Mechanisms of stabilization of integrative and conjugative elements

Burrus, Vincent

doi:10.1016/j.mib.2017.03.014

Cited by 59 publications

(37 citation statements)

References 52 publications

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“…According to this assumption, if the cell division occurs while the element is excised, the element would inevitably be lost in one of the daughter cells. Recent evidences on various models have now clearly demonstrated that ICEs use multiple strategies to ensure the transient maintenance of the excised element in the daughter cells and/or to leverage maintenance in cell populations (for a review see [ 20 ]). Even though the strategies used by IMEs to maintain as an extra-chromosomal form have not been described yet, the gene content of various IMEs and experimental data obtained for the IME SGI1 suggest that at least some of them use strategies that are similar to those of ICEs.…”

Section: Maintenance Of Imesmentioning

confidence: 99%

“…The MobT-encoding ICEs encode a non-canonical CP, related to the one of the plasmid pCW3 from the Firmicute Clostridium perfringens [ 18 , 19 ] and more distantly related to FtsK, or the TraB protein involved in dsDNA conjugative systems from Actinobacteria [ 14 , 17 ]. Although the maintenance of ICE is essentially based on their integrated form, recent data suggest that their replication as a circular form has a significant role in their maintenance (for reviews, see [ 12 , 20 , 21 ]). Like all other bacterial MGEs [ 22 ], ICEs have a modular structure, i.e., the genes involved in the same biological function (such as conjugation or integration/excision) are physically linked in a module [ 12 , 23 ].…”

Section: Introductionmentioning

confidence: 99%

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The Obscure World of Integrative and Mobilizable Elements, Highly Widespread Elements that Pirate Bacterial Conjugative Systems

Guédon

Libante

Coluzzi

et al. 2017

Genes

105

112

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Conjugation is a key mechanism of bacterial evolution that involves mobile genetic elements. Recent findings indicated that the main actors of conjugative transfer are not the well-known conjugative or mobilizable plasmids but are the integrated elements. This paper reviews current knowledge on “integrative and mobilizable elements” (IMEs) that have recently been shown to be highly diverse and highly widespread but are still rarely described. IMEs encode their own excision and integration and use the conjugation machinery of unrelated co-resident conjugative element for their own transfer. Recent studies revealed a much more complex and much more diverse lifecycle than initially thought. Besides their main transmission as integrated elements, IMEs probably use plasmid-like strategies to ensure their maintenance after excision. Their interaction with conjugative elements reveals not only harmless hitchhikers but also hunters that use conjugative elements as target for their integration or harmful parasites that subvert the conjugative apparatus of incoming elements to invade cells that harbor them. IMEs carry genes conferring various functions, such as resistance to antibiotics, that can enhance the fitness of their hosts and that contribute to their maintenance in bacterial populations. Taken as a whole, IMEs are probably major contributors to bacterial evolution.

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Section: Maintenance Of Imesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Obscure World of Integrative and Mobilizable Elements, Highly Widespread Elements that Pirate Bacterial Conjugative Systems

Guédon

Libante

Coluzzi

et al. 2017

Genes

105

112

View full text Add to dashboard Cite

show abstract

“…Recent studies have shown that integrative and conjugal elements should now be included in this group because their DTR modules also initiate vegetative RC replication. Moreover, this ability is likely to be a characteristic of ICEs ( Burrus, 2017 ), which redefines the properties of this group of MGEs.…”

Section: Discussionmentioning

confidence: 99%

The Different Faces of Rolling-Circle Replication and Its Multifunctional Initiator Proteins

