Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

Saijun Peng; Lijing Ye; Yongxue Li; Fanghan Wang; Tingting Sun; Lei Wang; Jianmin Zhao; Zhijun Dong

doi:10.1093/ismeco/ycae036

Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

ISME Commun. 2024 Mar 15;4(1):ycae036. doi: 10.1093/ismeco/ycae036. eCollection 2024 Jan.

Authors

Saijun Peng^{1

2}, Lijing Ye¹, Yongxue Li^{1

2}, Fanghan Wang^{1

2}, Tingting Sun¹, Lei Wang¹, Jianmin Zhao^{1

2}, Zhijun Dong^{1

2}

Affiliations

¹ Muping Coastal Environment Research Station, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, Shandong 264003, China.
² University of Chinese Academy of Sciences, Beijing 100049, China.

Abstract

Host-associated microbiomes can play key roles in the metamorphosis of animals. Most scyphozoan jellyfish undergo strobilation in their life cycles, similar to metamorphosis in classic bilaterians. The exploration of jellyfish microbiomes may elucidate the ancestral mechanisms and evolutionary trajectories of metazoan-microbe associations and interactions during metamorphosis. However, current knowledge of the functional features of jellyfish microbiomes remains limited. Here, we performed a genome-centric analysis of associated microbiota across four successive life stages (polyp, early strobila, advanced strobila, and ephyra) during strobilation in the common jellyfish Aurelia coerulea. We observed shifts in taxonomic and functional diversity of microbiomes across distinct stages and proposed that the low microbial diversity in ephyra stage may be correlated with the high expression of the host-derived antimicrobial peptide aurelin. Furthermore, we recovered 43 high-quality metagenome-assembled genomes and determined the nutritional potential of the dominant Vibrio members. Interestingly, we observed increased abundances of genes related to the biosynthesis of amino acids, vitamins, and cofactors, as well as carbon fixation during the loss of host feeding ability, indicating the functional potential of Aurelia-associated microbiota to support the synthesis of essential nutrients. We also identified several potential mechanisms by which jellyfish-associated microbes establish stage-specific community structures and maintain stable colonization in dynamic host environments, including eukaryotic-like protein production, bacterial secretion systems, restriction-modification systems, and clustered regularly interspaced short palindromic repeats-Cas systems. Our study characterizes unique taxonomic and functional changes in jellyfish microbiomes during strobilation and provides foundations for uncovering the ancestral mechanism of host-microbe interactions during metamorphosis.

Keywords: jellyfish blooms; metagenome; metamorphosis; microbiome; symbioses.