Viral activation and recruitment of metacaspases in the unicellular coccolithophore,
            <i>Emiliania huxleyi</i>

Bidle, Kay D.; Haramaty, Liti; Ramos, Joana Barcelos e; Falkowski, Paul G.

doi:10.1073/pnas.0701240104

Cited by 166 publications

(247 citation statements)

References 40 publications

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“…ROS was previously proposed to be associated with viral infection and specifically with induction of hallmarks of programmed cell death during the lytic phase of infection in E. huxleyi cultures (Evans et al, 2006) and mesocosm experiments (Vardi et al, 2012). Recent reports have shown a reduction in the photosystem II efficiency, chlorophyll degradation and carotenoid production during E. huxleyi infection, supporting a possible source for ROS generation (Evans et al, 2006;Bidle et al, 2007;Llewellyn et al, 2007;Bale et al, 2013;Kimmance et al, 2014). Our transcriptome analysis suggested an additional enzymatic source for ROS production by induction of NADPH oxidase (Figure 1).…”

Section: Discussionmentioning

confidence: 99%

“…Taken together, the results presented here clearly imply a pivotal role for ROS metabolism during this host-virus interaction. ROS can mediate the cross-talk between the main cellular pathways that are triggered during EhV infection: autophagy , sphingolipid metabolism (Vardi et al, 2009) and programmed cell death (Bidle et al, 2007), and therefore will determine the fate of the viral-infected blooms and influence the cycling of nutrients and carbon within microbial food webs in the marine ecosystem. We propose using this unique set of cellular markers as a novel tool to assess viral infection at different phases of algal blooms in the ocean.…”

Section: Modulation Of Host Ros Metabolismmentioning

confidence: 99%

“…This pathway was recently shown to have a critical role in EhV replication and in induction of E. huxleyi programmed cell death in cultures and during natural bloom demise (Pagarete et al, 2009;Vardi et al, 2009Vardi et al, , 2012. The viral-induced programmed cell death includes membrane blebbing, induction of caspase-like activity, expression of metacaspases and accumulation of reactive oxygen species (ROS) and specific viral-derived glycosphingolipids (Evans et al, 2006;Bidle et al, 2007;Vardi et al, 2009Vardi et al, , 2012. Nonetheless, the cellular signaling and infection mechanisms during the interaction of E. huxleyi with its specific virus are poorly understood.…”

Section: Introductionmentioning

confidence: 99%

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Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

et al. 2016

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The cosmopolitan coccolithophore Emiliania huxleyi is a unicellular eukaryotic alga responsible for vast blooms in the ocean. These blooms have immense impact on large biogeochemical cycles and are terminated by a specific large double-stranded DNA E. huxleyi virus (EhV, Phycodnaviridae). EhV infection is accompanied by induction of hallmarks of programmed cell death and production of reactive oxygen species (ROS). Here we characterized alterations in ROS metabolism and explored its role during infection. Transcriptomic analysis of ROS-related genes predicted an increase in glutathione (GSH) and H 2 O 2 production during infection. In accordance, using biochemical assays and specific fluorescent probes we demonstrated the overproduction of GSH during lytic infection. We also showed that H 2 O 2 production, rather than superoxide, is the predominant ROS during the onset of the lytic phase of infection. Using flow cytometry, confocal microscopy and multispectral imaging flow cytometry, we showed that the profound co-production of H 2 O 2 and GSH occurred in the same subpopulation of cells but at different subcellular localization. Positively stained cells for GSH and H 2 O 2 were highly infected compared with negatively stained cells. Inhibition of ROS production by application of a peroxidase inhibitor or an H 2 O 2 scavenger inhibited host cell death and reduced viral production. We conclude that viral infection induced remodeling of the host antioxidant network that is essential for a successful viral replication cycle. This study provides insight into viral replication strategy and suggests the use of specific cellular markers to identify and quantify the extent of active viral infection during E. huxleyi blooms in the ocean.

