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Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52.

Iyer LM, Koonin EV, Aravind L - BMC Genomics (2002)

Bottom Line: There are three evolutionarily distinct superfamilies of SSAPs, namely the RecT/Redbeta, ERF, and RAD52, that have different sequence conservation patterns and predicted folds.All these SSAPs appear to be primarily of bacteriophage origin and have been acquired by numerous phylogenetically distant cellular genomes.They generally occur in predicted operons encoding one or more of a set of conserved DNA recombination proteins that appear to be the principal functional partners of the SSAPs.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. lakshmin@ncbi.nlm.nih.gov

ABSTRACT

Background: The DNA single-strand annealing proteins (SSAPs), such as RecT, Redbeta, ERF and Rad52, function in RecA-dependent and RecA-independent DNA recombination pathways. Recently, they have been shown to form similar helical quaternary superstructures. However, despite the functional similarities between these diverse SSAPs, their actual evolutionary affinities are poorly understood.

Results: Using sensitive computational sequence analysis, we show that the RecT and Redbeta proteins, along with several other bacterial proteins, form a distinct superfamily. The ERF and Rad52 families show no direct evolutionary relationship to these proteins and define novel superfamilies of their own. We identify several previously unknown members of each of these superfamilies and also report, for the first time, bacterial and viral homologs of Rad52. Additionally, we predict the presence of aberrant HhH modules in RAD52 that are likely to be involved in DNA-binding. Using the contextual information obtained from the analysis of gene neighborhoods, we provide evidence of the interaction of the bacterial members of each of these SSAP superfamilies with a similar set of DNA repair/recombination protein. These include different nucleases or Holliday junction resolvases, the ABC ATPase SbcC and the single-strand-binding protein. We also present evidence of independent assembly of some of the predicted operons encoding SSAPs and in situ displacement of functionally similar genes.

Conclusions: There are three evolutionarily distinct superfamilies of SSAPs, namely the RecT/Redbeta, ERF, and RAD52, that have different sequence conservation patterns and predicted folds. All these SSAPs appear to be primarily of bacteriophage origin and have been acquired by numerous phylogenetically distant cellular genomes. They generally occur in predicted operons encoding one or more of a set of conserved DNA recombination proteins that appear to be the principal functional partners of the SSAPs.

No MeSH data available.


Related in: MedlinePlus

Maximum likelihood tree for the RecT/Redβ superfamily of proteins. The internal branches with RELL bootstrap support >70% are indicated by blue circles. Proteins are designated by their gene names and species abbreviations as in Fig. 1. The gene neighborhoods of the RecT/Redβ superfamily genes are shown in association with the corresponding branches whenever they they contained genes for proteins with plausible functional connections with SSAPs. The hatched boxes represent fragments of ERF (Indicated by E) and SSB (indicated by S) genes encoding C-terminal regions as described in the text. Gene abbreviations are as follows: GP46: GP46 of bacteriophage PSA, GP32:GP32 of bacteriophage PSA, ORF15:ORF15 of Streptococcus thermophilus bacteriophage 7201, ORF40: ORF40 of bacteriophage PVL ORF86:ORF86 of Staphylococcus aureus temperate phage φSLT, Orf100a:0rf100a of Staphylococcus aureus temperate phage φSLT, ORF364: ORF364 of bacteriophage φ31.1, Ec2360: b2360 of E. coli, AcylTr: N-Acyltransferase, Bro: Bro-N domain fused to XF0704, Met: DNA Methyltransferase
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Figure 2: Maximum likelihood tree for the RecT/Redβ superfamily of proteins. The internal branches with RELL bootstrap support >70% are indicated by blue circles. Proteins are designated by their gene names and species abbreviations as in Fig. 1. The gene neighborhoods of the RecT/Redβ superfamily genes are shown in association with the corresponding branches whenever they they contained genes for proteins with plausible functional connections with SSAPs. The hatched boxes represent fragments of ERF (Indicated by E) and SSB (indicated by S) genes encoding C-terminal regions as described in the text. Gene abbreviations are as follows: GP46: GP46 of bacteriophage PSA, GP32:GP32 of bacteriophage PSA, ORF15:ORF15 of Streptococcus thermophilus bacteriophage 7201, ORF40: ORF40 of bacteriophage PVL ORF86:ORF86 of Staphylococcus aureus temperate phage φSLT, Orf100a:0rf100a of Staphylococcus aureus temperate phage φSLT, ORF364: ORF364 of bacteriophage φ31.1, Ec2360: b2360 of E. coli, AcylTr: N-Acyltransferase, Bro: Bro-N domain fused to XF0704, Met: DNA Methyltransferase

