Remodeling of the cycling transcriptome of the oyster Crassostrea gigas by the harmful algae Alexandrium minutum

Laura Payton,Arnaud Huvet,Floriane Boullot,Damien Tran,Mohamedou Sow,Jean-Charles Massabuau,Mickael Perrigault,Hélène Hegaret,Caroline Fabioux,Claire Hoede

doi:10.1038/s41598-017-03797-4

Abstract

As a marine organism, the oyster Crassostrea gigas inhabits a complex biotope governed by interactions between the moon and the sun cycles. We used next-generation sequencing to investigate temporal regulation of oysters under light/dark entrainment and the impact of harmful algal exposure. We found that ≈6% of the gills’ transcriptome exhibits circadian expression, characterized by a nocturnal and bimodal pattern. Surprisingly, a higher number of ultradian transcripts were also detected under solely circadian entrainment. The results showed that a bloom of Alexandrium minutum generated a remodeling of the bivalve’s temporal structure, characterized by a loss of oscillations, a genesis of de novo oscillating transcripts, and a switch in the period of oscillations. These findings provide unprecedented insights into the diurnal landscape of the oyster’s transcriptome and pleiotropic remodeling due to toxic algae exposure, revealing the intrinsic plasticity of the cycling transcriptome in oysters.

Highlights

The physiological and behavioral processes of living organisms oscillate
To explore the effect of paralytic shellfish toxins (PSTs) ingestion, a second group of oysters was exposed to the PST-producing alga Alexandrium minutum (A.m condition), mimicking a harmful algal bloom (≈400 cells.mL−1)
Gills were sampled every 4 hr over 52 hr, and the cyclic transcriptome was analyzed by RNA sequencing (RNAseq) followed by ARSER41 to evaluate any significant cyclicity in the 20,846 transcripts

Summary

Introduction

The physiological and behavioral processes of living organisms oscillate. Temporal organization is a necessary adaptation to cope with an ecosystem governed by various periodic changes[1]. In the H.t oysters, 1300 (1247 + 53) significant circadian transcripts were identified, corresponding to 6.2% of total transcripts in the H.t gills (Fig. 1A–C; Supplementary Table S2). An increase in daytime peak expression with A. minutum exposure was observed in the 53 circadian transcripts common in both H.t and A.m (Fig. 1F).

Results

Conclusion