gene transfer agent, RcGTA. Mol. Microbiol. 85 (2012), 314–325.
15. Brimacombe, C.A., Ding, H., Beatty, J.T., Rhodobacter capsulatus DprA is essential for RecA-mediated gene transfer agent (RcGTA) recipient capability regulated by quorum-sensing and the CtrA response regulator. Mol. Microbiol. 92 (2014), 1260–1278.
16. Guglielmini, J., Quintais, L., Garcillán-Barcia, M.P., de la Cruz, F., Rocha, E.P.C., The repertoire of ICE in prokaryotes underscores the unity diversity, and ubiquity of conjugation. PLoS Genet., 7, 2011, e1002222.
17. Ambroset, C., Coluzzi, C., Guédon, G., Devignes, M.-D., Loux, V., Lacroix, T., Payot, S., Leblond-Bourget, N., New insights into the classification and integration specificity of Streptococcus integrative conjugative elements through extensive genome exploration. Front. Microbiol., 6, 2015, 1483.
18. Johnson, C.M., Grossman, A.D., Integrative and Conjugative Elements (ICEs): what they do and how they work. Annu. Rev. Genet. 49 (2015), 577–601.
19. Carraro, N., Poulin, D., Burrus, V., Replication and active partition of Integrative and Conjugative Elements (ICEs) of the SXT/R391 family: the line between ICEs and conjugative plasmids is getting thinner. PLOS Genet., 11, 2015, e1005298.
20. Grohmann, E., Autonomous plasmid-like replication of Bacillus ICE Bs1: a general feature of integrative conjugative elements?. Mol. Microbiol. 75 (2010), 261–263.
21. Dimopoulou, I.D., Russell, J.E., Mohd-Zain, Z., Herbert, R., Crook, D.W., Site-specific recombination with the chromosomal tRNA(Leu) gene by the large conjugative Haemophilus resistance plasmid. Antimicrob. Agents Chemother. 46 (2002), 1602–1603.
22. Guérillot, R., Da Cunha, V., Sauvage, E., Bouchier, C., Glaser, P., Modular evolution of TnGBSs, a new family of integrative and conjugative elements associating insertion sequence transposition, plasmid replication, and conjugation for their spreading. J. Bacteriol. 195 (2013), 1979–1990.
23. Lee, C.A., Babic, A., Grossman, A.D., Autonomous plasmid-like replication of a conjugative transposon. Mol. Microbiol. 75 (2010), 268–279.
24. Waldor, M.K., Mobilizable genomic islands: going mobile with oriT mimicry. Mol. Microbiol. 78 (2010), 537–540.
25. Bellanger, X., Payot, S., Leblond-Bourget, N., Guédon, G., Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol. Rev. 38 (2014), 720–760.
26. Hochhut, B., Marrero, J., Waldor, M.K., Mobilization of plasmids and chromosomal DNA mediated by the SXT element, a constin found in Vibrio cholerae O139. J. Bacteriol. 182 (2000), 2043–2047.
27. Beaber, J.W., Hochhut, B., Waldor, M.K., Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J. Bacteriol. 184 (2002), 4259–4269.
28. Salyers, A.A., Shoemaker, N.B., Stevens, A.M., Li, L.Y., Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol. Rev. 59 (1995), 579–590.
29. Daccord, A., Ceccarelli, D., Burrus, V., Integrating conjugative elements of the SXT/R391 family trigger the excision and drive the mobilization of a new class of Vibrio genomic islands. Mol. Microbiol. 78 (2010), 576–588.
30. Penadés, J.R., Christie, G.E., The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu. Rev. Virol. 2 (2015), 181–201.
31. Novick, R.P., Christie, G.E., Penadés, J.R., The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8 (2010), 541–551.
32. Quiles-Puchalt, N., Carpena, N., Alonso, J.C., Novick, R.P., Marina, A., Penadés, J.R., Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 6016–6021.
33. Frígols, B., Quiles-Puchalt, N., Mir-Sanchis, I., Donderis, J., Elena, S.F., Buckling, A., Novick, R.P., Marina, A., Penadés, J.R., Virus satellites drive viral evolution and ecology. PLoS Genet., 11, 2015, e1005609.
