Broad active metabolic pathways, autophagy, and antagonistic hormones regulate dinoflagellate cyst dormancy in marine sediments

This work aimed to reveal the molecular machinery regulating the dormancy of dinoflagellate resting cysts buried in marine sediments. Dinoflagellates play pivotal roles in marine ecosystems, particularly as major contributors of harmful algal blooms. Despite vital roles of cysts in blooming cycles and dinoflagellate ecology, the molecular processes controlling cyst dormancy have largely remained unexplored due to technological difficulties. Using DinoSL as a dinoflagellates-specific mRNA "hook" and SMRT sequencing, we analyzed metatranscriptomes of sediment-buried dinoflagellate cyst assemblages. The data show that most major metabolic and regulatory pathways, except photosynthesis, were transcriptionally active. This suggests the crucial importance of broad metabolic pathways in sustaining cyst viability and germination potential. Further expression analyses of 11 genes (relevant to autophagy and phytohormone gibberellin), lysosome/autolysosome staining, and germination experiments revealed vital roles of autophagy in energy generation, nutrient recycling, and of phytohormones abscisic acid/gibberellin in modulating dormancy/germination of resting cysts. Our findings lay a cornerstone for elucidating the molecular machinery regulating dinoflagellate cyst dormancy.