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Section: Discussionmentioning

confidence: 99%

Section: Modulation Of Host Ros Metabolismmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

et al. 2016

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“…This result can be explained by the programmed cell death (PCD) theory (Ross et al, 2006), which can induce the rapid collapse of algae (Kaneko et al, 2007;Frangeul et al, 2008). PCD can be caused by oxidative stress, ultraviolet irradiation, nutrient deprivation, salt stress, and heat (Bidle and Falkowski, 2004;Bidle et al, 2007), and finally lead the cells to perform genetically controlled cell suicide (Ameisen, 2002). Oxidative stress to cyanobacterial cells can be induced by chemical oxidants and cause PCD of cyanobacterial cells (Ding et al, 2012;Mikula et al, 2012).…”

Section: Effects Of Simulated Transportation Time On Cell Integrity Amentioning

confidence: 99%

Prechlorination of algae-laden water: The effects of transportation time on cell integrity, algal organic matter release, and chlorinated disinfection byproduct formation

Lan

Liu

et al. 2016

Water Research

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a b s t r a c tThe prechlorination-induced algal organic matter (AOM) released from Microcystis aeruginosa (M. aeruginosa) cells has been reported to serve as a source of precursors for chlorinated disinfection byproducts (DBPs). However, previous studies have mainly focused on the precursors either extracted directly from the cell suspension or derived immediately after algal suspension prechlorination. This study aims to investigate the impacts of water transportation time after algal suspension prechlorination on cell integrity, AOM release, and DBP formation during the dissolved phase chlorination. The damage to cell integrity after prechlorination was indicated to depend not only on chlorine dose but also on transportation time. The highest dissolved organic carbon (DOC) and dissolved organic nitrogen (DON) values were observed at 2 mg/L chlorine preoxidation before transportation, but were obtained at 0.4 mg/L chlorine after 480-min simulated transportation. The variation of DON with transportation time was indicated to be mainly influenced by the small molecular weight nitrogenous organic compounds, such as amino acids. Additionally, formation of the corresponding chlorinated carbonaceous disinfection byproducts (C-DBPs) and nitrogenous disinfection byproducts (N-DBPs) during the dissolved phase chlorination showed the same variation tendency as DOC and DON respectively. The highest C-DBP (98.4 mg/L) and N-DBP (5.5 mg/L) values were obtained at 0.4 mg/L chlorine preoxidation after 480-min simulated transportation. Therefore, when prechlorination is applied for algae-laden water pretreatment, not only chlorine dose but also transportation time needs to be considered with regard to their effects on cell integrity, AOM release, and chlorinated DBP formation.

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“…Despite these recent efforts to characterize the EhV sphingolipid biosynthesis genes, their function in the virus replication cycle remains unknown. Based on the role of ceramide as an inducer of cell death in mammalian and yeast cells (Susin et al 1997;Siskind 2005;Guenther et al 2008), several investigators proposed that the viral sphingolipid/ceramide pathway may activate host cell death, thus helping disseminate newly generated virions in the host population (Wilson et al 2005;Bidle et al 2007).…”

mentioning

confidence: 99%

Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus

Monier¹,

Pagarete²,

Vargas³

et al. 2009

Genome Res.

151

131

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International audienceInteractions between viruses and phytoplankton, the main primary producers in the oceans, affect global biogeochemical cycles and climate. Recent studies are increasingly revealing possible cases of gene transfers between cyanobacteria and phages, which might have played significant roles in the evolution of cyanobacteria/phage systems. However, little has been documented about the occurrence of horizontal gene transfer in eukaryotic phytoplankton/virus systems. Here we report phylogenetic evidence for the transfer of seven genes involved in the sphingolipid biosynthesis pathway between the cosmopolitan eukaryotic microalga Emiliania huxleyi and its large DNA virus EhV. PCR assays indicate that these genes are prevalent in E. huxleyi and EhV strains isolated from different geographic locations. Patterns of protein and gene sequence conservation support that these genes are functional in both E. huxleyi and EhV. This is the first clear case of horizontal gene transfer of multiple functionally linked enzymes in a eukaryotic phytoplankton-virus system. We examine arguments for the possible direction of the gene transfer. The virus-to-host direction suggests the existence of ancient viruses that controlled the complex metabolic pathway in order to infect primitive eukaryotic cells. In contrast, the host-to-virus direction suggests that the serial acquisition of genes involved in the same metabolic pathway might have been a strategy for the ancestor of EhVs to stay ahead of their closest relatives in the great evolutionary race for survival

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Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi

Abstract: algal blooms ͉ programmed cell death

Cited by 166 publications

References 40 publications

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

Prechlorination of algae-laden water: The effects of transportation time on cell integrity, algal organic matter release, and chlorinated disinfection byproduct formation

Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus

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