34. Tormo-Más, M.A., Mir, I., Shrestha, A., Tallent, S.M., Campoy, S., Lasa, I., Barbé, J., Novick, R.P., Christie, G.E., Penadés, J.R., Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465 (2010), 779–782.
35. Novick, R.P., Ram, G., The floating (pathogenicity) island: a genomic dessert. Trends Genet. 32 (2016), 114–126.
36. Maiques, E., Ubeda, C., Tormo, M.A., Ferrer, M.D., Lasa, I., Novick, R.P., Penades, J.R., Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J. Bacteriol. 189 (2007), 5608–5616.
37. 37• Martínez-Rubio, R., Quiles-Puchalt, N., Martí, M., Humphrey, S., Ram, G., Smyth, D., Chen, J., Novick, R.P., Penadés, J.R., Phage-inducible islands in the Gram-positive cocci. ISME J. 11 (2017), 1029–1042 Authors’ findings describe that the family of phage-inducible chromosomal islands include elements that are conserved in at least three genera of cocci, Staphylococci, Streptococci and Enterococci.
38. Lossouarn, J., Nesbø, C.L., Mercier, C., Zhaxybayeva, O., Johnson, M.S., Charchuck, R., Farasin, J., Bienvenu, N., Baudoux, A.C., Michoud, G., et al. “Ménage à trois”: a selfish genetic element uses a virus to propagate within Thermotogales. Environ. Microbiol. 17 (2015), 3278–3288.
39. Krupovic, M., Gonnet, M., Ben, Hania W., Forterre, P., Erauso, G., Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS One, 8, 2013, e49044.
40. Arnold, H.P., She, Q., Phan, H., Stedman, K., Prangishvili, D., Holz, I., Kristjansson, J.K., Garrett, R., Zillig, W., The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol. Microbiol. 34 (1999), 217–226.
41. Chen, J., Ram, G., Penadés, J.R., Brown, S., Novick, R.P., Pathogenicity island-directed transfer of unlinked chromosomal virulence genes. Mol. Cell 57 (2015), 138–149.
42. 42• Imamovic, L., Ballesté, E., Martínez-Castillo, A., García-Aljaro, C., Muniesa, M., Heterogeneity in phage induction enables the survival of the lysogenic population. Environ. Microbiol. 18 (2016), 957–969 Authors demonstrate that temperate phages induce differentially within the E. coli lysogenic population. Some cells induce phages, are lysed, allow the expression of the Shiga toxin and the spread of phages. A second fraction remain uninduced, allowing the population to prevail.
43. Tian, T., Burrage, K., Bistability and switching in the lysis/lysogeny genetic regulatory network of bacteriophage lambda. J. Theor. Biol. 227 (2004), 229–237.
44. Loś, J.M., Loś, M., Węgrzyn, A., Węgrzyn, G., Altruism of Shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results. Front. Cell. Infect. Microbiol., 2, 2012, 166.
45. Zeng, Z., Liu, X., Yao, J., Guo, Y., Li, B., Li, Y., Jiao, N., Wang, X., Cold adaptation regulated by cryptic prophage excision in Shewanella oneidensis. ISME J. 10 (2016), 2787–2800.
46. Werren, J.H., Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 10863–10870.
47. Díez-Villaseñor, C., Almendros, C., García-Martínez, J., Mojica, F.J.M., Diversity of CRISPR loci in Escherichia coli. Microbiology 156 (2010), 1351–1361.
48. 48•• Almendros, C., Mojica, F.J.M., Díez-Villaseñor, C., Guzmán, N.M., García-Martínez, J., CRISPR-Cas functional module exchange in Escherichia coli. MBio, 5, 2013 e00767–13 This work from the authors that first described the CRISPR-Cas systems, investigates the evolutionary pathways that have led to the significantly different CRISPR-Cas subtypes in E. coli. In doing so, this information offers a novel and wider understanding of the variety and relevance of these regions within the species.
49. Price, V.J., Huo, W., Sharifi, A., Palmer, K.L., CRISPR-cas and restriction-modification act additively against conjugative antibiotic resistance plasmid transfer in Enterococcus faecalis. mSphere 1 (2016), e00064–16.
