Novel modes of lateral gene transfer in bacteria

Understanding the mechanisms of lateral gene transfer (LGT) between bacteria is crucial to our understanding of microbial evolution. It is also important for human health as LGT facilitates the emergence and spread of bacterial virulence and antibiotic resistance. The three ‘classical’ mechanisms of LGT; transformation (in which naked DNA is taken up from the environment), transduction (by which bacteriophage facilitate gene transfer by packaging host DNA as well as their own) and conjugation (when plasmids encode a pilus by which they can be transferred from cell to cell) have been important in the emergence of molecular biology. Three other mechanisms by which DNA can be transferred between bacteria have come to light, potentially broadening our understanding of the importance of LGT in the microbial biosphere.

Gene Transfer Agents (GTAs)

GTAs are virus-like particles that carry random pieces of the producing cell’s genome. The best characterised GTA was discovered in 1974 from the purple, non-sulphur photosynthetic bacterium Rhodobacter capsulatus, a member of the alpha-proteobacteria. The R. capsulatus GTA (RcGTA) packages 4.5kb of DNA, but is encoded by a 14.1kb cluster of 15 genes on the R. capsulatus chromosome. Many of these genes have homology with bacteriophage structural genes. It is unclear how RcGTA particles are released from the cell, as no recognisable lysis genes have been identified. Transcription of the RcGTA gene cluster has been shown to be under the control of a sensor kinase/response regulatory system that transduces environmental signals. RcGTA-like gene clusters are widespread throughout the alpha-proteobacteria and phlogenetic trees based on RcGTA-like sequence recapitulate phylogenies based on 16s rRNA sequences suggesting that the RcGTA ancestor arose early in the evolution of the alpha-proteobacteria lineage.

Other GTAs (with probable independent origins) have been identified in a diverse range of prokarya including the archaebacterium Methanococcus voltae, the delta-proteobacterium Desulfovibrio desulfuricans and the spirochete Brachyspira hyodysenteriae.  None of them packages more than 14kb of DNA, and all of them take the form of small bacteriophage. It appears most likely that GTAs have been derived from bacteriophage that have lost their ability to self-propagate. Recent data suggests that alpha-proteobacterial GTAs are common in marine environments, and transfer genes at high frequency between diverse classes of alpha-proteobacteria. These ‘generalised transducing machines’, under the control of bacterial populations quorum sensing systems, are probably a major force in microbial evolution and ecology.

DNA transfer by membrane vesicle.

DNA encapsulated by MVs. A rosette-like structure is seen in the centre, a plasmid is in the box, linear DNA molecules - arrowheads.

Membrane vesicles (MVs), from gram –ve bacteria can traffic toxins, signals and other proteins between bacteria. They have also been shown to be able to mediate the transfer of DNA between cells. E.coli 0157:H7 MVs were found to contain linear DNA, circular plasmids and rosette-like DNA structures, that included genes from chromosomal DNA as well as plasmid and phage. The MVs were capable of transforming related enteric bacteria and increasing their cytotoxicity. DNA transfer by membrane vesicles could be a more widespread phenomenon than is currently appreciated, however as yet it is more commonly reported as an aside from other MV studies.

Intercellular nanotubes.

top two images show B. subtilis cells with nanotubes (note more intimate thin connections in circle). Lower three images show inter-specific nanotubes.

A year ago Dubey and Ben-Yehuda showed the existence of tubular conduits forming between Bacillus subtilis cells. These nanotubes were shown to be able to mediate the exchange of proteins and non-conjugative plasmids. Nanotubes were also formed between B. subtilis and Staphylococcus aureus (both gram +ve) and a thinner variety were formed between either of the gram +ve species, and gram –ve E.coli. The authors suggest that the formation of ‘syncytium-like synergistic consortia’ mediated by nanotube connections underlies many of the traits displayed by biofilms.

These three phenomena have a tantalising savour, suggesting the depths of our ignorance of the complexity of microbial ecosystems and prokaryotic evolution. However, I imagine that progress in these fields will accelerate. The explosion of microbial and environmental sequencing will be useful in identifying the prevalence of GTAs. Understanding all six modes of LGT will be crucial to our appreciation of the ecology of natural microbial communities and of bacterial evolution, as well as having important application for human health.

See also: A novel gene transfer agent from Bartonella

Stanton, T. (2007). Prophage-like gene transfer agents—Novel mechanisms of gene exchange for Methanococcus, Desulfovibrio, Brachyspira, and Rhodobacter species Anaerobe, 13 (2), 43-49 DOI: 10.1016/j.anaerobe.2007.03.004

Lang, A., & Beatty, J. (2007). Importance of widespread gene transfer agent genes in α-proteobacteria Trends in Microbiology, 15 (2), 54-62 DOI: 10.1016/j.tim.2006.12.001

McDaniel, L., Young, E., Delaney, J., Ruhnau, F., Ritchie, K., & Paul, J. (2010). High Frequency of Horizontal Gene Transfer in the Oceans Science, 330 (6000), 50-50 DOI: 10.1126/science.1192243

Yaron, S., Kolling, G., Simon, L., & Matthews, K. (2000). Vesicle-Mediated Transfer of Virulence Genes from Escherichia coli O157:H7 to Other Enteric Bacteria Applied and Environmental Microbiology, 66 (10), 4414-4420 DOI: 10.1128/AEM.66.10.4414-4420.2000

Dubey, G., & Ben-Yehuda, S. (2011). Intercellular Nanotubes Mediate Bacterial Communication Cell, 144 (4), 590-600 DOI: 10.1016/j.cell.2011.01.015


One response to “Novel modes of lateral gene transfer in bacteria

  1. Pingback: News » Blog Archive » Editor’s Selections: Crowdsourcing enzyme design, gene transfer induced by pathogenic gut microbes, and novel mechanisms of lateral gene transfer in bacteria

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