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Structure and function of a cyanophage-encoded peptide deformylase.

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Frank JA, Lorimer D, Youle M, Witte P, Craig T, Abendroth J, Rohwer F, Edwards RA, Segall AM, Burgin AB
OpenAccess logo ISME J 7 1150-60 (2013)
Related entries: 3uwb, 4dr8, 4dr9

Cited: 22 times
EuropePMC logo PMID: 23407310

Abstract

Bacteriophages encode auxiliary metabolic genes that support more efficient phage replication. For example, cyanophages carry several genes to maintain host photosynthesis throughout infection, shuttling the energy and reducing power generated away from carbon fixation and into anabolic pathways. Photodamage to the D1/D2 proteins at the core of photosystem II necessitates their continual replacement. Synthesis of functional proteins in bacteria requires co-translational removal of the N-terminal formyl group by a peptide deformylase (PDF). Analysis of marine metagenomes to identify phage-encoded homologs of known metabolic genes found that marine phages carry PDF genes, suggesting that their expression during infection might benefit phage replication. We identified a PDF homolog in the genome of Synechococcus cyanophage S-SSM7. Sequence analysis confirmed that it possesses the three absolutely conserved motifs that form the active site in PDF metalloproteases. Phylogenetic analysis placed it within the Type 1B subclass, most closely related to the Arabidopsis chloroplast PDF, but lacking the C-terminal α-helix characteristic of that group. PDF proteins from this phage and from Synechococcus elongatus were expressed and characterized. The phage PDF is the more active enzyme and deformylates the N-terminal tetrapeptides from D1 proteins more efficiently than those from ribosomal proteins. Solution of the X-ray/crystal structures of those two PDFs to 1.95 Å resolution revealed active sites identical to that of the Type 1B Arabidopsis chloroplast PDF. Taken together, these findings show that many cyanophages encode a PDF with a D1 substrate preference that adds to the repertoire of genes used by phages to maintain photosynthetic activities.

Reviews - 3uwa mentioned but not cited (1)

  1. A Review on Viral Metagenomics in Extreme Environments. Dávila-Ramos S, Castelán-Sánchez HG, Martínez-Ávila L, Sánchez-Carbente MDR, Peralta R, Hernández-Mendoza A, Dobson ADW, Gonzalez RA, Pastor N, Batista-García RA. Front Microbiol 10 2403 (2019)

Articles - 3uwa mentioned but not cited (1)

  1. Structure and function of a cyanophage-encoded peptide deformylase. Frank JA, Lorimer D, Youle M, Witte P, Craig T, Abendroth J, Rohwer F, Edwards RA, Segall AM, Burgin AB. ISME J 7 1150-1160 (2013)


Reviews citing this publication (5)

  1. Phage puppet masters of the marine microbial realm. Breitbart M, Bonnain C, Malki K, Sawaya NA. Nat Microbiol 3 754-766 (2018)
  2. Pseudomonas predators: understanding and exploiting phage-host interactions. De Smet J, Hendrix H, Blasdel BG, Danis-Wlodarczyk K, Lavigne R. Nat Rev Microbiol 15 517-530 (2017)
  3. N-terminal protein modifications: Bringing back into play the ribosome. Giglione C, Fieulaine S, Meinnel T. Biochimie 114 134-146 (2015)
  4. Shedding new light on viral photosynthesis. Puxty RJ, Millard AD, Evans DJ, Scanlan DJ. Photosynth Res 126 71-97 (2015)
  5. Marine phage genomics: the tip of the iceberg. Perez Sepulveda B, Redgwell T, Rihtman B, Pitt F, Scanlan DJ, Millard A. FEMS Microbiol Lett 363 fnw158 (2016)

Articles citing this publication (15)