50. Palmer, K.L., Gilmore, M.S., Multidrug-resistant enterococci lack CRISPR-cas. MBio, 1, 2010 e00227–10–e00227–19.
51. Almendros, C., Guzmán, N.M., García-Martínez, J., Mojica, F.J.M., Anti-cas spacers in orphan CRISPR4 arrays prevent uptake of active CRISPR-Cas I-F systems. Nat. Microbiol., 1, 2016, 16081.
52. Bondy-Denomy, J., Pawluk, A., Maxwell, K.L., Davidson, A.R., Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493 (2012), 429–432.
53. 53• Dalia, A.B., Seed, K.D., Calderwood, S.B., Camilli, A., A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. Proc. Natl. Acad. Sci. 112 (2015), 10485–10490 A study highlighting the relevance of transformation in HGT in Vibrio and a mechanism for inhibition of natural transformation as a strategy to regulate HGT in pathogenic bacteria.
54. Croucher, N.J., Mostowy, R., Wymant, C., Turner, P., Bentley, S.D., Fraser, C., Horizontal DNA transfer mechanisms of bacteria as weapons of intragenomic conflict. PLOS Biol., 14, 2016, e1002394.
55. Asadulghani, M., Ogura, Y., Ooka, T., Itoh, T., Sawaguchi, A., Iguchi, A., Nakayama, K., Hayashi, T., The defective prophage pool of Escherichia coli O157: prophage-prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog., 5, 2009, e1000408.
56. Davies, E.V., James, C.E., Williams, D., O'Brien, S., Fothergill, J.L., Haldenby, S., Paterson, S., Winstanley, C., Brockhurst, M.A., Temperate phages both mediate and drive adaptive evolution in pathogen biofilms. Proc. Natl. Acad. Sci. 113 (2016), 8266–8271.
57. Vale, F.F., Nunes, A., Oleastro, M., Gomes, J.P., Sampaio, D.A., Rocha, R., Vítor, J.M.B., Engstrand, L., Pascoe, B., Berthenet, E., et al. Genomic structure and insertion sites of Helicobacter pylori prophages from various geographical origins. Sci. Rep., 7, 2017, 42471.
58. Imamovic, L., Serra-Moreno, R., Jofre, J., Muniesa, M., Quantification of Shiga toxin 2-encoding bacteriophages, by real-time PCR and correlation with phage infectivity. J. Appl. Microbiol. 108 (2010), 1105–1114.
59. Karimova, M., Splith, V., Karpinski, J., Pisabarro, M.T., Buchholz, F., Discovery of Nigri/nox and Panto/pox site-specific recombinase systems facilitates advanced genome engineering. Sci. Rep., 6, 2016, 30130.
60. Berleman, J., Auer, M., The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ. Microbiol. 15 (2013), 347–354.
61. 61• Roier, S., Zingl, F.G., Cakar, F., Durakovic, S., Kohl, P., Eichmann, T.O., Klug, L., Gadermaier, B., Weinzerl, K., Prassl, R., et al. A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria. Nat. Commun., 7, 2016, 10515 Authors propose a new general mechanism of production of outer membrane vesicles based on phospholipid accumulation in the outer membrane. Their findings reveal a highly conserved mechanism among Gram-negative bacteria, and provides clues on the regulation of vesicles biogenesis.
62. Gaudin, M., Gauliard, E., Schouten, S., Houel-Renault, L., Lenormand, P., Marguet, E., Forterre, P., Hyperthermophilic archaea produce membrane vesicles that can transfer DNA. Environ. Microbiol. Rep. 5 (2013), 109–116.
63. 63•• Biller, S.J., Schubotz, F., Roggensack, S.E., Thompson, A.W., Summons, R.E., Chisholm, S.W., Bacterial vesicles in marine ecosystem. Science 343 (2014), 183–186 A work investigating the generation of extracellular vesicles in marine environments, and in phtoautotrophs, facilitating interactions between cells and their environment from a distance. Moreover, the report the abundance of vesicles carrying DNA from diverse bacteria in coastal and open-ocean seawater samples. Their implication in marine carbon flux and as agents of HGT in marine communities.
