Research Article: Unmasking cellular response of a bloom-forming alga to viral infection by resolving expression profiles at a single-cell level

Date Published: April 24, 2019

Publisher: Public Library of Science

Author(s): Shilo Rosenwasser, Uri Sheyn, Miguel J. Frada, David Pilzer, Ron Rotkopf, Assaf Vardi, Nigel Harry Grimsley.


Infection by large dsDNA viruses can lead to a profound alteration of host transcriptome and metabolome in order to provide essential building blocks to support the high metabolic demand for viral assembly and egress. Host response to viral infection can typically lead to diverse phenotypic outcome that include shift in host life cycle and activation of anti-viral defense response. Nevertheless, there is a major bottleneck to discern between viral hijacking strategies and host defense responses when averaging bulk population response. Here we study the interaction between Emiliania huxleyi, a bloom-forming alga, and its specific virus (EhV), an ecologically important host-virus model system in the ocean. We quantified host and virus gene expression on a single-cell resolution during the course of infection, using automatic microfluidic setup that captures individual algal cells and multiplex quantitate PCR. We revealed high heterogeneity in viral gene expression among individual cells. Simultaneous measurements of expression profiles of host and virus genes at a single-cell level allowed mapping of infected cells into newly defined infection states and allowed detection specific host response in a subpopulation of infected cell which otherwise masked by the majority of the infected population. Intriguingly, resistant cells emerged during viral infection, showed unique expression profiles of metabolic genes which can provide the basis for discerning between viral resistant and susceptible cells within heterogeneous populations in the marine environment. We propose that resolving host-virus arms race at a single-cell level will provide important mechanistic insights into viral life cycles and will uncover host defense strategies.

Partial Text

Marine viruses are recognized as major ecological and evolutionary drivers and have immense impact on the community structure and the flow of nutrients through marine microbial food webs [1–5]. The cosmopolitan coccolithophore Emiliania huxleyi (Prymnesiophyceae, Haptophyta) is a widespread unicellular eukaryotic alga, responsible for large oceanic blooms [6, 7]. Its intricate calcite exoskeleton accounts for ~1/3 of the total marine CaCO3 production [8]. E. huxleyi is also a key producer of dimethyl sulfide [9], a bioactive gas with a significant climate-regulating role that seemingly enhances cloud formation [10]. Therefore, the fate of these blooms may have a critical impact on carbon and sulfur biogeochemical cycles. E. huxleyi spring blooms are frequently terminated as a consequence of infection by a specific large dsDNA virus (E. huxleyi virus, EhV) [11, 12]. The availability of genomic and transcriptomic data and a suite of host isolates with a range of susceptibilities to various EhV strains, makes the E. huxleyi-EhV a trackable host-pathogen model system with important ecological significance [13–20].




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