  1. Clades of huge phages from across Earth's ecosystems. Al-Shayeb B, Sachdeva R, Chen LX, Ward F, Munk P, Devoto A, Castelle CJ, Olm MR, Bouma-Gregson K, Amano Y, He C, Méheust R, Brooks B, Thomas A, Lavy A, Matheus-Carnevali P, Sun C, Goltsman DSA, Borton MA, Sharrar A, Jaffe AL, Nelson TC, Kantor R, Keren R, Lane KR, Farag IF, Lei S, Finstad K, Amundson R, Anantharaman K, Zhou J, Probst AJ, Power ME, Tringe SG, Li WJ, Wrighton K, Harrison S, Morowitz M, Relman DA, Doudna JA, Lehours AC, Warren L, Cate JHD, Santini JM, Banfield JF. Nature 578 425-431 (2020)
  2. Depth-stratified functional and taxonomic niche specialization in the 'core' and 'flexible' Pacific Ocean Virome. Hurwitz BL, Brum JR, Sullivan MB. ISME J 9 472-484 (2015)
  3. High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection. De Smet J, Zimmermann M, Kogadeeva M, Ceyssens PJ, Vermaelen W, Blasdel B, Bin Jang H, Sauer U, Lavigne R. ISME J 10 1823-1835 (2016)
  4. Diversities and potential biogeochemical impacts of mangrove soil viruses. Jin M, Guo X, Zhang R, Qu W, Gao B, Zeng R. Microbiome 7 58 (2019)
  5. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Mizuno CM, Guyomar C, Roux S, Lavigne R, Rodriguez-Valera F, Sullivan MB, Gillet R, Forterre P, Krupovic M. Nat Commun 10 752 (2019)
  6. PhANNs, a fast and accurate tool and web server to classify phage structural proteins. Cantu VA, Salamon P, Seguritan V, Redfield J, Salamon D, Edwards RA, Segall AM. PLoS Comput Biol 16 e1007845 (2020)
  7. Formyl-methionine as a degradation signal at the N-termini of bacterial proteins. Piatkov KI, Vu TT, Hwang CS, Varshavsky A. Microb Cell 2 376-393 (2015)
  8. Heterogenic virulence in a diarrheagenic Escherichia coli: evidence for an EPEC expressing heat-labile toxin of ETEC. Dutta S, Pazhani GP, Nataro JP, Ramamurthy T. Int J Med Microbiol 305 47-54 (2015)
  9. Nitrogen sourcing during viral infection of marine cyanobacteria. Waldbauer JR, Coleman ML, Rizzo AI, Campbell KL, Lotus J, Zhang L. Proc Natl Acad Sci U S A 116 15590-15595 (2019)
  10. Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments. Zaragoza-Solas A, Rodriguez-Valera F, López-Pérez M. mSystems 5 e00905-19 (2020)
  11. Microbial community diversity and physical-chemical features of the Southwestern Atlantic Ocean. Alves Junior N, Meirelles PM, de Oliveira Santos E, Dutilh B, Silva GG, Paranhos R, Cabral AS, Rezende C, Iida T, de Moura RL, Kruger RH, Pereira RC, Valle R, Sawabe T, Thompson C, Thompson F. Arch Microbiol 197 165-179 (2015)
  12. Induction mechanisms and strategies underlying interprophage competition during polylysogeny. Silpe JE, Duddy OP, Bassler BL. PLoS Pathog 19 e1011363 (2023)
  13. Marine and giant viruses as indicators of a marine microbial community in a riverine system. Dann LM, Rosales S, McKerral J, Paterson JS, Smith RJ, Jeffries TC, Oliver RL, Mitchell JG. Microbiologyopen 5 1071-1084 (2016)
  14. The C-terminal residue of phage Vp16 PDF, the smallest peptide deformylase, acts as an offset element locking the active conformation. Grzela R, Nusbaum J, Fieulaine S, Lavecchia F, Bienvenut WV, Dian C, Meinnel T, Giglione C. Sci Rep 7 11041 (2017)
  15. The complete genome of Vibrio sp. 16 unveils two circular chromosomes and a distinctive 46-kb plasmid. Wu X, Segall AM, Giglione C, Meinnel T. Microbiol Resour Announc 13 e0122223 (2024)


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