64. Dubey, G.P., Ben-Yehuda, S., Intercellular nanotubes mediate bacterial communication. Cell 144 (2011), 590–600.
65. Dubey, G.P., Malli Mohan, G.B., Dubrovsky, A., Amen, T., Tsipshtein, S., Rouvinski, A., Rosenberg, A., Kaganovich, D., Sherman, E., Medalia, O., et al. Architecture and Characteristics of Bacterial Nanotubes. Dev. Cell 36 (2016), 453–461.
66. Naor, A., Gophna, U., Cell fusion and hybrids in Archaea: prospects for genome shuffling and accelerated strain development for biotechnology. Bioengineered 4 (2013), 126–129.
67. Hamilton, H.L., Dillard, J.P., Natural transformation of Neisseria gonorrhoeae: From DNA donation to homologous recombination. Mol. Microbiol. 59 (2006), 376–385.
68. Duffin, P.M., Seifert, H.S., Genetic transformation of Neisseria gonorrhoeae shows a strand preference. FEMS Microbiol. Lett. 334 (2012), 44–48.
69. Steinmoen, H., Knutsen, E., Håvarstein, L.S., Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 7681–7686.
70. Chiura, H.X., Generalized gene transfer by virus-like particules from marine bacteria. Aquat. Microb. Ecol. 13 (1997), 75–83.
71. Anderson, L.M., Bott, K.F., DNA packaging by the Bacillus subtilis defective bacteriophage PBSX. J. Virol. 54 (1985), 773–780.
72. Barbian, K.D., Minnick, M.F., A bacteriophage-like particle from Bartonella bacilliformis. Microbiology 146 (2000), 599–609.
73. Guy, L., Nystedt, B., Toft, C., Zaremba-Niedzwiedzka, K., Berglund, E.C., Granberg, F., Näslund, K., Eriksson, A.-S., Andersson, S.G.E., A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella. PLoS Genet., 9, 2013, e1003393.
74. Matson, E.G., Thompson, M.G., Humphrey, S.B., Zuerner, R.L., Stanton, T.B., Identification of genes of VSH-1, a prophage-like gene transfer agent of Brachyspira hyodysenteriae. J. Bacteriol. 187 (2005), 5885–5892.
75. Rapp, B.J., Wall, J.D., Genetic transfer in Desulfovibrio desulfuricans. Proc. Natl. Acad. Sci. U. S. A. 84 (1987), 9128–9130.
76. Bertani, G., Transduction-like gene transfer in the methanogen Methanococcus voltae. J Bacteriol 181 (1999), 2992–3002.
77. Biers, E.J., Wang, K., Pennington, C., Belas, R., Chen, F., Moran, M.A., Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Appl. Env. Microbiol. 74 (2008), 2933–2939.
78. Paul, J.H., Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas?. ISME J. 2 (2008), 579–589.
79. Lang, A.S., Beatty, J.T., Importance of widespread gene transfer agent genes in α-proteobacteria. Trends Microbiol. 15 (2007), 54–62.
80. Matos, R.C., Lapaque, N., Rigottier-Gois, L., Debarbieux, L., Meylheuc, T., Gonzalez-Zorn, B., Repoila, F., de Lopes, M.F., Serror, P., Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLoS Genet., 9, 2013.
81. Ruzin, A., Lindsay, J., Novick, R.P., Molecular genetics of SaPI1 – a mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 41 (2001), 365–377.
82. Mašlaňová, I., Doškař, J., Varga, M., Kuntová, L., Mužík, J., Malúšková, D., Růžičková, V., Pantůček, R., Bacteriophages of Staphylococcus aureus efficiently package various bacterial genes and mobile genetic elements including SCCmec with different frequencies. Environ. Microbiol. Rep. 5 (2013), 66–73.
83. Chen, J., Novick, R.P., Phage-mediated intergeneric transfer of toxin genes. Science 323 (2009), 139–141.
84. Scott, J., Thompson-Mayberry, P., Lahmamsi, S., King, C.J., McShan, W.M., Phage-associated mutator phenotype in group A Streptococcus. J. Bacteriol. 190 (2008), 6290–6301.
