The conjugative DNA-transfer apparatus of Streptomyces

Thoma, Lina; Muth, Günther

doi:10.1016/j.ijmm.2014.12.020

Cited by 37 publications

(46 citation statements)

References 48 publications

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“…[28]. However, whereas conjugation in Clostridium depends on a T4SS-like system with TcpA serving as a coupling protein, TraB functions independently, allowing for transfer of traB -containing plasmids as small as 10 kbp [15], and also of chromosomal genes, although with lower efficiency. Interestingly, TraB transfers dsDNA [29], in contrast to the ssDNA-transfer mediated by classical T4SS-based conjugation systems.…”

Section: Discussionmentioning

confidence: 99%

“…The TraB protein also has a DNA recognition motif at its C-terminus which is responsible for identification of specific cis-acting locus of transfer ( clt ) sequences in the plasmid and, with lower frequency, in the chromosome. The conjugative plasmid also encodes a few Spd proteins which are required along with TraB for further intramycelial transfer across the septa, leading to rapid colonization of the whole mycelium [15]. …”

Section: Introductionmentioning

confidence: 99%

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The transjugation machinery of Thermus thermophilus: Identification of TdtA, an ATPase involved in DNA donation

et al. 2017

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In addition to natural competence, some Thermus thermophilus strains show a high rate of DNA transfer via direct cell-to-cell contact. The process is bidirectional and follows a two-step model where the donor cell actively pushes out DNA and the recipient cell employs the natural competence system to take up the DNA, in a hybrid transformation-dependent conjugation process (transjugation). While the DNA uptake machinery is well known as in other bacterial species that undergo transformation, the pushing step of transjugation remains to be characterized. Here we have searched for hypothetical DNA translocases putatively involved in the pushing step of transjugation. Among candidates encoded by T. thermophilus HB27, the TdtA protein was found to be required for DNA pushing but not for DNA pulling during transjugation, without affecting other cellular processes. Purified TdtA shows ATPase activity and oligomerizes as hexamers with a central opening that can accommodate double-stranded DNA. The tdtA gene was found to belong to a mobile 14 kbp-long DNA element inserted within the 3′ end of a tRNA gene, flanked by 47 bp direct repeats. The insertion also encoded a homolog of bacteriophage site-specific recombinases and actively self-excised from the chromosome at high frequency to form an apparently non-replicative circular form. The insertion also encoded a type II restriction endonuclease and a NurA-like nuclease, whose activities were required for efficient transjugation. All these data support that TdtA belongs to a new type of Integrative and Conjugative Element which promotes the generalized and efficient transfer of genetic traits that could facilitate its co-selection among bacterial populations.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The transjugation machinery of Thermus thermophilus: Identification of TdtA, an ATPase involved in DNA donation

et al. 2017

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“…The high frequency of genetic exchange implied by these studies may be because conjugal DNA transfer in streptomycetes is much more efficient than it is in most other bacteria, at least in the laboratory: instead of a complex type IV secretion apparatus transferring single-stranded DNA, streptomycetes employ the products of traB genes encoded by autonomous or chromosomally integrated plasmids to transfer double-stranded DNA 45 . TraB proteins belong to the FtsK/SpoIIIE family needed in many bacteria to complete the segregation of chromosomes into newly formed daughter cells, but, while FtsK/SpoIIIE proteins assemble in the nascent septum, TraB proteins assemble at growing hyphal tips.…”

Section: Ecology and Evolutionmentioning

confidence: 99%

“…TraB proteins belong to the FtsK/SpoIIIE family needed in many bacteria to complete the segregation of chromosomes into newly formed daughter cells, but, while FtsK/SpoIIIE proteins assemble in the nascent septum, TraB proteins assemble at growing hyphal tips. Transfer, which is ATP dependent, involves the interaction of TraB with short recognition sequences (consensus 5′-GACCCGGA-3′ in plasmid pSVH1): 25 clusters of four such sequences are also spaced along the chromosome of S. coelicolor , accounting for chromosome mobilisation 45 . Initial plasmid transfer is followed by the remarkable spread of the plasmid, sometimes throughout most of the recipient mycelium, in a process in which specialised Spd proteins assemble with TraB in the vegetative septa that occur roughly once every 10–20 μm 45, 46 ( Figure 2).…”

Section: Ecology and Evolutionmentioning

confidence: 99%

“…Transfer, which is ATP dependent, involves the interaction of TraB with short recognition sequences (consensus 5′-GACCCGGA-3′ in plasmid pSVH1): 25 clusters of four such sequences are also spaced along the chromosome of S. coelicolor , accounting for chromosome mobilisation 45 . Initial plasmid transfer is followed by the remarkable spread of the plasmid, sometimes throughout most of the recipient mycelium, in a process in which specialised Spd proteins assemble with TraB in the vegetative septa that occur roughly once every 10–20 μm 45, 46 ( Figure 2). The importance of TraB for plasmid spread (presumably providing the ATPase-driven motor function lacking from Spd proteins) was nicely demonstrated by showing that the presence of TraB in a recipient permitted efficient spreading following the occasional transfer of a traB -deleted plasmid 46 .…”

Section: Ecology and Evolutionmentioning

confidence: 99%

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Recent advances in understanding Streptomyces

2016

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About 2,500 papers dated 2014–2016 were recovered by searching the PubMed database for Streptomyces, which are the richest known source of antibiotics. This review integrates around 100 of these papers in sections dealing with evolution, ecology, pathogenicity, growth and development, stress responses and secondary metabolism, gene expression, and technical advances. Genomic approaches have greatly accelerated progress. For example, it has been definitively shown that interspecies recombination of conserved genes has occurred during evolution, in addition to exchanges of some of the tens of thousands of non-conserved accessory genes. The closeness of the association of Streptomyces with plants, fungi, and insects has become clear and is reflected in the importance of regulators of cellulose and chitin utilisation in overall Streptomyces biology. Interestingly, endogenous cellulose-like glycans are also proving important in hyphal growth and in the clumping that affects industrial fermentations. Nucleotide secondary messengers, including cyclic di-GMP, have been shown to provide key input into developmental processes such as germination and reproductive growth, while late morphological changes during sporulation involve control by phosphorylation. The discovery that nitric oxide is produced endogenously puts a new face on speculative models in which regulatory Wbl proteins (peculiar to actinobacteria) respond to nitric oxide produced in stressful physiological transitions. Some dramatic insights have come from a new model system for Streptomyces developmental biology, Streptomyces venezuelae, including molecular evidence of very close interplay in each of two pairs of regulatory proteins. An extra dimension has been added to the many complexities of the regulation of secondary metabolism by findings of regulatory crosstalk within and between pathways, and even between species, mediated by end products. Among many outcomes from the application of chromosome immunoprecipitation sequencing (ChIP-seq) analysis and other methods based on “next-generation sequencing” has been the finding that 21% of Streptomyces mRNA species lack leader sequences and conventional ribosome binding sites. Further technical advances now emerging should lead to continued acceleration of knowledge, and more effective exploitation, of these astonishing and critically important organisms.

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