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

Luke R. Thompson, Qinglu Zeng, Libusha Kelly, Katherine H. Huang, Alexander U. Singer, JoAnne Stubbe, Sallie W. Chisholm

Research output: Contribution to journalArticle

151 Citations (Scopus)

Abstract

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 k cat/K m 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.

Original languageEnglish (US)
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number39
DOIs
StatePublished - Sep 27 2011
Externally publishedYes

Fingerprint

Bacteriophages
Carbon
Transaldolase
Pentose Phosphate Pathway
Genes
Photosynthesis
NADP
Carbon Cycle
Light
Prochlorococcus
Genome
Synechococcus
Cyanobacteria
Enzymes
Cats
Pressure
Infection

Keywords

  • Coevolution
  • Photosynthesis
  • Virus

ASJC Scopus subject areas

  • General

Cite this

Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. / Thompson, Luke R.; Zeng, Qinglu; Kelly, Libusha; Huang, Katherine H.; Singer, Alexander U.; Stubbe, JoAnne; Chisholm, Sallie W.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 39, 27.09.2011.

Research output: Contribution to journalArticle

Thompson, Luke R. ; Zeng, Qinglu ; Kelly, Libusha ; Huang, Katherine H. ; Singer, Alexander U. ; Stubbe, JoAnne ; Chisholm, Sallie W. / Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 39.
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