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

ABSTRACT: Lytic viral infection and programmed cell death (PCD) are thought to represent two distinct death mechanisms in phytoplankton, unicellular photoautotrophs that drift with ocean currents. Here, we demonstrate an interaction between autocatalytic PCD and lytic viral infection in the cosmopolitan coccolithophorid, Emiliania huxleyi. Successful infection of E. huxleyi strain 374 with a lytic virus, EhV1, resulted in rapid internal degradation of cellular components, a dramatic reduction in the photosynthetic efficiency (F(v)/F(m)), and an up-regulation of metacaspase protein expression, concomitant with induction of caspase-like activity. Caspase activation was confirmed through in vitro cleavage in cell extracts of the fluorogenic peptide substrate, IETD-AFC, and direct, in vivo staining of cells with the fluorescently labeled irreversible caspase inhibitor, FITC-VAD-FMK. Direct addition of z-VAD-FMK to infected cultures abolished cellular caspase activity and protein expression and severely impaired viral production. The absence of metacaspase protein expression in resistant E. huxleyi strain 373 during EhV1 infection further demonstrated the critical role of these proteases in facilitating viral lysis. Together with the presence of caspase cleavage recognition sequences within virally encoded proteins, we provide experimental evidence that coccolithoviruses induce and actively recruit host metacaspases as part of their replication strategy. These findings reveal a critical role for metacaspases in the turnover of phytoplankton biomass upon infection with viruses and point to coevolution of host-virus interactions in the activation and maintenance of these enzymes in planktonic, unicellular protists.

SUBMITTER: Bidle KD

PROVIDER: S-EPMC1838821 | biostudies-literature | 2007 Apr

REPOSITORIES: biostudies-literature

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

Bidle Kay D KD Haramaty Liti L Barcelos E Ramos Joana J Falkowski Paul P

Proceedings of the National Academy of Sciences of the United States of America 20070328 14

Lytic viral infection and programmed cell death (PCD) are thought to represent two distinct death mechanisms in phytoplankton, unicellular photoautotrophs that drift with ocean currents. Here, we demonstrate an interaction between autocatalytic PCD and lytic viral infection in the cosmopolitan coccolithophorid, Emiliania huxleyi. Successful infection of E. huxleyi strain 374 with a lytic virus, EhV1, resulted in rapid internal degradation of cellular components, a dramatic reduction in the photo ...[more]

PMID: 17392426

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Project description:The species concept in marine phytoplankton is defined based on genomic, morphological, and functional properties. Reports of intraspecific diversity are widespread across major phytoplankton groups but the impacts of this variation on ecological and biogeochemical processes are often overlooked. Intraspecific diversity is well known within coccolithophores, which play an important role in the marine carbon cycle via production of particulate inorganic carbon. In this study, we investigated strain-specific responses to temperature in terms of morphology, carbon production, and carbonate mineralogy using a combination of microscopy, elemental analysis, flow cytometry, and nuclear magnetic resonance. Two strains of the cosmopolitan coccolithophore E. huxleyi isolated from different regions (subtropical, CCMP371; temperate, CCMP3266) were cultured under a range of temperature conditions (10°C, 15°C, and 20°C) using batch cultures and sampled during both exponential and stationary growth. Results for both strains showed that growth rates decreased at lower temperatures while coccosphere size increased. Between 15°C and 20°C, both strains produced similar amounts of total carbon, but differed in allocation of that carbon between particulate inorganic carbon (PIC) and particulate organic carbon (POC), though temperature effects were not detected. Between 10°C and 20°C, temperature effects on daily production of PIC and POC, as well as the cellular quota of POC were detected in CCMP3266. Strain-specific differences in coccolith shedding rates were found during exponential growth. In addition, daily shedding rates were negatively related to temperature in CCMP371 but not in CCMP3266. Despite differences in rates of particulate inorganic carbon production, both strains were found to produce coccoliths composed entirely of pure calcite, as established by solid-state 13C and 43Ca NMR and X-ray diffraction measurements. These results highlight the limitations of the species concept and the need for a trait-based system to better quantify diversity within marine phytoplankton communities.

Dataset Information

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

Publications

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

Similar Datasets

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