Abstract

The endoparasitic dinoflagellate Amoebophrya infects a number of marine dinoflagellates, including toxic and harmful algal bloom-forming species. The parasite kills its host and has been proposed to be a determining factor in the demise of dinoflagellate blooms in restricted coastal waters. Previous studies have mainly focused on the occurrence, prevalence, and diversity of Amoebophrya, while the interactions between the parasite and its host have received limited attention. Herein, an Amoebophrya sp.-Akashiwo sanguinea co-culture was established from Chinese coastal waters, and morphological, physiological, and transcriptional changes throughout an infection cycle of the parasite were systemically studied. The parasitic dinoflagellate was very infectious, resulting in an infection rate up to 85.83% at a dinospore:host ratio of 10:1. Infected host cells died eventually and released approximately 370 dinospores/cell. The host nuclear structures were rapidly degraded by Amoebophrya infection, and the chloroplasts of parasitized host cells remained intact until the parasite filled the almost entire cell structure. Nevertheless, infected cultures showed sustained but lower levels of photosynthetic performance (∼64% of control cultures), and the photosynthesis-related genes were significantly down-regulated. These findings provide a better understanding of the biological basis of the complex parasite-host interactions, which will be helpful to further elucidate the ecological significance of parasitic dinoflagellates in marine ecosystems.

Highlights

  • Marine dinoflagellates represent a key component of marine ecosystems

  • Species of Amoebophrya have a relatively simple life cycle consisting of a free-swimming infective dinospore that attaches to the host and penetrates the host cell membrane, an endoparasitic trophont grows inside the host cell by completely digesting the cell contents, and a multinucleate flagellated vermiform is released upon death of the host and divides into hundreds of infectious dinospores (Cachon, 1964; Coats and Bockstahler, 1994; Chambouvet et al, 2008)

  • The parasitic dinoflagellate Amoebophrya infects a wide range of marine dinoflagellates and is closely associated with succession of harmful algal blooms (Taylor, 1968; Coats, 1999; Chambouvet et al, 2008; Mazzillo et al, 2011), leading to growing interest between the parasite and its dinoflagellate hosts

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Summary

Introduction

Marine dinoflagellates represent a key component of marine ecosystems. Besides being major contributors of primary production, dinoflagellates possess a variety of other life and feeding strategies, including osmotrophy, phagotrophy, mixotrophy, symbiosis, and parasitism (Taylor, 1987; Fensome et al, 1996), thereby playing complicated ecological roles in the marineAmoebophrya Infection in Planktonic Dinoflagellate environment. The parasitic dinoflagellates of the family Amoebophryidae, the major component of the order Syndiniales or marine Alveolate group II, are known to infect a wide range of unicellular planktonic organisms, and have been associated with the demise of harmful algal blooms (Mazzillo et al, 2011; Lima-Mendez et al, 2015). The latest molecular approaches have revealed enormous diversity and abundance of Amoebophryidae organisms in the global plankton interactome (Guillou et al, 2008; Chambouvet et al, 2011b; de Vargas et al, 2015; Lima-Mendez et al, 2015; Chen et al, 2019; Cai et al, 2020), and stimulated attention on the biological characteristics and ecological significance of the parasitic dinoflagellates

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