Oyster transcriptome response to Alexandrium exposure is related to saxitoxin load and characterized by disrupted digestion, energy balance, and calcium and sodium signaling

• Published in: Aquatic toxicology 2018-06, Vol.199, p.127-137
• Main Authors: Mat, Audrey M., Klopp, Christophe, Payton, Laura, Jeziorski, Céline, Chalopin, Morgane, Amzil, Zouher, Tran, Damien, Wikfors, Gary H., Hégaret, Hélène, Soudant, Philippe, Huvet, Arnaud, Fabioux, Caroline
• Format: Article
• Language: English
• Subjects: Biodiversity and Ecology; Ecology, environment; Elastic-net regression; Environmental Sciences; Ions channels; Life Sciences; Paralytic shellfish toxins; Transcriptomic
• ISSN: 0166-445X; 1879-1514
• DOI: 10.1016/j.aquatox.2018.03.030

•A RNA-seq approach was used to study the global and without a priori response of oyster to the toxic Alexandrium minutum.•Toxin load was the main driver of transcriptomic variations.•A limited number of metabolic pathways in oysters covaried with PST load.•A correlation between PST load and transcript abundance described by only 70 of the ∼29,000 oyster genes was shown.•Association between toxin load, genotype, and mRNA level opens new doors to investigate PST inter-individual variability. Harmful Algal Blooms are worldwide occurrences that can cause poisoning in human seafood consumers as well as mortality and sublethal effets in wildlife, propagating economic losses. One of the most widespread toxigenic microalgal taxa is the dinoflagellate Genus Alexandrium, that includes species producing neurotoxins referred to as PST (Paralytic Shellfish Toxins). Blooms cause shellfish harvest restrictions to protect human consumers from accumulated toxins. Large inter-individual variability in toxin load within an exposed bivalve population complicates monitoring of shellfish toxicity for ecology and human health regulation. To decipher the physiological pathways involved in the bivalve response to PST, we explored the whole transcriptome of the digestive gland of the Pacific oyster Crassostrea gigas fed experimentally with a toxic Alexandrium minutum culture. The largest differences in transcript abundance were between oysters with contrasting toxin loads (1098 transcripts), rather than between exposed and non-exposed oysters (16 transcripts), emphasizing the importance of toxin load in oyster response to toxic dinoflagellates. Additionally, penalized regressions, innovative in this field, modeled accurately toxin load based upon only 70 transcripts. Transcriptomic differences between oysters with contrasting PST burdens revealed a limited suite of metabolic pathways affected, including ion channels, neuromuscular communication, and digestion, all of which are interconnected and linked to sodium and calcium exchanges. Carbohydrate metabolism, unconsidered previously in studies of harmful algal effects on shellfish, was also highlighted, suggesting energy challenge in oysters with high toxin loads. Associations between toxin load, genotype, and mRNA levels were revealed that open new doors for genetic studies identifying genetically-based low toxin accumulation.