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Plant Cell. 2014 Jun;26(6):2689-2707. doi: 10.1105/tpc.114.125641. Epub 2014 Jun 10.

Rewiring Host Lipid Metabolism by Large Viruses Determines the Fate of Emiliania huxleyi, a Bloom-Forming Alga in the Ocean.

The Plant cell

Shilo Rosenwasser, Michaela A Mausz, Daniella Schatz, Uri Sheyn, Sergey Malitsky, Asaph Aharoni, Eyal Weinstock, Oren Tzfadia, Shifra Ben-Dor, Ester Feldmesser, Georg Pohnert, Assaf Vardi

Affiliations

  1. Department of Plant Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel.
  2. Institute of Inorganic and Analytical Chemistry/Bioorganic Analytics, Friedrich Schiller University Jena, 07743 Jena, Germany Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute, 07745 Jena, Germany.
  3. Bioinformatics and Biological Computing Unit, Weizmann Institute of Science, Rehovot 7610001, Israel.
  4. The Nancy and Stephen Grand Israel National Center for Personalized Medicine, Weizmann Institute of Science, Rehovot 7610001, Israel.
  5. Institute of Inorganic and Analytical Chemistry/Bioorganic Analytics, Friedrich Schiller University Jena, 07743 Jena, Germany.
  6. Department of Plant Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel [email protected].

PMID: 24920329 PMCID: PMC4114960 DOI: 10.1105/tpc.114.125641

Abstract

Marine viruses are major ecological and evolutionary drivers of microbial food webs regulating the fate of carbon in the ocean. We combined transcriptomic and metabolomic analyses to explore the cellular pathways mediating the interaction between the bloom-forming coccolithophore Emiliania huxleyi and its specific coccolithoviruses (E. huxleyi virus [EhV]). We show that EhV induces profound transcriptome remodeling targeted toward fatty acid synthesis to support viral assembly. A metabolic shift toward production of viral-derived sphingolipids was detected during infection and coincided with downregulation of host de novo sphingolipid genes and induction of the viral-encoded homologous pathway. The depletion of host-specific sterols during lytic infection and their detection in purified virions revealed their novel role in viral life cycle. We identify an essential function of the mevalonate-isoprenoid branch of sterol biosynthesis during infection and propose its downregulation as an antiviral mechanism. We demonstrate how viral replication depends on the hijacking of host lipid metabolism during the chemical "arms race" in the ocean.

© 2014 American Society of Plant Biologists. All rights reserved.

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