Unconventional lateral gene transfer in extreme thermophilic bacteria

International Microbiology

Volumn 14, Issue 4, 2011, Pages 187-199

  César, Carolina E ^a   Álvarez, Laura ^a   Bricio, Carlos ^a   van Heerden, Esta ^b   Littauer, Dereck ^b   Berenguer, José ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF THE FREE STATE   (South Africa)

Author keywords

Conjugation; Lateral gene transfer; Thermophiles; Thermus; Transformation

Indexed keywords

EID: 84862579401     PISSN: 11396709     EISSN: 16181905     Source Type: Journal    
DOI: 10.2436/20.1501.01.148     Document Type: Review

References (56)

1. Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, Shinkai A (2010) Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J Mol Biol 395:270-281
2. Al-Attar S, Westra ER, van der Oost J, Brouns SJ (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol Chem 392:277-289
3. Albers SV, Pohlschroder M (2009) Diversity of archaeal type IV pilinlike structures. Extremophiles 13:403-410
4. Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775-808
5. Alvarez L, Bricio C, Gómez MJ, Berenguer J (2011) Lateral transfer of the denitrification pathway genes among Thermus thermophilus strains. Appl Environ Microbiol 77:1352-1358
6. Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV (1998) Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14:442-444
7. Averhoff B (2009) Shuffling genes around in hot environments: the unique DNA transporter of Thermus thermophilus. FEMS Microbiol Rev 33:611-626
8. Bahl H, Scholz H, Bayan N, Charni M, Leblon G, Gulik-Krzywicki T, Shechter E, Fouet A, Mesnage S, Tosi-Couture E, Gounon P, Mock M, Conway de Macario E, Macario AJ, Fernandez-Herrero LA, Olabarria G Berenguer J, Blaser MJ, Kuen B, Lubitz W, Sara M, Pouwels PH, Kolen CP, Boot HJ, Resch S (1997) Molecular biology of S-layers. FEMS Microbiol Rev 20:47-98
9. Bricio C, Alvarez L, Gómez MJ, Berenguer J (2011) Partial and complete denitrification in Thermus thermophilus: lessons from genome drafts. Biochem Soc Trans 39:249-253
10. Bruggemann H, Chen C (2006) Comparative genomics of Thermus thermophilus: Plasticity of the megaplasmid and its contribution to a thermophilic lifestyle. J Biotechnol 124:654-661
11. Burkhardt J, Vonck J, Averhoff B (2011) Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27. J Biol Chem 286:9977-9984
12. Cabezón E, de la Cruz F (2006) TrwB: an F(1)-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Res Microbiol 157:299-305
13. Cava F, de Pedro MA, Schwarz H, Henne A, Berenguer J (2004) Binding to pyruvylated compounds as an ancestral mechanism to anchor the outer envelope in primitive bacteria. Mol Microbiol 52:677-690
14. Cava F, Hidalgo A, Berenguer J (2009) Thermus thermophilus as biological model. Extremophiles 13:213-231
15. Claverys JP, Martin B (2003) Bacterial competence genes: signatures of active transformation, or only remnants? Trends Microbiol 11:161-165
16. Claverys JP, Prudhomme M, Martin B (2006) Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Micrnhiol 60:451 -475
17. Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2:241-249
18. Draper O, César CE, Machon C, de la Cruz F, Llosa M (2005) Site-spe-cific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc Natl Acad Sci USA 102:16385-16390
19. Ferrnández-Lopez R, Garcillán-Barcia MP, Revilla C, Lázaro M, Vielva L, de la Cruz F (2006) Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol Rev 30:942-966
20. Friedrich A, Prust C, Hartsch T, Henne A, Averhoff B (2002) Molecular analyses of the natural transformation machinery and identification of pilus structures in the extremely thermmophilic bacterium Thermus thermophilus strain HB27 Appl Environ Microbiol 68:745-755
21. Friedrich A, Rumszauer J, Henne A, Averhoff B (2003) Pilin-like proteins in the extremely thermophilic bacterium Thermus thermophilus HB27: implication in competence for natural transformation and links to type IV pilus biogenesis. Appl Environ Microbiol 69:3695-3700
22. Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67:277-301
23. Hidaka Y, Hasegawa M, Nakahara T, Hoshino T (1994) The entire population of Thermus thermophilus cells is always competent at any growth phase. Biosci Biotechnol Biochem 58:1338-1339
24. Israel DA, Lou AS, Blaser MJ (2000) Characteristics of Helicobacter pylori natural transformation. FEMS Microbiol Lett 186:275-80
