The PRC-barrel: a widespread, conserved domain shared by photosynthetic reaction center subunits and proteins of RNA metabolism

Abstract

Background: The H subunit of the purple bacterial photosynthetic reaction center (PRC-H) is important for the assembly of the photosynthetic reaction center and appears to regulate electron transfer during the reduction of the secondary quinone. It contains a distinct cytoplasmic beta-barrel domain whose fold has no close structural relationship to any other well known beta-barrel domain.

Results: We show that the PRC-H beta-barrel domain is the prototype of a novel superfamily of protein domains, the PRC-barrels, approximately 80 residues long, which is widely represented in bacteria, archaea and plants. This domain is also present at the carboxyl terminus of the pan-bacterial protein RimM, which is involved in ribosomal maturation and processing of 16S rRNA. A family of small proteins conserved in all known euryarchaea are composed entirely of a single stand-alone copy of the domain. Versions of this domain from photosynthetic proteobacteria contain a conserved acidic residue that is thought to regulate the reduction of quinones in the light-induced electron-transfer reaction. Closely related forms containing this acidic residue are also found in several non-photosynthetic bacteria, as well as in cyanobacteria, which have reaction centers with a different organization. We also show that the domain contains several determinants that could mediate specific protein-protein interactions.

Conclusions: The PRC-barrel is a widespread, ancient domain that appears to have been recruited to a variety of biological systems, ranging from RNA processing to photosynthesis. Identification of this versatile domain in numerous proteins could aid investigation of unexplored aspects of their biology.

Figure 1

A ribbon representation of the H (gold) and the M (gray) subunits of the photosynthetic reaction complex (PDB 1 eys). The PRC-barrel is colored purple to highlight it. The two acidic residues projecting in the direction of the membrane, including the glutamate (E) involved in regulation of quinone reduction, are shown in space-filling representation. The peptide from the amino-terminal tail of the M subunit that interacts with a cleft in the PRC-barrel (PCR-M peptide) is also shown in space-filling representation.

Figure 2

A comparison of the PRC-barrel with the analogous β-barrels, namely the SH3-like barrel and the OB fold. (a) The representative of the SH3-like barrel is the dihydrofolate reductase subunit (PDB 1vie) and (b) the representative of the OB fold is the cold-shock protein S1-like RNA-binding domain (PDB 1mjc). Note the difference in packing of the last strand of the OB fold with respect to the first strand in the SH3-like barrel and (c) the PRC-barrel. In the case of the OB fold, note the difference in orientation of the second strand with respect to the first as compared to the other two β-barrels.

Figure 3

A multiple alignment of the PRC-barrel was constructed using T-Coffee [38] and realigning the sequences by parsing high-scoring pairs from PSI-BLAST search results. The secondary structure assigned by PHD [22] is shown above the alignment, with E representing a β-strand, and H an α-helix. The 85% consensus shown below the alignment was derived using the following amino-acid classes: hydrophobic (h, ALICVMYFW, yellow shading); the aliphatic subset of the hydrophobic class (l, ALIVMC, yellow shading); small (s, ACDGNPSTV, green) and polar (p, CDEHKNQRST, blue). A 'G' denotes the conserved G of the tiny subset of the small class. Columns of residues that are peculiar to a particular category of PRC-barrels (see text) are colored red. The limits of the domains are indicated by the residue positions on each side. The numbers within the alignment are non-conserved inserts that have not been shown. The different families are shown on the right. The sequences are denoted by their gene name followed by the species abbreviation and GenBank identifier (gi). The species abbreviations are: Archaea: Af, Archaeoglobus fulgidus; Hsp, Halobacterium sp. NRC-1; Mac, Methanosarcina acetivorans; Mta, Methanobacterium thermoautotrophicum; Mj, Methanococcus jannaschii; Ph, Pyrococcus horikoshii; Tac, Thermoplasma acidophilum; Bacteria: Atu, Agrobacterium tumefaciens; Aae, Aquifex aeolicus; Ana, Anabaena sp.; Bs, Bacillus subtilis; Bb, Borrelia burgdorferi; Bmel, Brucella melitensis; Cac, Clostridium acetobutylicum; Ccr, Caulobacter crescentus; Cj, Campylobacter jejuni; Des, Desulfitobacterium hafniense; Drad, Deinococcus radiodurans; Ec, Escherichia coli; Hi, Haemophilus influenzae; Hp, Helicobacter pylori; Mlo, Mesorhizobium loti; Mtu, Mycobacterium tuberculosis; Nm, Neisseria meningitidis; Pae, Pseudomonas aeruginosa; Pmar, Prochlorococcus marinus; Rcap, Rhodobacter capsulatus; Rp, Rickettsia prowazekii; Rsp, Rhodobacter sphaeroides; Rvi, Rhodopseudomonas viridis; Sli, Streptomyces lividans; Sme, Sinorhizobium meliloti; Scoe, Streptomyces coelicolor A3; Syco, Synechococcus sp.; Ssp, Synechocystis sp.; Tm, Thermotoga maritima; Tp, Treponema pallidum; Ter, Trichodesmium erythraeum; Tsyn, Thermosynechococcus elongatus; Ttep, Thermochromatium tepidum; Xf, Xylella fastidiosa; Plants: At, Arabidopsis thaliana.

Figure 4

Phylogenetic relationships of the PRC-barrel-containing proteins along with the domain architectures. The phyletic pattern of each family is shown, along with the number of proteins (if there is more than one). Species abbreviations are as in Figure 3. The RELL bootstrap values for the major branches are shown at their base. The thickness of a given branch is approximately proportional to the number of proteins contained within it. Ysnf, a repeat domain typified by the Bacillus subtilis YsnF protein; N-term, the specific amino-terminal domain of the RimM proteins.