Viral infection of the marine alga <i>Emiliania huxleyi</i> triggers lipidome remodeling and induces the production of highly saturated triacylglycerol

Malitsky, Sergey; Ziv, Carmit; Rosenwasser, Shilo; Zheng, Shuning; Schatz, Daniella; Porat, Ziv; Ben‐Dor, Shifra; Aharoni, Asaph; Vardi, Assaf

doi:10.1111/nph.13852

Cited by 106 publications

(136 citation statements)

References 67 publications

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“…Consistent with the idea that viral proteins act to amend host N metabolic function, a putative glutamine synthetase gene has also been identified in the genomes of NCLDVs such as Mimivirus and Mamavirus (76). These data suggest that viral reprogramming of host N metabolism may be a wider phenomenon (21,77), as has been shown for photosynthetic function (78), sulfur oxidation (79), and lipid (25)(26)(27) and phosphate metabolism (80). Evidence that a viral lineage can acquire host genes to amend host nutrient uptake has implications for our understanding of phytoplankton ecology.…”

Section: Viral Manipulation Of Host Elemental Compositionsupporting

confidence: 58%

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Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

Monier

Chambouvet

Milner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Phytoplankton community structure is shaped by both bottomup factors, such as nutrient availability, and top-down processes, such as predation. Here we show that marine viruses can blur these distinctions, being able to amend how host cells acquire nutrients from their environment while also predating and lysing their algal hosts. Viral genomes often encode genes derived from their host. These genes may allow the virus to manipulate host metabolism to improve viral fitness. We identify in the genome of a phytoplankton virus, which infects the small green alga Ostreococcus tauri, a host-derived ammonium transporter. This gene is transcribed during infection and when expressed in yeast mutants the viral protein is located to the plasma membrane and rescues growth when cultured with ammonium as the sole nitrogen source. We also show that viral infection alters the nature of nitrogen compound uptake of host cells, by both increasing substrate affinity and allowing the host to access diverse nitrogen sources. This is important because the availability of nitrogen often limits phytoplankton growth. Collectively, these data show that a virus can acquire genes encoding nutrient transporters from a host genome and that expression of the viral gene can alter the nutrient uptake behavior of host cells. These results have implications for understanding how viruses manipulate the physiology and ecology of phytoplankton, influence marine nutrient cycles, and act as vectors for horizontal gene transfer.Phycodnaviridae | NCLDV | prasinophytes | Mamiellophyceae | lateral gene transfer

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Section: Viral Manipulation Of Host Elemental Compositionsupporting

confidence: 58%

“…lipid biosynthesis of eukaryotic algal cells (25)(26)(27). AMGs are thought to modulate host function to improve fitness of the virus and, in some cases, temporarily the host.…”

Section: Significancementioning

confidence: 99%

Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

Monier

Chambouvet

Milner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In the marine alga Emiliania huxleyi infected with a lytic virus, MGDG and DGDG levels decreased and TAGs increased within 48 hr of viral infection. The latter had more saturated fatty acid chains than TAG from uninfected cells and genes involved in TAG biosynthesis were up-regulated [68]. In Arabidopsis, major phospholipids but not galactolipids decreased when cold acclimated plants (4 o C) were exposed to freezing stress (-8 o C) over 12 hr [45].…”

Section: Discussionmentioning

confidence: 99%

Defense related decadienal elicits membrane lipid remodeling in the diatom Phaeodactylum tricornutum

2017

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Diatoms rapidly release extracellular oxylipins (oxygenated lipids) including polyunsaturated aldehydes in response to herbivory and other stresses. Oxylipins have several defense-related activities including inhibition of reproduction in herbivores and signaling to distant diatoms. Physiological changes in diatoms exposed to varying levels of oxylipins are only beginning to be understood. In this study, Phaeodactylum tricornutum cultures were treated with sublethal concentrations of the polyunsaturated aldehyde trans,trans-2,4-decadienal (DD) to assess effects on lipid composition and membrane permeability. In cells treated with DD for 3 hr, all measured saturated and unsaturated fatty acids significantly decreased (0.46–0.69 fold of levels in solvent control cells) except for 18:2 (decreased but not significantly). The decrease was greater in the polyunsaturated fatty acid pool than the saturated and monounsaturated fatty acid pool. Analysis of lipid classes revealed increased abundances of phosphatidylethanolamine and phosphatidylcholine at 3 and 6 hr. Concomitantly, these and other membrane lipids exhibited increased saturated and monounsaturated acyl chains content relative to polyunsaturated acyl chains compared to control cells. Evidence of decreased plasma membrane permeability in DD treated cells was obtained, based on reduced uptake of two of three dyes relative to control cells. Additionally, cells pre-conditioned with a sublethal DD dose for 3 hr then treated with a lethal DD dose for 2 hr exhibited greater membrane integrity than solvent pre-conditioned control cells that were similarly treated. Taken together, the data are supportive of the hypothesis that membrane remodeling induced by sublethal DD is a key element in the development of cellular resistance in diatoms to varying and potentially toxic levels of polyunsaturated aldehydes in environments impacted by herbivory or other stresses.

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“…The role of lipids during EhV-86 infection is not well understood, but it is thought that the control of lipid production could be associated with host membrane interactions, which facilitate the intracellular transport and subsequent budding of virus particles [41,42]. The HNH endonuclease family protein (ehv093) (Table S1), a type of restriction endonuclease, was present in the haploid transcriptome.…”

Section: Discussionmentioning

confidence: 99%

Schrödinger’s Cheshire Cat: Are Haploid Emiliania huxleyi Cells Resistant to Viral Infection or Not?

Mordecai

Verret

Highfield

et al. 2017

Viruses

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Emiliania huxleyi is the main calcite producer on Earth and is routinely infected by a virus (EhV); a double stranded DNA (dsDNA) virus belonging to the family Phycodnaviridae. E. huxleyi exhibits a haplodiploid life cycle; the calcified diploid stage is non-motile and forms extensive blooms. The haploid phase is a non-calcified biflagellated cell bearing organic scales. Haploid cells are thought to resist infection, through a process deemed the “Cheshire Cat” escape strategy; however, a recent study detected the presence of viral lipids in the same haploid strain. Here we report on the application of an E. huxleyi CCMP1516 EhV-86 combined tiling array (TA) that further confirms an EhV infection in the RCC1217 haploid strain, which grew without any signs of cell lysis. Reverse transcription polymerase chain reaction (RT-PCR) and PCR verified the presence of viral RNA in the haploid cells, yet indicated an absence of viral DNA, respectively. These infected cells are an alternative stage of the virus life cycle deemed the haplococcolithovirocell. In this instance, the host is both resistant to and infected by EhV, i.e., the viral transcriptome is present in haploid cells whilst there is no evidence of viral lysis. This superimposed state is reminiscent of Schrödinger’s cat; of being simultaneously both dead and alive.

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Viral infection of the marine alga Emiliania huxleyi triggers lipidome remodeling and induces the production of highly saturated triacylglycerol

Cited by 106 publications

References 67 publications

Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

Defense related decadienal elicits membrane lipid remodeling in the diatom Phaeodactylum tricornutum

Schrödinger’s Cheshire Cat: Are Haploid Emiliania huxleyi Cells Resistant to Viral Infection or Not?

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