Phages reconstitute NAD+ to counter bacterial immunity

Nature. 2024 Oct;634(8036):1160-1167. doi: 10.1038/s41586-024-07986-w. Epub 2024 Sep 25.

Abstract

Bacteria defend against phage infection through a variety of antiphage defence systems1. Many defence systems were recently shown to deplete cellular nicotinamide adenine dinucleotide (NAD+) in response to infection, by cleaving NAD+ into ADP-ribose (ADPR) and nicotinamide2-7. It was demonstrated that NAD+ depletion during infection deprives the phage of this essential molecule and impedes phage replication. Here we show that a substantial fraction of phages possess enzymatic pathways allowing reconstitution of NAD+ from its degradation products in infected cells. We describe NAD+ reconstitution pathway 1 (NARP1), a two-step pathway in which one enzyme phosphorylates ADPR to generate ADPR pyrophosphate (ADPR-PP), and the second enzyme conjugates ADPR-PP and nicotinamide to generate NAD+. Phages encoding NARP1 can overcome a diverse set of defence systems, including Thoeris, DSR1, DSR2, SIR2-HerA and SEFIR, all of which deplete NAD+ as part of their defensive mechanism. Phylogenetic analyses show that NARP1 is primarily encoded on phage genomes, suggesting a phage-specific function in countering bacterial defences. A second pathway, NARP2, allows phages to overcome bacterial defences by building NAD+ using metabolites different from ADPR-PP. Our findings reveal a unique immune evasion strategy in which viruses rebuild molecules depleted by defence systems, thus overcoming host immunity.

MeSH terms

  • Adenosine Diphosphate Ribose / chemistry
  • Adenosine Diphosphate Ribose / metabolism
  • Bacteria* / immunology
  • Bacteria* / metabolism
  • Bacteria* / virology
  • Bacteriophages* / genetics
  • Bacteriophages* / immunology
  • Bacteriophages* / metabolism
  • Bacteriophages* / physiology
  • Evolution, Molecular
  • Genome, Viral / genetics
  • Immune Evasion*
  • NAD* / biosynthesis
  • NAD* / chemistry
  • NAD* / metabolism
  • Niacinamide / chemistry
  • Niacinamide / metabolism
  • Phosphorylation
  • Phylogeny

Substances

  • Adenosine Diphosphate Ribose
  • NAD
  • Niacinamide