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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

Multiple sequence alignment of the ERF protein superfamily. The coloring reflects the amino acid conservation at 85% consensus. The coloring scheme and secondary structure assignment abbreviations are as in Fig. 1. Species abbreviations are as follows: Bbcp32-4: Borrelia burgdorferi cicular plasmid (cp) 32-4, Bbcp32-7: B. burgdorferi cp 32-7, Bbcp32-8: B. burgdorferi cp 32-8, Bbcp8.3: B. burgdorferi cp 8.3, Bbcp9: B burgdorferi cp 9, bIL67: bacteriophage IL67, c2: Lactococcus phage c2, D3: Pseudomonas phage D3, HK97: bacteriophage HK97, Lj771: Lactobacillus johnsonii prophage Lj771, Lm: Listeria monocytogenes, MM1: Streptococcus pneumoniae bacteriophage MM1, BPmv4: Bacteriophage mv4, P22: Bacteriophage P22, phiPV83: Bacteriophage φPV83, phiSLT: Staphylococcus aureus temperate phage φSLT, ST7201: Streptococcus thermophilus bacteriophage 7201, Unk: Unknown.
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Figure 3: Multiple sequence alignment of the ERF protein superfamily. The coloring reflects the amino acid conservation at 85% consensus. The coloring scheme and secondary structure assignment abbreviations are as in Fig. 1. Species abbreviations are as follows: Bbcp32-4: Borrelia burgdorferi cicular plasmid (cp) 32-4, Bbcp32-7: B. burgdorferi cp 32-7, Bbcp32-8: B. burgdorferi cp 32-8, Bbcp8.3: B. burgdorferi cp 8.3, Bbcp9: B burgdorferi cp 9, bIL67: bacteriophage IL67, c2: Lactococcus phage c2, D3: Pseudomonas phage D3, HK97: bacteriophage HK97, Lj771: Lactobacillus johnsonii prophage Lj771, Lm: Listeria monocytogenes, MM1: Streptococcus pneumoniae bacteriophage MM1, BPmv4: Bacteriophage mv4, P22: Bacteriophage P22, phiPV83: Bacteriophage φPV83, phiSLT: Staphylococcus aureus temperate phage φSLT, ST7201: Streptococcus thermophilus bacteriophage 7201, Unk: Unknown.

Mentions: The ERF protein of phage P22 is involved in the circularization of the linear dsDNA phage genome upon entry into the host cell [21-23]. Experimental studies have shown that, mutations in ERF are complemented by Redβ and that in vitro ERF adopts quaternary structures analogous to those of Redβ and RecT [14,17,24,25]. However, in the comprehensive analysis of the RecT/Redβ superfamily no statistically significant similarity could be detected between these proteins and the ERF proteins. To explore the evolutionary affinities of the ERF domains, we carried out a sequence profile analysis as described above for the RecT case using transitive PSI-BLAST analysis. As a result of these searches, homologs of ERF encoded in several bacterial and phage genomes from diverse taxa were identified. The alignments generated in these searches consistently pointed to a region of approximately 150 amino acids that is conserved in all these proteins, with a characteristic motif of the form: GuXXoYhp + YXhXXhh (where G is glycine, Y-tyrosine, u is a tiny residue, h-hydrophobic, p is a polar residue, o is an alcohol residue, + is a basic residue, and X is any residue; Fig. 3). This suggested that ERF was the prototype of a family of conserved bacterial domains.


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

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

Multiple sequence alignment of the ERF protein superfamily. The coloring reflects the amino acid conservation at 85% consensus. The coloring scheme and secondary structure assignment abbreviations are as in Fig. 1. Species abbreviations are as follows: Bbcp32-4: Borrelia burgdorferi cicular plasmid (cp) 32-4, Bbcp32-7: B. burgdorferi cp 32-7, Bbcp32-8: B. burgdorferi cp 32-8, Bbcp8.3: B. burgdorferi cp 8.3, Bbcp9: B burgdorferi cp 9, bIL67: bacteriophage IL67, c2: Lactococcus phage c2, D3: Pseudomonas phage D3, HK97: bacteriophage HK97, Lj771: Lactobacillus johnsonii prophage Lj771, Lm: Listeria monocytogenes, MM1: Streptococcus pneumoniae bacteriophage MM1, BPmv4: Bacteriophage mv4, P22: Bacteriophage P22, phiPV83: Bacteriophage φPV83, phiSLT: Staphylococcus aureus temperate phage φSLT, ST7201: Streptococcus thermophilus bacteriophage 7201, Unk: Unknown.
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Figure 3: Multiple sequence alignment of the ERF protein superfamily. The coloring reflects the amino acid conservation at 85% consensus. The coloring scheme and secondary structure assignment abbreviations are as in Fig. 1. Species abbreviations are as follows: Bbcp32-4: Borrelia burgdorferi cicular plasmid (cp) 32-4, Bbcp32-7: B. burgdorferi cp 32-7, Bbcp32-8: B. burgdorferi cp 32-8, Bbcp8.3: B. burgdorferi cp 8.3, Bbcp9: B burgdorferi cp 9, bIL67: bacteriophage IL67, c2: Lactococcus phage c2, D3: Pseudomonas phage D3, HK97: bacteriophage HK97, Lj771: Lactobacillus johnsonii prophage Lj771, Lm: Listeria monocytogenes, MM1: Streptococcus pneumoniae bacteriophage MM1, BPmv4: Bacteriophage mv4, P22: Bacteriophage P22, phiPV83: Bacteriophage φPV83, phiSLT: Staphylococcus aureus temperate phage φSLT, ST7201: Streptococcus thermophilus bacteriophage 7201, Unk: Unknown.
Mentions: The ERF protein of phage P22 is involved in the circularization of the linear dsDNA phage genome upon entry into the host cell [21-23]. Experimental studies have shown that, mutations in ERF are complemented by Redβ and that in vitro ERF adopts quaternary structures analogous to those of Redβ and RecT [14,17,24,25]. However, in the comprehensive analysis of the RecT/Redβ superfamily no statistically significant similarity could be detected between these proteins and the ERF proteins. To explore the evolutionary affinities of the ERF domains, we carried out a sequence profile analysis as described above for the RecT case using transitive PSI-BLAST analysis. As a result of these searches, homologs of ERF encoded in several bacterial and phage genomes from diverse taxa were identified. The alignments generated in these searches consistently pointed to a region of approximately 150 amino acids that is conserved in all these proteins, with a characteristic motif of the form: GuXXoYhp + YXhXXhh (where G is glycine, Y-tyrosine, u is a tiny residue, h-hydrophobic, p is a polar residue, o is an alcohol residue, + is a basic residue, and X is any residue; Fig. 3). This suggested that ERF was the prototype of a family of conserved bacterial domains.

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