Structure and function of a cyanophage-encoded peptide deformylase.

Bacteriophages encode auxiliary metabolic genes that support more efficient phage replication. Forexample, cyanophages carry several genes to maintain host photosynthesis throughout infection,shuttling the energy and reducing power generated away from carbon fixation and into anabolicpathways. Photodamage to the D1/D2 proteins at the core of photosystem II necessitates theircontinual replacement. Synthesis of functional proteins in bacteria requires co-translational removalof the N-terminal formyl group by a peptide deformylase (PDF). Analysis of marine metagenomes toidentify phage-encoded homologs of known metabolic genes found that marine phages carry PDFgenes, suggesting that their expression during infection might benefit phage replication. Weidentified a PDF homolog in the genome of Synechococcus cyanophage S-SSM7. Sequence analysisconfirmed that it possesses the three absolutely conserved motifs that form the active site in PDFmetalloproteases. Phylogenetic analysis placed it within the Type 1B subclass, most closely relatedto the Arabidopsis chloroplast PDF, but lacking the C-terminal a-helix characteristic of that group.PDF proteins from this phage and from Synechococcus elongatus were expressed andcharacterized. The phage PDF is the more active enzyme and deformylates the N-terminaltetrapeptides from D1 proteins more efficiently than those from ribosomal proteins. Solution ofthe X-ray/crystal structures of those two PDFs to 1.95A˚ resolution revealed active sites identical tothat of the Type 1B Arabidopsis chloroplast PDF. Taken together, these findings show that manycyanophages encode a PDF with a D1 substrate preference that adds to the repertoire of genes usedby phages to maintain photosynthetic activities.The ISME Journal advance online publication, 14 February 2013; doi:10.1038/ismej.2013.4Subject Category: Integrated genomics and post-genomics approaches in microbial ecologyKeywords: peptide deformylase; virus–host interactions; cyanophage; enzyme structure;photosynthesis; phage–host interactions