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Mechanisms Of, and Barriers To, Horizontal Gene Transfer Between Bacteria

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Mechanisms Of, and Barriers To, Horizontal Gene Transfer Between Bacteria FOCUS ON HORIZONTAL GENE TRANSFER MECHANISMS OF, AND BARRIERS TO, HORIZONTAL GENE TRANSFER BETWEEN BACTERIA Christopher M. Thomas* and Kaare M. Nielsen‡ Abstract | Bacteria evolve rapidly not only by mutation and rapid multiplication, but also by transfer of DNA, which can result in strains with beneficial mutations from more than one parent. Transformation involves the release of naked DNA followed by uptake and recombination. Homologous recombination and DNA-repair processes normally limit this to DNA from similar bacteria. However, if a gene moves onto a broad-host-range plasmid it might be able to spread without the need for recombination. There are barriers to both these processes but they reduce, rather than prevent, gene acquisition. The first evidence that horizontal gene transfer (HGT) informational genes of the central cellular machinery could occur was the recognition that virulence deter- such as DNA replication, transcription or translation minants could be transferred between pneumococci in tend not to spread rapidly, even if they confer anti biotic infected mice, a phenomenon that was later shown to resistance, compared for example to single-function- be mediated by the uptake of the genetic material DNA resistance determinants such as β-lactamases or in a process called transformation1. The subsequent aminoglycoside-modifying enzymes. However, the identification of gene transfer mediated by both plas- nature of the transfer mechanism can also determine the mids and viruses and the recognition of transposable organisms and genes that are most often involved. The elements provided the stepping stones to our current purpose of this review is to describe some of the mecha- picture of gene flux and the importance of mobile nisms that lead to horizontal gene acquisitions with a genetic elements2. Compositional analysis has revealed view to understanding what limitations there are to that considerable proportions of most bacterial genomes these processes. The journey therefore starts with DNA consist of horizontally acquired genes3. in a potential donor and considers the various steps (as Many horizontally acquired genes are likely to cause outlined in FIG. 1) until the DNA becomes a functional deleterious effects in the chromosome of the bacterial part of a recipient genome. We focus on natural trans- *School of Biosciences, University of Birmingham, recipient. Therefore, these bacteria will be lost from the formation and conjugation and consider single-cell Edgbaston, Birmingham population over time in the same way that deleterious events only. The subsequent population-dynamic aspects B15 2TT, UK. mutations are lost. Some horizontal acquisitions might of HGT events are dealt with elsewhere (see the article ‡Department of Pharmacy, be effectively neutral, and their survival will depend on by J.P. Gogarten and J.P. Townsend in this issue)5. University of Tromsø, chance events. However, horizontally acquired chro- N9037 Tromsø, Norway, and The Norwegian mosomal DNA that confers a selective advantage to the Natural transformation Institute of Gene Ecology, host, or mobile genetic elements that encode their own Natural transformation — the stable uptake, integ ration Science Park N9028 transfer and maintenance functions, have the potential and functional expression of extracellular DNA that can Tromsø, Norway. to spread rapidly within a bacterial population. Where occur under natural bacterial growth conditions — is e-mails: [email protected]; HGTs succeed between distantly related organisms, the only mechanism that can potentially explain how [email protected] the genes most likely to be involved tend to belong to bacteria acquire DNA from foreign species beyond the doi:10.1038/nrmicro1234 the simplest sets of functional networks4. Therefore, host range of mobile genetic elements or bacterio phages. NATURE REVIEWS | MICROBIOLOGY VOLUME 3 | SEPTEMBER 2005 | 711 © 2005 Nature Publishing Group REVIEWS Donor Deinococcus spp., green sulphur bacteria and many other Gram-negative bacteria8,9. Many human patho- 1 Entry into the transfer process • Release of naked DNA genic bacteria, including representatives of the genera • Integration of plasmid into chromosome Campylobacter, Haemophilus, Helicobacter, Neisseria, • Interaction with mating-pair formation apparatus Pseudomonas, Staphylococcus and Streptococcus, are • Presence of pac sites naturally transformable9. The conserved ability to • Packaging into phage particle acquire DNA molecules by natural transformation among a broad range of bacteria indicates that the genetic trait is functionally important in the environ- ment, enabling access to DNA as a