Evolutionary convergence and divergence in archaeal chromosomal proteins and Chromo-like domains from bacteria and eukaryotes - PubMed (original) (raw)

Evolutionary convergence and divergence in archaeal chromosomal proteins and Chromo-like domains from bacteria and eukaryotes

Gurmeet Kaur et al. Sci Rep. 2018.

Abstract

SH3-fold-β-barrel domains of the chromo-like superfamily recognize epigenetic marks in eukaryotic proteins. Their provenance has been placed either in archaea, based on apparent structural similarity to chromatin-compacting Sul7d and Cren7 proteins, or in bacteria based on the presence of sequence homologs. Using sequence and structural evidence we establish that the archaeal Cren7/Sul7 proteins emerged from a zinc ribbon (ZnR) ancestor. Further, we show that the ancestral eukaryotic chromo-like domains evolved from bacterial versions, likely acquired from early endosymbioses, which already possessed an aromatic cage for recognition of modified amino-groups. These bacterial versions are part of a radiation of secreted SH3-fold domains, which spawned both chromo-like domains and classical SH3 domains in the context of peptide-recognition in the peptidoglycan or the extracellular matrix. This establishes that Cren7/Sul7 converged to a "SH3"-like state from a ZnR precursor via the loss of metal-chelation and acquisition of stronger hydrophobic interactions; it is unlikely to have participated in the evolution of the chromo-like domains. We show that archaea possess several Cren7/Sul7-related proteins with intact Zn-chelating ligands, which we predict to play previously unstudied roles in chromosome segregation during cell-division comparable to the PRC barrel and CdvA domain proteins.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1

Figure 1

Comparative structural view of the major secondary elements (A–I) and binding interfaces (J–M) in ZnRs, SH3s and Cren7. (A) Type-1A ZnR (PR domain-containing protein 11, PDB: 3RAY_A) (B) Type-1B zinc ribbon (Rubrerythrin, PDB: 1NNQ_A) (C) Type-2 zinc ribbon (Archaeal exosome RNA binding protein CSL4, PDB: 2BA1_A) (D) Type-2 zinc ribbon (Uncharacterized BCR cg1592, PDB: 2JNY_A) (E) ZnRs with three strands on each side (Anaerobic ribonucleoside-triphosphate reductase, PDB: 1H8K_A) (F) Type-2 zinc finger (Transcriptional Elongation Factor SII, PDB: 1TFI_A) (G) Cren7 (PDB: 3KXT_A) (H) Sso7 (PDB: 1C8C_A) (I) SH3-like fold (Tudor domain-containing protein 3, PDB: 3PNW_O). (J) DNA bound zinc ribbon domain (putative integrase [Bacteriophage A118], PDB: 4KIS_A) (K) DNA and peptide bound chromodomain (Male specific Lethal-3, PDB: 3OA6_A) (L) peptide bound SH3 domain (Tyrosine-protein kinase ABL1, PDB: 1BBZ_A) (M) DNA bound Cren7 (PDB: 3KXT_A). In all the panels, the Zn ion is represented by an orange sphere, side chains of zinc-chelating and other functionally-important amino acids are represented as sticks, bound peptides are yellow colored stick, the sugar-phosphate backbone of DNA is orange with nucleotides in green. Color scheme for (A–I): For type-2 zinc ribbons, the N-terminal β-hairpin is colored purple, the third β-strand is colored gray, the zinc knuckles are colored red and the C-terminal β-hairpin is colored yellow. The equivalent β-strands in type-2, -1A and -1B are colored alike. The Tudor domain is colored in a gradient of blue to red from the N- to the C-terminal. In panels (J–M): All β-strands are colored in blue, all loops in pink and α-helices in green.

Figure 2

Figure 2

Multiple sequence alignment (MSA) and domain architectures of Cren7 proteins. (A) Structure-based MSA of representative sequences of Sul7, Cren7, Cren7Znr and bona fide ZnRs. Accession number or the PDB identifier, and the alignment range are indicated for each sequence. For Sul7, Cren7 and Cren7Znr proteins, the organism names are also mentioned after the accession number/PDB. Zn-chelating residues are boxed in black and small amino acids (Gly, Pro) just after the Zn-binding ligands are colored in red. At positions with a 70% consensus, charged or polar residues are highlighted in blue, and hydrophobic, apolar and aliphatic residues are in yellow. Some insertions are not displayed for clarity, and the number of omitted residues is indicated. Regions of circular permutation in ZnRs are separated by a blue ‘|’ mark and the sequence numbers of the permuted ZnRs are shown in red. The consensus secondary structures are depicted above the alignment. (B) Domain architectures of Cren7 and Cren7Znr proteins. Representative sequence identifier with organism name are mention below individual architectures.

Figure 3

Figure 3

Multiple sequence alignment (MSA), probable phylogeny and domain architectures of chromo-like domains. (A) MSA of representative bacterial chromo-like domains. (B) Structure-based MSA of representative eukaryotic chromo-like domains. Coloring scheme for panel (A) and (B) follows Fig. 2(A). The amino acids at positions that are likely to be involved in forming the peptide-binding aromatic cage are highlighted in orange and marked with the asterisk above the MSA. (C) View of the peptide-binding aromatic cage of Arabidopsis Morf Related Gene (MRG) group protein MRG2 chromo domain (PDB: 4PL6). The aromatic cage is marked by a dashed ellipse and the aromatic residue positions from the N- to C- terminus are marked by numbers 1–5. (D) Probable phylogenetic relationships between the various chromo-like domains. (E) Domain architectures of bacterial chromo domains. Parallel architectures among bacterial chromo and bacterial SH3 domains are grouped at the bottom. SP indicates signal peptide. Besides the architectures shown in the figure, there are various other bacteria proteins with 2 to 14 tandem SH3 domains and 2 to 6 tandem chromo domains. (see Supplementary Material S3 for details).

Figure 4

Figure 4

Comparative graphical view of the conservation of aromatic residues at the five positions that make up the peptide-binding aromatic cage in chromo-like domains. Individual graphs are labelled on the top by the family they represent. The X-axis represents positions corresponding to those shown in Fig. 3(C). The Y-axis represents the fraction of aromatic amino acids (Y, W, F, H) at those positions in the respective families.

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