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, Zeng, Qinglu, Kelly, Libusha, Huang, Katherine H., Singer, Alexander U., Stubbe, JoAnne, Chisholm, Sallie (Penny)
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2012
Online Access:http://hdl.handle.net/1721.1/70139
https://orcid.org/0000-0001-8076-4489
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author Thompson, Luke Richard
Zeng, Qinglu
Kelly, Libusha
Huang, Katherine H.
Singer, Alexander U.
Stubbe, JoAnne
Chisholm, Sallie (Penny)
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Thompson, Luke Richard
Zeng, Qinglu
Kelly, Libusha
Huang, Katherine H.
Singer, Alexander U.
Stubbe, JoAnne
Chisholm, Sallie (Penny)
author_sort Thompson, Luke Richard
collection MIT
description 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.
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spelling mit-1721.1/701392022-10-01T07:42:21Z Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism Thompson, Luke Richard Zeng, Qinglu Kelly, Libusha Huang, Katherine H. Singer, Alexander U. Stubbe, JoAnne Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Chemistry Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Stubbe, JoAnne Stubbe, JoAnne Thompson, Luke Richard Zeng, Qinglu Kelly, Libusha Huang, Katherine H. Chisholm, Sallie (Penny) 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. Gordon and Betty Moore Foundation United States. Dept. of Energy (Genomics:GTL Program) National Science Foundation (U.S.) (Center for Microbial Oceanography: Research and Education) National Institutes of Health (U.S.) (Training Grant) 2012-04-25T20:37:40Z 2012-04-25T20:37:40Z 2011-09 2011-02 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/70139 Thompson, L. R. et al. “Phage Auxiliary Metabolic Genes and the Redirection of Cyanobacterial Host Carbon Metabolism.” Proceedings of the National Academy of Sciences 108.39 (2011): E757–E764. Web. https://orcid.org/0000-0001-8076-4489 en_US http://dx.doi.org/10.1073/pnas.1102164108 Proceedings of the National Academy of Sciences of the United States of America Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS
spellingShingle Thompson, Luke Richard
Zeng, Qinglu
Kelly, Libusha
Huang, Katherine H.
Singer, Alexander U.
Stubbe, JoAnne
Chisholm, Sallie (Penny)
Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title_full Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title_fullStr Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title_full_unstemmed Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title_short Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
title_sort phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
url http://hdl.handle.net/1721.1/70139
https://orcid.org/0000-0001-8076-4489
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