Mentions: Phylogenetic analyses of the RecT/Redβ superfamily using the least squares and maximum likelihood methods distinguished three distinct groups, namely the RecT-like, the Redβ-like and the EHAP1-like families (Fig. 2). Previously, the RecT proteins have been known from very few bacteria and Redβ has only been detected in λ and closely related phages. However, we showed that the Redβ family is widespread in bacteria, such as Borrelia hermsii, Xylella, Ureaplasma, Listeria, Streptococcus pyogenes, Mesorhizobium loti. The RecT family is predominantly seen in the low-GC Gram-positive bacteria, such as Bacillus, Streptococcus, Lactococcus and Listeria, and their phages (Fig. 2). E. coli and Legionella pneumophila are the only two γ-proteobacteria that possess this protein, suggesting that they might have acquired RecT via a relatively recent horizontal transfer from Gram-positive bacteria. The sporadic distribution of the RecT and Redβ family proteins in bacterial genomes and their presence in phages suggest that these proteins ultimately are of phage origin and have been co-opted by the bacterial DNA recombination/repair systems. Consistent with this, practically all the bacterial members of these families appear to belong to prophages or their remnants, as they are mostly in the neighborhood of what appear to be clearly phage-derived genes. The EHAP1-like family is extremely divergent and represented thus far only in E. coli and the closely related Salmonella. Practically all members of the RecT/Redβ superfamily are single-domain proteins showing extended similarity to each other throughout their globular regions. The only exceptions are the E. coli EHAP1 and the PF161 protein encoded in the Borrelia hermsii circular plasmid, which are fused to C-terminal fragments of the ERF protein (see below).


Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52.

Iyer LM, Koonin EV, Aravind L - BMC Genomics (2002)

Maximum likelihood tree for the RecT/Redβ superfamily of proteins. The internal branches with RELL bootstrap support >70% are indicated by blue circles. Proteins are designated by their gene names and species abbreviations as in Fig. 1. The gene neighborhoods of the RecT/Redβ superfamily genes are shown in association with the corresponding branches whenever they they contained genes for proteins with plausible functional connections with SSAPs. The hatched boxes represent fragments of ERF (Indicated by E) and SSB (indicated by S) genes encoding C-terminal regions as described in the text. Gene abbreviations are as follows: GP46: GP46 of bacteriophage PSA, GP32:GP32 of bacteriophage PSA, ORF15:ORF15 of Streptococcus thermophilus bacteriophage 7201, ORF40: ORF40 of bacteriophage PVL ORF86:ORF86 of Staphylococcus aureus temperate phage φSLT, Orf100a:0rf100a of Staphylococcus aureus temperate phage φSLT, ORF364: ORF364 of bacteriophage φ31.1, Ec2360: b2360 of E. coli, AcylTr: N-Acyltransferase, Bro: Bro-N domain fused to XF0704, Met: DNA Methyltransferase
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Related In: Results  -  Collection

