Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism

Cyanophages infecting the marine cyanobacteria Prochlorococcus and Synechococcus encode and express genes for the photosynthetic light reactions. Sequenced cyanophage genomes lack Calvin cycle genes, however, suggesting that photosynthetic energy harvested via phage proteins is not used for carbon f...

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Main Authors: Thompson, Luke Richard (Contributor), Zeng, Qinglu (Contributor), Kelly, Libusha (Contributor), Huang, Katherine H. (Contributor), Singer, Alexander U. (Author), Stubbe, JoAnne (Contributor), Chisholm, Sallie (Penny) (Contributor)
Other Authors: Massachusetts Institute of Technology. Department of Biology (Contributor), Massachusetts Institute of Technology. Department of Chemistry (Contributor), Massachusetts Institute of Technology. Department of Civil and Environmental Engineering (Contributor)
Format: Article
Language:English
Published: National Academy of Sciences (U.S.), 2012-04-25T20:37:40Z.
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Online Access:Get fulltext
LEADER 03540 am a22003853u 4500
001 70139
042 |a dc 
100 1 0 |a Thompson, Luke Richard  |e author 
100 1 0 |a Massachusetts Institute of Technology. Department of Biology  |e contributor 
100 1 0 |a Massachusetts Institute of Technology. Department of Chemistry  |e contributor 
100 1 0 |a Massachusetts Institute of Technology. Department of Civil and Environmental Engineering  |e contributor 
100 1 0 |a Stubbe, JoAnne  |e contributor 
100 1 0 |a Stubbe, JoAnne  |e contributor 
100 1 0 |a Thompson, Luke Richard  |e contributor 
100 1 0 |a Zeng, Qinglu  |e contributor 
100 1 0 |a Kelly, Libusha  |e contributor 
100 1 0 |a Huang, Katherine H.  |e contributor 
100 1 0 |a Chisholm, Sallie   |q  (Penny)   |e contributor 
700 1 0 |a Zeng, Qinglu  |e author 
700 1 0 |a Kelly, Libusha  |e author 
700 1 0 |a Huang, Katherine H.  |e author 
700 1 0 |a Singer, Alexander U.  |e author 
700 1 0 |a Stubbe, JoAnne  |e author 
700 1 0 |a Chisholm, Sallie   |q  (Penny)   |e author 
245 0 0 |a Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism 
260 |b National Academy of Sciences (U.S.),   |c 2012-04-25T20:37:40Z. 
856 |z Get fulltext  |u http://hdl.handle.net/1721.1/70139 
520 |a Cyanophages infecting the marine cyanobacteria Prochlorococcus and Synechococcus encode and express genes for the photosynthetic light reactions. Sequenced cyanophage genomes lack Calvin cycle genes, however, suggesting that photosynthetic energy harvested via phage proteins is not used for carbon fixation. We report here that cyanophages carry and express a Calvin cycle inhibitor, CP12, whose host homologue directs carbon flux from the Calvin cycle to the pentose phosphate pathway (PPP). Phage CP12 was coexpressed with phage genes involved in the light reactions, deoxynucleotide biosynthesis, and the PPP, including a transaldolase gene that is the most prevalent PPP gene in cyanophages. Phage transaldolase was purified to homogeneity from several strains and shown to be functional in vitro, suggesting that it might facilitate increased flux through this key reaction in the host PPP, augmenting production of NADPH and ribose 5-phosphate. Kinetic measurements of phage and host transaldolases revealed that the phage enzymes have kcat/Km values only approximately one third of the corresponding host enzymes. The lower efficiency of phage transaldolase may be a tradeoff for other selective advantages such as reduced gene size: we show that more than half of host-like cyanophage genes are significantly shorter than their host homologues. Consistent with decreased Calvin cycle activity and increased PPP and light reaction activity under infection, the host NADPH/NADP ratio increased two-fold in infected cells. We propose that phage-augmented NADPH production fuels deoxynucleotide biosynthesis for phage replication, and that the selection pressures molding phage genomes involve fitness advantages conferred through mobilization of host energy stores. 
520 |a Gordon and Betty Moore Foundation 
520 |a United States. Dept. of Energy (Genomics:GTL Program) 
520 |a National Science Foundation (U.S.) (Center for Microbial Oceanography: Research and Education) 
520 |a National Institutes of Health (U.S.) (Training Grant) 
546 |a en_US 
655 7 |a Article 
773 |t Proceedings of the National Academy of Sciences of the United States of America