Microbiota regulates life-cycle transition and nematocyte dynamics in jellyfish

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

doi:10.1016/j.isci.2023.108444

Cited by 2 publications

(7 citation statements)

References 65 publications

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“…It has the unique advantages of a typical diphasic life cycle (sessile benthic phase and free-living pelagic phase), well-established laboratory culture methods, and easy access to samples. The necessity of robust microbial communities for the strobilation process has been confirmed in previous studies of the common moon jellyfish A. aurita and A. coerulea , with microbes functioning as promoters of strobilation initiation and regulators of host fitness [ 6 , 27 , 28 ]. In this study, a sterile culture environment was set up to eliminate the interference of opportunistic environmental microbes, making it more likely to reveal the core mechanism of microbial action in the ancient metamorphosis process.…”

Section: Introductionmentioning

confidence: 77%

“…The methods for generation of sterile Artemia nauplii are described by Peng et al . [ 6 ] with minor modifications. Briefly, Artemia salina cysts were hydrated at room temperature for 1 h and then bleached with sodium hypochlorite and NaOH solution to obtain naked cysts.…”

Section: Methodsmentioning

confidence: 99%

“…We identified a gene that expresses an antimicrobial peptide (aurelin) from our previous RNA-seq data set representing the transcriptomes of four life stages (polyp, early strobila, advanced strobila, and ephyra) during the strobilation of A. coerulea (NCBI accession number: PRJNA1013748) [ 6 ]. This previous study and the present study used the same batch of polyps and set the same culture conditions; thus the transcriptomic results meet the premise of combined analysis with the microbiome data in this study.…”

Section: Methodsmentioning

confidence: 99%

“…This previous study and the present study used the same batch of polyps and set the same culture conditions; thus the transcriptomic results meet the premise of combined analysis with the microbiome data in this study. For technical details on the transcriptomic sequencing and differentially expressed gene analysis, see reference [ 6 ].…”

Section: Methodsmentioning

confidence: 99%

“…lifestyle transformation from benthic to planktonic) is one of the factors driving diversification and prosperity of scyphozoans, which have been reported to form periodic blooms in many sea areas worldwide [ 17–19 ]. The life-stage-specific diversity of associated microbiota has been uncovered in scyphozoans Aurelia aurita [ 20 ], Aurelia coerulea [ 6 , 21 ], Cyanea lamarckii [ 22 ], Chrysaora plocamia [ 23 ], and Chrysaora hysoscella [ 22 ]. However, the typical marker gene (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

Peng,

Ye,

et al. 2024

ISME Communications

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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 colonisation 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 characterises unique taxonomic and functional changes in jellyfish microbiomes during strobilation and provides foundations for uncovering the ancestral mechanism of host–microbe interactions during metamorphosis.

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Section: Introductionmentioning

confidence: 77%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

Peng,

Ye,

et al. 2024

ISME Communications

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Microbial Diversity and Screening for Potential Pathogens and Beneficial Bacteria of Five Jellyfish Species-Associated Microorganisms Based on 16S rRNA Sequencing

Li,

Zhu,

et al. 2024

Polish Journal of Microbiology

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Jellyfish, microorganisms, and the marine environment collectively shape a complex ecosystem. This study aimed to analyze the microbial communities associated with five jellyfish species, exploring their composition, diversity, and relationships. Microbial diversity among the species was assessed using 16S rRNA gene sequencing and QIIME analysis. Significant differences in bacterial composition were found, with distinct dominant taxa in each species: Mycoplasmataceae (99.21%) in Aurelia coerulea, Sphingomonadaceae (22.81%) in Cassiopea andromeda, Alphaproteobacteria_unclassified (family level) (64.09%) in Chrysaora quinquecirrha, Parcubacteria_unclassified (family level) (93.11%) in Phacellophora camtschatica, and Chlamydiaceae (35.05%) and Alphaproteobacteria_unclassified (family level) (38.73%) in Rhopilema esculentum. C. andromeda showed the highest diversity, while A. coerulea exhibited the lowest. Correlations among dominant genera varied, including a positive correlation between Parcubacteria_unclassified (genus level) and Chlamydiaceae_unclassified (genus level). Genes were enriched in metabolic pathways and ABC transporters. The most abundant potential pathogens at the phylum level were Proteobacteria, Tenericutes, Chlamydiae, and Epsilonbacteraeota. The differing microbial compositions are likely influenced by species and their habitats. Interactions between jellyfish and microorganisms, as well as among microorganisms, showed interdependency or antagonism. Most microbial gene functions focused on metabolic pathways, warranting further study on the relationship between pathogenic bacteria and these pathways.

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Microbiota regulates life-cycle transition and nematocyte dynamics in jellyfish

Cited by 2 publications

References 65 publications

Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

Metagenomic insights into jellyfish-associated microbiome dynamics during strobilation

Microbial Diversity and Screening for Potential Pathogens and Beneficial Bacteria of Five Jellyfish Species-Associated Microorganisms Based on 16S rRNA Sequencing

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