Transcriptomic insights into the shift of trophic strategies in mixotrophic dinoflagellate Lepidodinium in the warming ocean

Jiawei Chen; Lixia Deng; Mengwen Pang; Yingdong Li; Zhimeng Xu; Xiaodong Zhang; Hongbin Liu

doi:10.1093/ismeco/ycae087

Transcriptomic insights into the shift of trophic strategies in mixotrophic dinoflagellate Lepidodinium in the warming ocean

ISME Commun. 2024 Jun 19;4(1):ycae087. doi: 10.1093/ismeco/ycae087. eCollection 2024 Jan.

Authors

Jiawei Chen¹, Lixia Deng¹, Mengwen Pang¹, Yingdong Li², Zhimeng Xu¹, Xiaodong Zhang¹, Hongbin Liu^{1

3}

Affiliations

¹ Department of Ocean Science, Hong Kong University of Science and Technology, Hong Kong SAR, China.
² Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, China.
³ Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Hong Kong SAR, China.

Abstract

The shift between photoautotrophic and phagotrophic strategies in mixoplankton significantly impacts the planktonic food webs and biogeochemical cycling. Considering the projected global warming, studying how temperature impacts this shift is crucial. Here, we combined the transcriptome of in-lab cultures (mixotrophic dinoflagellate Lepidodinium sp.) and the metatranscriptome dataset of the global ocean to investigate the mechanisms underlying the shift of trophic strategies and its relationship with increasing temperatures. Our results showed that phagocytosis-related pathways, including focal adhesion, regulation of actin cytoskeleton, and oxidative phosphorylation, were significantly stimulated in Lepidodinium sp. when cryptophyte prey were added. We further compared the expression profiles of photosynthesis and phagocytosis genes in Lepidodinium sp. in the global sunlit ocean. Our results indicated that Lepidodinium sp. became more phagotrophic with increasing temperatures when the ambient chlorophyll concentration was >0.3 mg.m^-3 (~20.58% of the ocean surface) but became more photoautotrophic with increasing temperatures when the chlorophyll concentration was between 0.2 and 0.3 mg.m^-3 (~11.47% of the ocean surface). Overall, we emphasized the crucial role of phagocytosis in phago-mixotrophy and suggested that the expression profile of phagocytosis genes can be a molecular marker to target the phagotrophic activity of mixoplankton in situ.

Keywords: dinoflagellate; mixoplankton; phagocytosis; temperature; transcriptome.