Dinoflagellate Host Chloroplasts and Mitochondria Remain Functional During Amoebophrya Infection.

Ehsan Kayal,Estelle Bigeard,Lourdes Velo-Suarez,Joanne Monjol,Betina M Porcel,Christophe Six,Benjamin Noel,Jeremy Szymczak,Catharina Alves-De-Souza,Erwan Corre,Sarah Farhat,Dominique Marie,Laure Guillou

doi:10.3389/fmicb.2020.600823

Abstract

Dinoflagellates are major components of phytoplankton that play critical roles in many microbial food webs, many of them being hosts of countless intracellular parasites. The phototrophic dinoflagellate Scrippsiella acuminata (Dinophyceae) can be infected by the microeukaryotic parasitoids Amoebophrya spp. (Syndiniales), some of which primarily target and digest the host nucleus. Early digestion of the nucleus at the beginning of the infection is expected to greatly impact the host metabolism, inducing the knockout of the organellar machineries that highly depend upon nuclear gene expression, such as the mitochondrial OXPHOS pathway and the plastid photosynthetic carbon fixation. However, previous studies have reported that chloroplasts remain functional in swimming host cells infected by Amoebophrya. We report here a multi-approach monitoring study of S. acuminata organelles over a complete infection cycle by nucleus-targeting Amoebophrya sp. strain A120. Our results show sustained and efficient photosystem II activity as a hallmark of functional chloroplast throughout the infection period despite the complete digestion of the host nucleus. We also report the importance played by light on parasite production, i.e., the amount of host biomass converted to parasite infective propagules. Using a differential gene expression analysis, we observed an apparent increase of all 3 mitochondrial and 9 out of the 11 plastidial genes involved in the electron transport chains (ETC) of the respiration pathways during the first stages of the infection. The longer resilience of organellar genes compared to those encoded by the nucleus suggests that both mitochondria and chloroplasts remain functional throughout most of the infection. This extended organelle functionality, along with higher parasite production under light conditions, suggests that host bioenergetic organelles likely benefit the parasite Amoebophrya sp. A120 and improve its fitness during the intracellular infective stage.

Highlights

Many parasites infecting unicellular eukaryotes are necrotrophs, i.e., they kill their host before digesting them
We assembled a reference transcriptome for the host that contained 322,673 transcripts and 400,339 Transdecoderpredicted peptides, with 105,075 of the latter having GO-term annotations. By screening both the host T0 transcriptome and predicted proteome, we identified key genes involved in the electron transfer chains (ETC) of the mitochondrial oxidative phosphorylation (OXPHOS) pathway (Supplementary Figure S3 and Supplementary Table S1) and the chloroplastidial thylakoidal light phase of photosynthesis (Supplementary Figure S4 and Supplementary Table S2)
Our result show that the absence of light during the infection had no effect on the duration of the internal development nor the prevalence of the parasite

Summary

Introduction

Many parasites infecting unicellular eukaryotes are necrotrophs, i.e., they kill their host before digesting them. Dinoflagellate cells infected by Amoebophrya spp. maintain a degenerating but steady swimming behavior until the release of dinospores. The decline in the swimming speed of the infected dinoflagellate host has been linked to lower energy availability, likely resulting from the disruption of cellular functions (Park et al, 2002b). It is not clear whether this lower energy availability is the result of the degradation of the cell-machinery (following the consumption of the host cell) and/or the concomitant energy uptake by the developing parasite

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Results

Conclusion