2017

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Horizontal gene transfer (HGT) contributes greatly to the plasticity and evolution of prokaryotic and eukaryotic genomes. The main carriers of foreign DNA in HGT are mobile genetic elements (MGEs) that have extremely diverse genetic structures and properties. Various strategies are used for the maintenance and spread of MGEs, including (i) vegetative replication, (ii) transposition (and other types of recombination), and (iii) conjugal transfer. In many MGEs, all of these processes are dependent on rolling-circle replication (RCR). RCR is one of the most well characterized models of DNA replication. Although many studies have focused on describing its mechanism, the role of replication initiator proteins has only recently been subject to in-depth analysis, which indicates their involvement in multiple biological process associated with RCR. In this review, we present a general overview of RCR and its impact in HGT. We focus on the molecular characteristics of RCR initiator proteins belonging to the HUH and Rep_trans protein families. Despite analogous mechanisms of action these are distinct groups of proteins with different catalytic domain structures. This is the first review describing the multifunctional character of various types of RCR initiator proteins, including the latest discoveries in the field. Recent reports provide evidence that (i) proteins initiating vegetative replication (Rep) or mobilization for conjugal transfer (Mob) may also have integrase (Int) activity, (ii) some Mob proteins are capable of initiating vegetative replication (Rep activity), and (iii) some Rep proteins can act like Mob proteins to mobilize plasmid DNA for conjugal transfer. These findings have significant consequences for our understanding of the role of RCR, not only in DNA metabolism but also in the biology of many MGEs.

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“…However, in the absence of such active stabilization modules, spurious excision of ICEs from their host chromosomes may lead to their loss (Burrus, 2017). Therefore, any mechanisms that can reduce or prevent spurious excision likely stabilize ICEs in the long term.…”

Section: Passive Stabilizationmentioning

confidence: 99%

Evolutionary persistence of tripartite integrative and conjugative elements

Haskett

Ramsay

Bekuma

et al. 2017

Plasmid

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Integrative and conjugative elements (ICEs) are generally regarded as regions of contiguous DNA integrated within a bacterial genome that are capable of excision and horizontal transfer via conjugation. We recently characterized a unique group of ICEs present in Mesorhizobium spp., which exist as three entirely separate but inextricably linked chromosomal regions termed α, β and γ. These regions occupy three different recombinase attachment (att) sites; however, they do not excise independently. Rather, they recombine the host chromosome to form a single contiguous region prior to excision and conjugative transfer. Like the single-part ICE carried by M. loti R7A (ICEMlSym), these "tripartite" ICEs (ICEs) are widespread throughout the Mesorhizobium genus and enable strains to form nitrogen-fixing symbioses with a variety of legumes. ICEs have likely evolved following recombination between three separate ancestral integrative elements, however, the persistence of ICE structure in diverse mesorhizobia is perplexing due to its seemingly unnecessary complexity. In this study, examination of ICEs revealed that most symbiosis genes are carried on the large α fragment. Some ICE-β and γ regions also carry genes that potentially contribute to the symbiosis, or to persistence in the soil environment, but these regions have been frequently subjected to recombination events including deletions, insertions and recombination with genes located on other integrative elements. Examination of a new ICE in M. ciceri Ca181 revealed it has jettisoned the genetic cargo from its β region and recruited a serine recombinase gene within its γ region, resulting in replacement of one of the three ICE integration sites. Overall the recombination loci appear to be the only conserved features of the β and γ regions, suggesting that the tripartite structure itself provides a selective benefit to the element. We propose the ICE structure provides enhanced host range, host stability and resistance to destabilization by tandem insertion of competing integrative elements. Furthermore, we suspect the ICE tripartite structure increases the likelihood of gene capture from integrative elements sharing the same attachment sites.

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Mechanisms of stabilization of integrative and conjugative elements

Cited by 59 publications

References 52 publications

The Obscure World of Integrative and Mobilizable Elements, Highly Widespread Elements that Pirate Bacterial Conjugative Systems

The Obscure World of Integrative and Mobilizable Elements, Highly Widespread Elements that Pirate Bacterial Conjugative Systems

The Different Faces of Rolling-Circle Replication and Its Multifunctional Initiator Proteins

Evolutionary persistence of tripartite integrative and conjugative elements

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