D-family DNA polymerase - DP2 subunit

Julia Borys '21 and Sam Schaffner '21


Contents:


I. Introduction

DNA polymerases (DNAPs) have evolved across all life forms in order to perform highly accurate and processive replication of the genome, repair of DNA, and resolution of Okazaki fragments. DNA polymerase D (PolD) is an atypical class of DNA polymerases found in archaea. PolD initiates DNA synthesis for both the leading and lagging strands in all archaea with the exception of Crenarchaea. PolD contains two subunits: a proofreading exonuclease subunit (DP1) and a polymerase catalytic subunit (DP2), shown here from hyperthermophilic archaea species Pyrococcus abyssi. The active site of DP2 shows surprising structural similarity to the “two-double-psi ß-barrel” (DPBB) family of RNAPs, suggesting a complex evolutionary history to the archaeal DNA polymerase.


II. Structure of DP2

The polymerase catalytic DP2 subunit of PolD is made of the N-terminal domain, the central domain, the catalytic domain, and part of the C-terminal domain. There is substantial interaction between the N-terminal domain and the catalytic domain that forms the DNAP active site surrounded by two double-psi ß-barrels (DPBBs). The N-terminal domain has a 45-residue long N-terminal extension named the , which interacts with the catalytic domain (ß33). The N-terminal self-assembly region has a long that makes the most connections with the catalytic domain and a short . The interactions between the N-terminal domain and catalytic domain include , contacts between hydrophobic residues, and secondary structure interactions between ß1 and ß33.

The DP2 subunit contains two domains that sit on either side of the protein’s . This loop is solvent-exposed and located within a crevice that is 55 angstroms long and 25 angstroms wide, which is suited for a 1.5 helical turn of B-DNA.

The putative DNA binding region is located in the catalytic domain between two zinc-modules, Other than the tetrahedral coordination of the Zn2+ ions by two pairs of cysteines, the modules have separate structures.


III. DPBB Architecture

is located in the central domain. The crystallized structure for DPBB only shows 5 of the 6 expected beta-strands, but the missing strand is expected to be located in the stretch of 17 missing residues. The central domain also contains a seven-stranded antiparallel ß-sheet (ß10-12 and ß14-17) that is wrapped by six alpha-helices (alpha13-14 and alpha19-22).

The catalytic domain has a central six-stranded . The most conserved sequence motif of the DP2 is the right-handed alpha-helix and a 10-residue long loop that connects the fifth (ß31) and sixth (ß32) ß-strands. This motif contains the catalytically critical aspartic residues (also named D961 and D963 in reference to the literature).


IV. Structural Relationship to Other RNAPs

The unique two DPBB motif structure of DP2 is not structurally similar to any other known DNAPs. However, the two DPBB structure shares unexpected homology to the ‘two-barrel’ family of RNAP. DBPP-A of multi-subunit RNAP chelate catalytic Mg2+ with a DFDGDE signature. The two invariant aspartic residues on DBPP-2 (D956 and D958) are aligned with three catalytic aspartic residues in RNAP (see figure below). DBPP-B of RNAP contains two lysine residues for DNA binding. Unfortunately, the corresponding residues for PolD are found in a stretch of missing residues.

 


VI. References

Raia P, Carroni M, Henry E, Pehau-Arnaudet G, Brûlé S, Béguin P, et al. (2019). Structure of the DP1–DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases. PLoS Biol 17 (1), 3000122.

Sauguet L, Raia P, Henneke G et al. (2016). Shared active site architecture between archaeal PolD and multi-subunit RNA polymerases revealed by X-ray crystallography. Nat Commun 7, 12227.

Shen Y et al. (2001). Invariant Asp-1122 and Asp-1124 are essential residues for polymerization catalysis of family D DNA polymerase from Pyrococcus horikoshii. J. Biol. Chem. 276, 27376–27383.

Werner F, Grohmann D. (2011). Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9, 85–98.

Amino Acid Color Key

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