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Structural Basis of the Arbitrium Peptide–Aimr Communication System in the Phage Lysis–Lysogeny Decision

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Structural Basis of the Arbitrium Peptide–Aimr Communication System in the Phage Lysis–Lysogeny Decision ARTICLES https://doi.org/10.1038/s41564-018-0239-y Structural basis of the arbitrium peptide–AimR communication system in the phage lysis–lysogeny decision Qiang Wang1,4, Zeyuan Guan1,4, Kai Pei1, Jing Wang1, Zhu Liu1, Ping Yin1, Donghai Peng2 and Tingting Zou 3* A bacteriophage can replicate and release virions from a host cell in the lytic cycle or switch to a lysogenic process in which the phage integrates itself into the host genome as a prophage. In Bacillus cells, some types of phages employ the arbitrium com- munication system, which contains an arbitrium hexapeptide, the cellular receptor AimR and the lysogenic negative regulator AimX. This system controls the decision between the lytic and lysogenic cycles. However, both the mechanism of molecular recognition between the arbitrium peptide and AimR and how downstream gene expression is regulated remain unknown. Here, we report crystal structures for AimR from the SPbeta phage in the apo form and the arbitrium peptide-bound form at 2.20 Å and 1.92 Å, respectively. With or without the peptide, AimR dimerizes through the C-terminal capping helix. AimR assembles a superhelical fold and accommodates the peptide encircled by its tetratricopeptide repeats, which is reminiscent of RRNPP fam- ily members from the quorum-sensing system. In the absence of the arbitrium peptide, AimR targets the upstream sequence of the aimX gene; its DNA binding activity is prevented following peptide binding. In summary, our findings provide a structural basis for peptide recognition in the phage lysis–lysogeny decision communication system. uring the infection of a bacterial host, a temperate phage can The AimP protein consists of 43 amino acids that encode an either enter the lytic cycle or the lysogenic cycle. In the lytic N-terminal signal sequence and a C-terminal protease-cleavage Dcycle, multiple phage particles are produced and released into site. AimP is secreted by bacteria into the extracellular environment the environment, whereas in the lysogenic cycle, a phage incorpo- and is processed into a mature six-residue peptide called the arbi- rates its DNA into the host genome to establish a potentially ben- trium peptide. The arbitrium peptide concentration increases in the eficial relationship with the host1. The phage harnesses two types late infection stages as the number of phage particles increases. The of life-cycle transitions to survive under different conditions. arbitrium peptide can be taken up by other B. subtilis cells through Numerous studies have focused on the lysis–lysogeny decision of the bacterial oligopeptide permease transporter and binds to the bacteriophage lambda in Escherichia coli2–4. Some gene regulatory AimR receptor, inhibiting its DNA binding activity. As a result, the circuits in the phage genome, including the pL and pR lytic pro- lytic cycle is strongly suppressed and the phage switches to the lyso- moters, initiate early transcription and induce expression of the genic life cycle. This type of arbitrium communication system has lysogenic regulators CII and CIII5,6. In addition, intracellular signal- been identified in more than 100 Bacillus phages or prophages; arbi- ling factors play important roles in the lysis–lysogeny decision. For trium hexapeptide sequences are variable in the first three positions example, the accumulation of the lysogenic regulator CII protein but are more conserved in the last three positions (Supplementary promotes phage genome integration into the bacterial chromo- Fig. 1). Each hexapeptide binds specifically to the corresponding some7. However, few studies have focused on signal transduction in AimR receptor from the same phage to trigger the lysis-to-lysogeny other phage infection systems. transition. However, the molecular basis of the specific recogni- Recently, a communication system that contributes to the deci- tion between the arbitrium peptide and AimR remains unknown. sion process between lysis and lysogeny was characterized for SPbeta Moreover, the mechanism by which the arbitrium peptide regulates group phages during infection of Bacillus subtilis cells. This system, AimR DNA binding activity needs to be investigated. demonstrated using a phi3T phage, contains three phage genes: Here, we report the crystal structures of the SPbeta phage AimR aimP, encoding a small peptide as a signal molecule; aimR, encod- alone and in complex with the arbitrium peptide (GMPRGA) at ing a receptor for perceiving the signal peptide; and aimX, encod- resolutions of 2.20 Å and 1.92 Å, respectively. Both the apo and the ing a regulatory protein that inhibits the lysogenic process8–10. AimR peptide-bound forms dimerized via the C-terminal capping helix. includes a predicted N-terminal helix–turn–helix DNA binding