Abstract
Horizontal gene flow is a driving force for bacterial adaptation. Among the three distinct mechanisms of gene transfer in bacteria, conjugation, transduction, and transformation, the latter, which includes competence induction, DNA binding, and DNA uptake, is perhaps the most versatile mechanism and allows the incorporation of free DNA from diverse bacterial species. Here we review DNA transport machineries mediating uptake of naked DNA in gram-positive and gram-negative bacteria. Different putative models of transformation machineries comprising components similar to proteins of type IV pili are presented. Emphasis is placed on a comparative discussion of the underlying mechanisms of DNA transfer in mesophilic and extremely thermophilic bacteria, highlighting conserved and distinctive features of these transformation machineries.
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Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, Koomey M (2002) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46:749–760
Aravind I, Tatusov RL, Wolf YL, Walker DR, Koonin EV (1998) Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends in Gen 14:442–444
Bitter W (2003) Secretins of Pseudomonas aeruginosa: large holes in the outer membrane. Arch Microbiol 179:307–314
Caston J, Carrascosa J, de Pedro M, Berenguer J (1988) Identification of a crystalline layer on the cell envelope of the thermophilic eubacterium Thermus thermophilus. FEMS Lett 51:225–230
Chen I, Gotschlich EC (2001) ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J Bacteriol 183:3160–3168
Chen I, Dubnau D (2003) DNA transport during transformation. Frontiers Biosci 8:544–556
Chen LY, Chen DY, Miaw J, Hu NT (1996) XpsD, an outer membrane protein required for protein secretion by Xanthomonas campestris pv. campestris, forms a multimer. J Biol Chem 271:2703–2708
Claverys JP, Havarstein LS (2002) Extracellular-peptide control of competence for genetic transformation in Streptococcus pneumoniae. Frontiers Biosci 7:1798–1814
Collins RF, Davidsen L, Derrick JP, Ford RC, Tonjum T (2001) Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J Bacteriol 183:3825–3832
De Vries J, Meier P, Wackernagel W (2001) The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiol Lett 195:211–215
Doolittle WF (1999) Lateral genomics. Trends Cell Bio 9:M5-M8
Dougherthy BA, Smith HO (1999) Identification of Haemophilus influenzae Rd transformation genes using cassette mutagenesis. Microbiology 145:401–409
Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244
Forest KT, Tainer JA (1997) Type-4-pilus-structure:outside to inside and top to bottom. Gene 192:165–169
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 67:3140–3148
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 thermophilic bacterium Thermus thermophilus HB27. Appl Environ Microbiol 68:745–755
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
Fussenegger M, Rudel T, Barten R, Ryll R, Meyer TF (1997) Transformation competence and type-4-pilus biogenesis in Neisseria gonorrhoeae - a review. Gene 192:125–134
Genin S, Boucher CA (1994) A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet 243:112–118
Graupner S, Weger N, Sohni M, Wackernagel W (2001) Requirement of novel competence genes pilT and pilU of Pseudomonas stutzeri for natural transformation and suppression of pilT deficiency by a hexahistidine tag on the type IV pilus protein PilAI. J Bacteriol 183:4694–4701
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
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 10:233–243
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 41:379–391
Kaiser D (2000) Bacterial motility: How do pili pull? Current Biol 10:R777-R780
Kang Y, Liu H, Genin S, Schell MA, Denny TP (2002) Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol Microbiol 46:427–437
Karudapuram S, Zhao X, Barcak GJ (1995) DNA sequence and characterization of Haemophilus influenzae dprA +, a gene required for chromosomal but not plasmid DNA transformation. J Bacteriol 177:3235–3240
Koyama Y, Hoshino T, Tomizuka N, Furukawa K (1986) Genetic transformation of the extreme thermophile Thermus thermophilus and other Thermus spp. J Bacteriol 166:338–340
Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602
Maier E, Polleichtner G, Boeck B, Schinzel R, Benz R (2001) Identification of the outer membrane porin of Thermus thermophilus HB8: the channel-forming complex has an unusually high molecular mass and an extremely large single-channel conductance. J Bacteriol 183:800–803
Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314
Merz AJ, So M (2000) Interactions of pathogenic Neisseriae with epithelial cell membranes. Annu Rev Cell Dev Biol 16:423–457
Merz AJ, So M, Sheetz MP (2000) Pilus retraction powers bacterial twitching motility. Nature 407:98–102
Nelson KE, Clayton R A, 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, Fraser CM, et al. (1999) Evidence for lateral gene transfer between archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329
Nouwen N, Stahlberg AP, Pugsley AP, Engel A (2000) Domain structure of secretin PulD revealed by limited proteolysis and electron microscopy. Embo J 19:2229–2236
Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial evolution. Nature 405:299–304
Palmen R, Hellingwerf KJ (1997) Uptake and processing of DNA by Acinetobacter calcoaceticus. Gene 192:179–190
Pestova EV, Morrison DA (1998) Isolation and characterization of three Streptococcus pneumoniae transformation-specific loci by use of a lacZ reporter insertion vector. J Bacteriol 180:2701–2710
Porstendörfer D, Drotschmann U, Averhoff B (1997) A novel competence gene, comP, is essential for natural transformation of Acinetobacter sp. strain BD413. Appl Environ Microbiol 63:4150–4157
Provvedi R, Dubnau D (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Mol Microbiol 31:271–280
Sauvonnet N, Vignon G, Pugsley AP, Gounon P (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 19:2221–2228
Smeets LC, Kusters JG (2002) Natural transformation in Helicobacter pylori: DNA transport in an unexpected way. Trends Microbiol 10:159–162
Strom MS, Lory S (1993) Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 47:565–596
Thanassi DG (2002) Ushers and secretins: channels for the secretion of folded proteins across the bacterial outer membrane. J Mol Microbiol Biotechnol 4:11–20
Tonjum T, Koomey M (1997) The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/function relationship—a review. Gene 192:155–163
White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, et al (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577
Wolfgang M, Lauer P, Hae-Sun P, Brossay L, Herbert J, Koomey M (1998) PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29:321–330
Wolfgang M, van Putten JP, Hayes SF, Koomey M (1999) The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol Microbiol 31:1345–1357
Yoshihara S, Geng X, Okamoto S, Yura K, Murata T, Go M, Ohmori M, Ikeuchi M (2001) Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile Synechocystis sp. PCC6803. Plant Cell Physiol 42:63–73
Acknowledgements
Work from the authors laboratory was supported by grants Av 9/4–4, Av/9/4–5 and Av9/5–1 from the Deutsche Forschungsgemeinschaft. A. Friedrich was supported by the Stiftung Stipendien Fonds des Verbandes der Chemischen Industrie. The authors thank Nathan Weyand (Oregon Health Sciences University, Portland, Oregon) for critically reading the manuscript.
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Averhoff, B., Friedrich, A. Type IV pili-related natural transformation systems: DNA transport in mesophilic and thermophilic bacteria. Arch Microbiol 180, 385–393 (2003). https://doi.org/10.1007/s00203-003-0616-6
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DOI: https://doi.org/10.1007/s00203-003-0616-6