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The lambda red proteins promote efficient recombination between diverged sequences: implications for bacteriophage genome mosaicism.

Martinsohn JT, Radman M, Petit MA - PLoS Genet. (2008)

Bottom Line: However, the precise molecular processes underlying this mosaicism are unknown.To test this, we have measured the efficiency of homeologous recombination between diverged oxa gene pairs inserted into lambda.The recombination editing proteins, MutS and UvrD, showed only marginal effects on lambda recombination.

View Article: PubMed Central - PubMed

Affiliation: Faculté de Médecine R. Descartes, INSERM U571, Université Paris Descartes, Paris, France.

ABSTRACT
Genome mosaicism in temperate bacterial viruses (bacteriophages) is so great that it obscures their phylogeny at the genome level. However, the precise molecular processes underlying this mosaicism are unknown. Illegitimate recombination has been proposed, but homeologous recombination could also be at play. To test this, we have measured the efficiency of homeologous recombination between diverged oxa gene pairs inserted into lambda. High yields of recombinants between 22% diverged genes have been obtained when the virus Red Gam pathway was active, and 100 fold less when the host Escherichia coli RecABCD pathway was active. The recombination editing proteins, MutS and UvrD, showed only marginal effects on lambda recombination. Thus, escape from host editing contributes to the high proficiency of virus recombination. Moreover, our bioinformatics study suggests that homeologous recombination between similar lambdoid viruses has created part of their mosaicism. We therefore propose that the remarkable propensity of the lambda-encoded Red and Gam proteins to recombine diverged DNA is effectively contributing to mosaicism, and more generally, that a correlation may exist between virus genome mosaicism and the presence of Red/Gam-like systems.

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Evolutionary history of event between diverged viruses A and B, produces virus C which is similar to A but for a patch of DNA (hit) coming from B.Alignment of phage B to C reveals at the border of the patch two regions of intermediate similarity (shoulders, here drawn in grey). Below is shown the % identity profile of the B to C virus alignment.
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pgen-1000065-g005: Evolutionary history of event between diverged viruses A and B, produces virus C which is similar to A but for a patch of DNA (hit) coming from B.Alignment of phage B to C reveals at the border of the patch two regions of intermediate similarity (shoulders, here drawn in grey). Below is shown the % identity profile of the B to C virus alignment.

Mentions: To explore the potential role of homeologous recombination in the evolution of virus genomes, we looked for hallmarks of such events by a comparative bioinformatics analysis of a variety of lambdoid phage genomes. Consider ancestral viruses A and B sharing overall 60% identity except for two 80% identical segments (I, in Figure 5). Homeologous recombination within the 80% identity segments would give rise to phage C consisting of the A sequence with a patch of B. If so, one would expect to find, in the virus C to B alignment, two regions of 80% identity, called hereafter “shoulders”, flanking a patch of 100% identity, called “hit” (II, in Figure 5). Subsequent divergence between ancestral phages B and C would finally lead to 90% identical hits, flanked by 70% shoulders, over a background of 50% identical sequences (III, in Figure 5).


The lambda red proteins promote efficient recombination between diverged sequences: implications for bacteriophage genome mosaicism.

Martinsohn JT, Radman M, Petit MA - PLoS Genet. (2008)

Evolutionary history of event between diverged viruses A and B, produces virus C which is similar to A but for a patch of DNA (hit) coming from B.Alignment of phage B to C reveals at the border of the patch two regions of intermediate similarity (shoulders, here drawn in grey). Below is shown the % identity profile of the B to C virus alignment.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2327257&req=5

pgen-1000065-g005: Evolutionary history of event between diverged viruses A and B, produces virus C which is similar to A but for a patch of DNA (hit) coming from B.Alignment of phage B to C reveals at the border of the patch two regions of intermediate similarity (shoulders, here drawn in grey). Below is shown the % identity profile of the B to C virus alignment.
Mentions: To explore the potential role of homeologous recombination in the evolution of virus genomes, we looked for hallmarks of such events by a comparative bioinformatics analysis of a variety of lambdoid phage genomes. Consider ancestral viruses A and B sharing overall 60% identity except for two 80% identical segments (I, in Figure 5). Homeologous recombination within the 80% identity segments would give rise to phage C consisting of the A sequence with a patch of B. If so, one would expect to find, in the virus C to B alignment, two regions of 80% identity, called hereafter “shoulders”, flanking a patch of 100% identity, called “hit” (II, in Figure 5). Subsequent divergence between ancestral phages B and C would finally lead to 90% identical hits, flanked by 70% shoulders, over a background of 50% identical sequences (III, in Figure 5).

Bottom Line: However, the precise molecular processes underlying this mosaicism are unknown.To test this, we have measured the efficiency of homeologous recombination between diverged oxa gene pairs inserted into lambda.The recombination editing proteins, MutS and UvrD, showed only marginal effects on lambda recombination.

View Article: PubMed Central - PubMed

Affiliation: Faculté de Médecine R. Descartes, INSERM U571, Université Paris Descartes, Paris, France.

ABSTRACT
Genome mosaicism in temperate bacterial viruses (bacteriophages) is so great that it obscures their phylogeny at the genome level. However, the precise molecular processes underlying this mosaicism are unknown. Illegitimate recombination has been proposed, but homeologous recombination could also be at play. To test this, we have measured the efficiency of homeologous recombination between diverged oxa gene pairs inserted into lambda. High yields of recombinants between 22% diverged genes have been obtained when the virus Red Gam pathway was active, and 100 fold less when the host Escherichia coli RecABCD pathway was active. The recombination editing proteins, MutS and UvrD, showed only marginal effects on lambda recombination. Thus, escape from host editing contributes to the high proficiency of virus recombination. Moreover, our bioinformatics study suggests that homeologous recombination between similar lambdoid viruses has created part of their mosaicism. We therefore propose that the remarkable propensity of the lambda-encoded Red and Gam proteins to recombine diverged DNA is effectively contributing to mosaicism, and more generally, that a correlation may exist between virus genome mosaicism and the presence of Red/Gam-like systems.

Show MeSH
Related in: MedlinePlus