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Figure 2: Maximum likelihood tree for the RecT/Redβ superfamily of proteins. The internal branches with RELL bootstrap support >70% are indicated by blue circles. Proteins are designated by their gene names and species abbreviations as in Fig. 1. The gene neighborhoods of the RecT/Redβ superfamily genes are shown in association with the corresponding branches whenever they they contained genes for proteins with plausible functional connections with SSAPs. The hatched boxes represent fragments of ERF (Indicated by E) and SSB (indicated by S) genes encoding C-terminal regions as described in the text. Gene abbreviations are as follows: GP46: GP46 of bacteriophage PSA, GP32:GP32 of bacteriophage PSA, ORF15:ORF15 of Streptococcus thermophilus bacteriophage 7201, ORF40: ORF40 of bacteriophage PVL ORF86:ORF86 of Staphylococcus aureus temperate phage φSLT, Orf100a:0rf100a of Staphylococcus aureus temperate phage φSLT, ORF364: ORF364 of bacteriophage φ31.1, Ec2360: b2360 of E. coli, AcylTr: N-Acyltransferase, Bro: Bro-N domain fused to XF0704, Met: DNA Methyltransferase
Mentions: Phylogenetic analyses of the RecT/Redβ superfamily using the least squares and maximum likelihood methods distinguished three distinct groups, namely the RecT-like, the Redβ-like and the EHAP1-like families (Fig. 2). Previously, the RecT proteins have been known from very few bacteria and Redβ has only been detected in λ and closely related phages. However, we showed that the Redβ family is widespread in bacteria, such as Borrelia hermsii, Xylella, Ureaplasma, Listeria, Streptococcus pyogenes, Mesorhizobium loti. The RecT family is predominantly seen in the low-GC Gram-positive bacteria, such as Bacillus, Streptococcus, Lactococcus and Listeria, and their phages (Fig. 2). E. coli and Legionella pneumophila are the only two γ-proteobacteria that possess this protein, suggesting that they might have acquired RecT via a relatively recent horizontal transfer from Gram-positive bacteria. The sporadic distribution of the RecT and Redβ family proteins in bacterial genomes and their presence in phages suggest that these proteins ultimately are of phage origin and have been co-opted by the bacterial DNA recombination/repair systems. Consistent with this, practically all the bacterial members of these families appear to belong to prophages or their remnants, as they are mostly in the neighborhood of what appear to be clearly phage-derived genes. The EHAP1-like family is extremely divergent and represented thus far only in E. coli and the closely related Salmonella. Practically all members of the RecT/Redβ superfamily are single-domain proteins showing extended similarity to each other throughout their globular regions. The only exceptions are the E. coli EHAP1 and the PF161 protein encoded in the Borrelia hermsii circular plasmid, which are fused to C-terminal fragments of the ERF protein (see below).

Bottom Line: There are three evolutionarily distinct superfamilies of SSAPs, namely the RecT/Redbeta, ERF, and RAD52, that have different sequence conservation patterns and predicted folds.All these SSAPs appear to be primarily of bacteriophage origin and have been acquired by numerous phylogenetically distant cellular genomes.They generally occur in predicted operons encoding one or more of a set of conserved DNA recombination proteins that appear to be the principal functional partners of the SSAPs.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. lakshmin@ncbi.nlm.nih.gov

ABSTRACT

Background: The DNA single-strand annealing proteins (SSAPs), such as RecT, Redbeta, ERF and Rad52, function in RecA-dependent and RecA-independent DNA recombination pathways. Recently, they have been shown to form similar helical quaternary superstructures. However, despite the functional similarities between these diverse SSAPs, their actual evolutionary affinities are poorly understood.

Results: Using sensitive computational sequence analysis, we show that the RecT and Redbeta proteins, along with several other bacterial proteins, form a distinct superfamily. The ERF and Rad52 families show no direct evolutionary relationship to these proteins and define novel superfamilies of their own. We identify several previously unknown members of each of these superfamilies and also report, for the first time, bacterial and viral homologs of Rad52. Additionally, we predict the presence of aberrant HhH modules in RAD52 that are likely to be involved in DNA-binding. Using the contextual information obtained from the analysis of gene neighborhoods, we provide evidence of the interaction of the bacterial members of each of these SSAP superfamilies with a similar set of DNA repair/recombination protein. These include different nucleases or Holliday junction resolvases, the ABC ATPase SbcC and the single-strand-binding protein. We also present evidence of independent assembly of some of the predicted operons encoding SSAPs and in situ displacement of functionally similar genes.

Conclusions: There are three evolutionarily distinct superfamilies of SSAPs, namely the RecT/Redbeta, ERF, and RAD52, that have different sequence conservation patterns and predicted folds. All these SSAPs appear to be primarily of bacteriophage origin and have been acquired by numerous phylogenetically distant cellular genomes. They generally occur in predicted operons encoding one or more of a set of conserved DNA recombination proteins that appear to be the principal functional partners of the SSAPs.

No MeSH data available.


Related in: MedlinePlus