Abstract

A newly identified arbitrium communication system regulates the lysis-to-lysogeny decision in a Bacillus bacteriophage. This system contains an arbitrium hexapeptide as a signal, the cellular receptor AimR, and the lysogenic negative regulator AimX. AimR specifically targets the downstream DNA to activate aimX gene expression. The arbitrium peptide binds to AimR, inhibiting its DNA-binding to promote phage lysogeny. Recently, we and other groups have elucidated how arbitrium peptide sensed by AimR. However, the molecular mechanisms of DNA recognition by AimR and the regulation of its DNA-binding activity by the peptide remain largely unknown. Here, we report the crystal structure of the AimR–DNA complex at 2.1 Å resolution. The N-terminal HTH motif recognizes the palindromic DNA sequence, buttressed by interactions between positively charged residues and the DNA phosphate groups. The DNA-bound AimR assembles a more closed dimer than the peptide-bound form. Single-molecule FRET and crosslinking assays revealed that the AimR protein samples both open and closed conformations in solution. Arbitrium peptide binding induces a closed-to-open conformational change of AimR, eliminating DNA targeting. Our structural and functional analysis provides new insights into the DNA recognition mechanism of AimR and its regulation by the arbitrium peptide in the context of phage lysis-lysogeny decisions.

Highlights

  • 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Introduction Gram-positive bacteria communicate with each other via secreted peptide signals to adapt to the environment by regulating gene expression related to bacterial sporulation, biofilm formation, the virulence activation process, etc.[1,2,3,4,5,6,7]

  • 5- to 10-amino acid signal peptides are sensed by receptors, leading to allosteric regulation of the receptors’ activity

  • We reported the structures of AimR with and without the arbitrium peptide from SPbeta group phages[15]

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Summary

Introduction

Gram-positive bacteria communicate with each other via secreted peptide signals to adapt to the environment by regulating gene expression related to bacterial sporulation, biofilm formation, the virulence activation process, etc.[1,2,3,4,5,6,7]. In Bacillus phages, a peptide communication system named the arbitrium system was identified that plays an essential role in lysis–lysogeny decisions during infection of Bacillus host cells[11,12,13,14]. This system requires the arbitrium hexapeptide to bind to its cellular receptor AimR to regulate transcription of the lysogeny negative regulator gene aimX. The premature peptides are secreted to the extracellular environment and cleaved by bacterial extracellular proteases to generate the mature

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