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Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean.
ISME J. 2016 07; 10(7):1742-54.IJ

Abstract

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 H2O2 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 H2O2 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 H2O2 and GSH occurred in the same subpopulation of cells but at different subcellular localization. Positively stained cells for GSH and H2O2 were highly infected compared with negatively stained cells. Inhibition of ROS production by application of a peroxidase inhibitor or an H2O2 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.

Authors+Show Affiliations

Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.Department of Biological Services, Weizmann Institute of Science, Rehovot, Israel.Department of Biological Services, Weizmann Institute of Science, Rehovot, Israel.Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

26784355

Citation

Sheyn, Uri, et al. "Modulation of Host ROS Metabolism Is Essential for Viral Infection of a Bloom-forming Coccolithophore in the Ocean." The ISME Journal, vol. 10, no. 7, 2016, pp. 1742-54.
Sheyn U, Rosenwasser S, Ben-Dor S, et al. Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J. 2016;10(7):1742-54.
Sheyn, U., Rosenwasser, S., Ben-Dor, S., Porat, Z., & Vardi, A. (2016). Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. The ISME Journal, 10(7), 1742-54. https://doi.org/10.1038/ismej.2015.228
Sheyn U, et al. Modulation of Host ROS Metabolism Is Essential for Viral Infection of a Bloom-forming Coccolithophore in the Ocean. ISME J. 2016;10(7):1742-54. PubMed PMID: 26784355.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. AU - Sheyn,Uri, AU - Rosenwasser,Shilo, AU - Ben-Dor,Shifra, AU - Porat,Ziv, AU - Vardi,Assaf, Y1 - 2016/01/19/ PY - 2014/10/26/received PY - 2014/10/13/revised PY - 2015/11/06/accepted PY - 2016/1/20/entrez PY - 2016/1/20/pubmed PY - 2017/9/28/medline SP - 1742 EP - 54 JF - The ISME journal JO - ISME J VL - 10 IS - 7 N2 - 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 H2O2 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 H2O2 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 H2O2 and GSH occurred in the same subpopulation of cells but at different subcellular localization. Positively stained cells for GSH and H2O2 were highly infected compared with negatively stained cells. Inhibition of ROS production by application of a peroxidase inhibitor or an H2O2 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. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/26784355/Modulation_of_host_ROS_metabolism_is_essential_for_viral_infection_of_a_bloom_forming_coccolithophore_in_the_ocean_ L2 - https://doi.org/10.1038/ismej.2015.228 DB - PRIME DP - Unbound Medicine ER -