85. Han, X., Du, X.-D., Southey, L., Bulach, D.M., Seemann, T., Yan, X.-X., Bannam, T.L., Rood, J.I., Functional analysis of a bacitracin resistance determinant located on ICECp1, a novel Tn916-like element from a conjugative plasmid in Clostridium perfringens. Antimicrob. Agents Chemother. 59 (2015), 6855–6865.
86. De Maayer, P., Chan, W.-Y., Martin, D.A.J., Blom, J., Venter, S.N., Duffy, B., Cowan, D.A., Smits, T.H.M., Coutinho, T.A., Integrative conjugative elements of the ICEPan family play a potential role in Pantoea ananatis ecological diversification and antibiosis. Front. Microbiol., 6, 2015.
87. Mata, C., Navarro, F., Miro, E., Walsh, T.R., Mirelis, B., Toleman, M., Prevalence of SXT/R391-like integrative and conjugative elements carrying blaCMY-2 in Proteus mirabilis. J. Antimicrob. Chemother. 66 (2011), 2266–2270.
88. Rodríguez-Blanco, A., Lemos, M.L., Osorio, C.R., Unveiling the pan-genome of the SXT/R391 family of ICEs: molecular characterisation of new variable regions of SXT/R391-like ICEs detected in Pseudoalteromonas sp. and Vibrio scophthalmi. Antonie Van Leeuwenhoek 109 (2016), 1141–1152.
89. Pembroke, J.T., Piterina, A.V., A novel ICE in the genome of Shewanella putrefaciens W3-18-1: comparison with the SXT/R391 ICE-like elements. FEMS Microbiol. Lett. 264 (2006), 80–88.
90. Rumbo, C., Fernández-Moreira, E., Merino, M., Poza, M., Mendez, J.A., Soares, N.C., Mosquera, A., Chaves, F., Bou, G., Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob. Agents Chemother. 55 (2011), 3084–3090.
91. Hagemann, S., Stöger, L., Kappelmann, M., Hassl, I., Ellinger, A., Velimirov, B., DNA-bearing membrane vesicles produced by Ahrensia kielensis and Pseudoalteromonas marina. J. Basic Microbiol. 54 (2014), 1062–1072.
92. Jiang, Y., Kong, Q., Roland, K.L., Curtiss, R., Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity. Int. J. Med. Microbiol. 304 (2014), 431–443.
93. Kolling, G.L., Matthews, K.R., Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl. Environ. Microbiol. 65 (1999), 1843–1848.
94. Dorward, D.W., Garon, C.F., Judd, R.C., Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 171 (1989), 2499–2505.
95. Klieve, A.V., Yokoyama, M.T., Forster, R.J., Ouwerkerk, D., Bain, P.A., Mawhinney, E.L., Naturally occurring DNA transfer system associated with membrane vesicles in cellulolytic Ruminococcus spp. of ruminal origin. Appl. Environ. Microbiol. 71 (2005), 4248–4253.
96. Pérez-Cruz, C., Carrión, O., Delgado, L., Martinez, G., López-Iglesias, C., Mercade, E., New type of outer membrane vesicle produced by the gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl. Environ. Microbiol. 79 (2013), 1874–1881.
97. Liao, S., Klein, M.I., Heim, K.P., Fan, Y., Bitoun, J.P., Ahn, S.-J., Burne, R.A., Koo, H., Brady, L.J., Wen, Z.T., Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J. Bacteriol. 196 (2014), 2355–2366.
98. Soler, N., Marguet, E., Verbavatz, J.M., Forterre, P., Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res. Microbiol. 159 (2008), 390–399.
99. Mevarech, M., Werczberger, R., Genetic transfer in Halobacterium volcanii. J. Bacteriol. 162 (1985), 461–462.
100. Schleper, C., Holz, I., Janekovic, D., Murphy, J., Zillig, W., A multicopy plasmid of the extremely thermophilic archaeon Sulfolobus effects its transfer to recipients by mating. J. Bacteriol. 177 (1995), 4417–4426.
101. Kearns, D.B., A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8 (2010), 634–644.