Probing molecular processes regulating the dormancy of dinoflagellate resting cysts buried in marine sediments

Ying Zhong Tang¹*，Yunyan Deng¹, Senjie Lin^2
1CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China.
²Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA.
*Corresponding author. Email: yingzhong.tang@qdio.ac. cn

While resting cyst of dinoflagellates has been well-known as a significant life cycle stage and to play pivotal roles in the ecology of HABs, how the molecular machinery operates during cyst dormancy in sediments is virtually unexplored. We used the dinoflagellates-specific DinoSL coupled with SMRT sequencing to analyze metatranscriptomes of sediment-buried dinoflagellate cyst assemblages. We retrieved 159,431 non-redundant full-length transcripts, which were assigned to dinoflagellates in functional annotation, with most major metabolic and regulatory pathways being well represented in the metatranscriptomes, except for photosynthesis pathway. The active metabolic pathways included energy generation, autophagy, phytohormone signaling, and others. These results demonstrated the cruciality of broad active metabolic pathways for sustaining the viability and germination potential of cysts. To gain further insights, we used the tractable cyst-producing Scrippsiella acuminata as a representative for gene expression and enzyme activity analyses. Compared to vegetative cells, the expressions of 8 autophagy-related genes (ATGs) and a phytohormone gibberellin (GA) inactivation gene and lysosome/autolysosome activity were significantly up-regulated in cysts, whereas the expressions of two GA biosynthesis-related genes were down-regulated along with the extension of cyst dormancy. Additionally, extracellularly-added ABA and GA regulated antagonistically cyst germination. These results suggest vital roles of autophagy for energy generation and nutrient recycling in cysts and ABA/GA for modulating cysts dormancy and germination. This study generates the first transcriptomic dataset for natural cyst assemblages and sheds light on the molecular mechanism for dormancy maintenance and generation modulation, setting a necessary stepping-stone for elucidating the molecular machinery regulating dinoflagellate resting cysts’ dormancy.

Keywords: Autophagy; Dinoflagellate Resting cysts; Phytohormones

Funding: This work was supported by the Key Deployment Project of the Centre for Ocean Mega-Research of Science, Chinese Academy of Sciences (Grant No. COMS2019Q09), the National Science Foundation of China (Grant No. 42176207).