25. Jacob F, Wollman EL (1961) Viruses and genes. Sci Am 204:93-107
26. Jain R, Rivera MC, Moore JE, Lake JA (2003) Horizontal gene transfer accelerates genome innovation and evolution. Mol Biol Evol 20:1598-1602
27. Jakubowski SJ, Krishnamoorthy V, Cascales E, Christie PJ (2004) Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J Mol Biol 341:961-977
28. Johnsborg O, Eldholm V, Havarstein LS (2007) Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158: 767-778
29. Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36:6688-6719
30. Kovacs AT, Smits WK, Mironczuk AM, Kuipers OP (2009) Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environ Microbiol 11:1911-1922
31. Koyama Y, Hoshino T, Tomizuka N, Furukawa K (1986) Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp. J Bacteriol 166:338-340
32. Lawrence JG (1997) Selfish operons and speciation by gene transfer. Trends Microbiol 5:355-359
33. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563-602
34. Maier B, Potter L, So M, Long CD, Seifert HS, Sheetz MP (2002) Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 99:16012-16017
35. Mortier-Barriere I, Velten M, Dupaigne P, Mirouze N, Pietrement O, McGovern S, Fichant G, Martin B, Noirot P, Le Cam E, Polard P, Claverys JP (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130:824-836
36. Mossey P, Hudacek A, Das A (2010) Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7, and VirB8 for stabilization. J Bacteriol 192:2830-2838
37. Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, White O, Salzberg SL, Smith HO, Venter JC, Fraser CM (1999) Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399:323-329
38. Nunn DN, Lory S (1991) Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci USA 88: 3281-3285
39. Ochman H, Davalos LM (2006) The nature and dynamics of bacterial genomes. Science 311:1730-1733
40. Omelchenko MV, Wolf Yl, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Daly MJ, Koonin EV, Makarova KS (2005) Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5:57
41. Palmen R, Hellingwerf KJ (1997) Uptake and processing of DNA by Acinetobacter calcoaceticus-a review. Gene 192:179-190
42. Pérez-Mendoza D, de la Cruz F (2009) Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any? BMC Genomics 10-71
43. Ramírez-Arcos S, Fernández-Herrero LA, Berenguer J (1998) A thermophilic nitrate reductase is responsible for the strain specific anaerobic growth of Thermus thermophilus HB8. Biochim Biophys Acta 1396:215-227
44. Ramírez-Arcos S, Fernández-Herrero LA, Marín I, Berenguer J (1998) Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. J Bacteriol 180:3137-3143
45. Redfield RJ (1993) Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered 84:400-404
46. Rumszauer J, Schwarzenlander C, Averhoff B (2006) Identification, subcellular localization and functional interactions of PilMNOWQ and PilA4 involved in transformation competency and pilus biogenesis in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273:3261-3272
47. Ryan FJ, Lederberg J (1946) Reverse-mutation and adaptation in leucineless Neurospora. Proc Natl Acad Sci USA 32:163-173
48. Schwarzenlander C, Averhoff B (2006) Characterization of DNA transport in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273: 4210-4218
49. Schwarzenlander C, Haase W, Averhoff B (2009) The role of single subunits of the DNA transport machinery of Thermus thermophilus HB27 in DNA binding and transport. Environ Microbiol 11:801-808
50. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EP, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74:434-452
51. Waksman G, Fronzes R (2010) Molecular architecture of bacterial type IV secretion systems. Trends Biochem Sci 35:691-698
52. Wallden K, Rivera-Calzada A, Waksman G (2010) Type IV secretion systems: versatility and diversity in function. Cell Microbiol 12;1203-1212
53. Wozniak RA, Waldor MK (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8:552-863
54. Yu MX, Slater MR, Ackermann HW (2006) Isolation and characterization of Thermus bacteriophages. Arch Virol 151:663-679
55. Zahrl D, Wagner M, Bischof K, Bayer M, Zavecz B, Beranek A, Ruckenstuhl C, Zarfel GE, Koraimann G(2005) Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems. Microbiology 151:3455-3467
56. Zupan J, Hackworth CA, Aguilar J, Ward D, Zambryski P (2007) VirB1* promotes T-pilus formation in the vir-Type IV secretion system ofAgrobacterium tumefaciens. J Bacteriol 189:6551-6563