Virus infection of Haptolina ericina and Phaeocystis pouchetii implicates evolutionary conservation of programmed cell death induction in marine haptophyte-virus interactions.

Jessica L Ray,Helen F Fredricks,Ruth-Anne Sandaa,Benjamin A S Van Mooy,Aud Larsen,Liti Haramaty,Runar Thyrhaug,Kay D Bidle

doi:10.1093/plankt/fbu029

Abstract

The mechanisms by which phytoplankton cope with stressors in the marine environment are neither fully characterized nor understood. As viruses are the most abundant entities in the global ocean and represent a strong top-down regulator of phytoplankton abundance and diversity, we sought to characterize the cellular response of two marine haptophytes to virus infection in order to gain more knowledge about the nature and diversity of microalgal responses to this chronic biotic stressor. We infected laboratory cultures of the haptophytes Haptolina ericina and Phaeocystis pouchetii with CeV-01B or PpV-01B dsDNA viruses, respectively, and assessed the extent to which host cellular responses resemble programmed cell death (PCD) through the activation of diagnostic molecular and biochemical markers. Pronounced DNA fragmentation and activation of cysteine aspartate-specific proteases (caspases) were only detected in virus-infected cultures of these phytoplankton. Inhibition of host caspase activity by addition of the pan-caspase inhibitor z-VAD-fmk did not impair virus production in either host–virus system, differentiating it from the Emiliania huxleyi-Coccolithovirus model of haptophyte–virus interactions. Nonetheless, our findings point to a general conservation of PCD-like activation during virus infection in ecologically diverse haptophytes, with the subtle heterogeneity of cell death biochemical responses possibly exerting differential regulation on phytoplankton abundance and diversity.

Highlights

Marine phytoplankton account for a large proportion ( 50%) of global primary production and have a strong influence on global nutrient cycling (Field et al, 1998)
Our investigation of host–virus interactions in the H. ericina-CeV and P. pouchetii-PpV systems focused on the multi-faceted nature of programmed cell death (PCD), given its documented role in regulating the host–virus “arms race” in another haptophyte system (Bidle and Vardi, 2011)
Using classical PCD markers, including DNA fragmentation and induction of caspase-like proteolytic activity (Ameisen, 2002), we demonstrate that viral infection induces a PCD-like pathway in H. ericina and P. pouchetii

Summary

INTRODUCTION

Marine phytoplankton account for a large proportion ( 50%) of global primary production and have a strong influence on global nutrient cycling (Field et al, 1998). PCD-like markers such as chromatin condensation, reactive oxygen species (ROS) production and cysteine aspartate protease (caspase) activation have been observed during virus infection of other phytoplankton (Lawrence et al, 2001; Evans et al, 2006; Bidle et al, 2007) These markers are diagnostically associated with PCD in metazoans and other unicellular eukaryotic organisms (Ameisen, 2002; Bidle and Falkowski, 2004; Franklin et al, 2006; Bruchhaus et al, 2007). Lytic viruses infecting H. ericina (CeV-01B) (Sandaa et al, 2001) and P. pouchetii (PpV-01B) (Jacobsen et al, 1996) have been isolated from Norwegian coastal waters and are well studied in laboratory cultures These haptophyte–virus systems provided a unique opportunity to assess the expression of PCD-like traits during virus infection in these haptophytes, and thereby contribute to the greater body of knowledge concerning haptophyte–virus interactions in the marine environment

METHOD

Findings

DISCUSSION