AimR comprises four atypical TPR repeats that form a peptide motif followed by a tetratricopeptide repeat (TPR) domain, which accommodation pocket with other helices, which is reminiscent of is a typical motif found in intracellular peptide receptors of the other RRNPP family members. Together with biochemical analyses, RRNPP (named for the different sensors: Rgg, Rap, NprR, PlcR and we show that AimR directly recognizes the upstream sequence of PrgX) family in quorum-sensing systems11–14. During the lytic cycle, the aimX gene in vitro but abrogates its DNA binding activity fol- AimR binds upstream of the aimX gene, activating its transcription. lowing arbitrium peptide binding. This study provides a structural 1National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Huazhong Agricultural University, Wuhan, China. 2State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China. 3College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China. 4These authors contributed equally: Qiang Wang, Zeyuan Guan. *e-mail: [email protected] NatURE MICROBIOLOgy | www.nature.com/naturemicrobiology ARTICLES NATURE MICROBIOLOGY a a 100 Å α4 N α5 N α2 9 37 Å L386 L386 α α6 α10 α3 α7 α1 L383 L384 L383 α8 α11 60 Å L384 α14 α12 CC L380 L380 18 13 α AimR α AimR A α16 B Helix 20 Helix 20 α20 AimRA AimRB 17 α15 α α19 b 44.1 kDa 88.0 kDa 50 Å 1.5 ) 125 b 93.3 ± 1.7 kDa 100 1.0 75 47.6 ± 1.5 kDa c(s) 50 0.5 25 0.0 Molecular mass (kDa 0 2 468 13 14 15 16 17 18 Sedimentation coefficient (S) Volume (ml) Fig. 2 | Effect of the AimR α20 on dimerization. a, Close-up view of the AimR dimerization interface. The residues L380, L383, L384 and L386 Fig. 1 | Crystal structure of the apo form of AimR. a, The overall structure from protomer A (α 20), as well as their counterparts from protomer B, of apo AimR. Dimeric AimR has the shape of an inverted trapezoid that is that are involved in hydrophobic interactions, are highlighted with sticks. 60 Å deep, with sides measuring 100 Å and 50 Å. The width of the inner b, Molecular mass of full-length AimR and the AimR Δ C mutant (residues cavity is approximately 37 Å. The two protomers are coloured from blue to 1–373), as measured by SV-AUC (left) and SLS (right). Full-length AimR is red along their length. The N terminus and C terminus of each protomer shown in black, and the AimR Δ C mutant in blue. The calculated molecular are indicated. The number of α -helices are sequentially named from the N masses are indicated above each panel. c(s) represents continuous terminus and are labelled on the cylinders. b, Surface features of the AimR (sedimentation coefficient distribution) analysis model. These experiments homodimer by electrostatic potential (blue, basic; red, acidic). Two regions were performed twice with equivalent results. Values in the right panel on the top side (indicated by the pink dashed outlines) are surrounded by represent mean ± s.d. positively charged amino acids. basis for the arbitrium communication system in phages during the of 20 α-helices, eight of which assemble into four atypical TPR lysis–lysogeny decision process. motifs: TPR1 (residues 186–226), TPR2 (residues 227–263), TPR3 (residues 295–327) and TPR4 (residues 328–361) (Supplementary Results Fig. 3). A Dali search using AimR as a query showed that 6 of 11 Crystal structure of apo AimR. To elucidate the mechanism of retrieved structures, comprising RapF, RapJ, NprR, PlcR, RapI and peptide recognition by the AimR protein, we determined the crystal RapH, with Z-scores higher than 13, were RRNPP family mem- structures of AimR with and without the AimP peptide. We sys- bers (Supplementary Table 2)15–20. These structural features are tematically screened the expression and peptide-binding activities consistent with previous analyses reporting that AimR belongs to of AimR homologues from Bacillus aerophilus, Bacillus sonorensis the RRNPP family, which is found in quorum-sensing systems of L12 and Bacillus phages phi3T and SPbeta. After numerous crystal- Gram-positive bacteria8. lization attempts, we crystallized the full-length apo and peptide- The C-terminal helix (α20), named the capping helix, mediates bound forms of AimR from the SPbeta group phage. The complex AimR dimerization (Fig. 1a and Fig. 2a) and has a solvent-accessible structure was determined using the single-wavelength anomalous area of approximately 810 Å2. Several residues from each capping diffraction method and was refined to a resolution of 1.92 Å. The helix, including L380, L383, L384 and L386, form a network of structure of the apo form was determined at a 2.20 Å resolution and van der Waals interactions (Fig. 2a). To investigate the oligomer- solved by molecular replacement using the coordinates of the AimP ization state of AimR in solution, we performed sedimentation peptide–AimR complex structure. The electron density of the N ter- velocity analytical ultracentrifugation (SV-AUC) and static light minus of AimR (amino acid residues 1–43) does not result in a well- scattering (SLS) analyses.
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