source of nutri- 2 Selection of recipient ents or genetic information. Prerequisites for natural • Uptake sequences in DNA • Binding of naked DNA transformation include the release and persistence of • Phage receptor specificity extracellular DNA, the presence of competent bacte- • Pilus specificity rial cells and the ability of translocated chromosomal • Surface exclusion DNA to be stabilized by integration into the bacterial genome or the ability of translocated plasmid DNA to integrate or recircularize into self-replicating plasmids 3 Uptake + successful entry (FIG. 2). • Restriction • Antirestriction systems Release of extracellular DNA in the environment. • Selection against restriction sites Natural transformation relies on bacterial exposure to extracellular DNA molecules in the environment. DNA continually enters the environment upon release from decomposing cells, disrupted cells or viral particles, Recipient or through excretion from living cells. The release of 4 Establishment intact DNA from decomposing cells depends on the • Replication activity and location of nucleases and reactive chemi- • Integration • Homologous recombination cals. Active excretion of DNA has been reported for • Illegitimate recombination many genera of bacteria, including Acinetobacter, Alcaligenes, Azotobacter, Bacillus, Flavobacterium, Micrococcus, Pseudomonas and Streptococcus8–10. For Figure 1 | The process of horizontal gene transfer. instance, extracellular DNA has been found at con- A schematic outlining the stages through which DNA must µ go on its journey from donor to recipient bacteria. The centrations of up to 1–3 g per ml in liquid cultures 11 process begins with DNA in a potential donor cell becoming of an Acinetobacter sp. and Bacillus subtilis and up to available and ends when this DNA becomes a functional part 780 µg per ml in cultures of the environmental isolate of a recipient cell’s genome. Pseudomonas aeruginosa KYU-1 REF. 12. Recently, extracellular DNA has been identified as an important component in biofilm formation13. Nevertheless, the For natural transformation to occur, bacterial cells extent of, and role of, active release of DNA by bacteria must first develop a regulated physio logical state in natural, nutrient-limited habitats remains to be fully of COMPETENCE, which has been found to involve understood. approximately 20 to 50 proteins. With the exception Passive release of DNA from dead bacteria occurs of Neisseria gonorrhoeae, most naturally transform- after self-induced lysis, a process that results in broken able bacteria develop time-limited competence in cell walls and membranes and the subsequent exposure response to specific environmental conditions such to, and release of, cytoplasmic contents, including DNA, as altered growth conditions, nutrient access, cell in the environment14. Pathogenic microorganisms can density (by quorum sensing) or starvation. The also undergo lysis caused either by the host immune proportion of bacteria that develop competence in a system or the antibiotic treatment of infections. From bacterial population might range from near zero to studies of 14C-labelled Escherichia coli, it has been almost 100%. As the growth environments and factors estimated that between 95% and 100% of the bacte- that regulate competence development vary between rial DNA is released after contact with the immune bacterial species and strains6, there is no universal system15. Most of this DNA is probably degraded approach to determine if a given bacterial isolate can by DNases present in human serum and plasma. In develop competence as a part of its life cycle. To the one study, the mean DNase activity of 50 patients extent investigated, the proportion of bacteria found destroyed 90% of the added DNA of Haemophilus to be naturally transformable is approximately 1% of influenzae within a few minutes16. A different study, the validly described bacterial species7. The ability to however, reported longer persistence times for both take up naked DNA by natural transformation has chromosomal and plasmid DNA in serum17 — large been detected in archaea and divergent subdivisions plasmids and chromosomal DNA were substantially COMPETENCE The ability of bacteria to take up (phyla) of bacteria, including representatives of the degraded after a 4-hour exposure of a serum-sensitive extracellular DNA. Gram-positive bacteria, cyanobacteria, Thermus spp., E. coli strain, but smaller plasmids (pBR322 and 712 | SEPTEMBER 2005 | VOLUME 3 www.nature.com/reviews/micro © 2005 Nature Publishing Group FOCUS ON HORIZONTAL GENE TRANSFER Release of DNA by growing or decaying cells Stability of extracellular DNA in the environment. The persistence of extracellular DNA will determine the bacterial exposure time, and therefore the natural TRANSFORMATION FREQUENCY. The degradation kinetics of extracellular DNA
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