Stress-Induced Mucus Secretion and Its Composition by a Combination of Proteomics and Metabolomics of the Jellyfish Aurelia coerulea

Abstract

Background: Jellyfish respond quickly to external stress that stimulates mucus secretion as a defense. Neither the composition of secreted mucus nor the process of secretion are well understood. Methods: Aurelia coerulea jellyfish were stimulated by removing them from environmental seawater. Secreted mucus and tissue samples were then collected within 60 min, and analyzed by a combination of proteomics and metabolomics using liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) and ultra-performance liquid chromatography/quadrupole time-of-flight mass spectrometry (UPLC-QTOF-MS/MS), respectively. Results: Two phases of sample collection displayed a quick decrease in volume, followed by a gradual increase. A total of 2421 and 1208 proteins were identified in tissue homogenate and secreted mucus, respectively. Gene Ontology (GO) analysis showed that the mucus-enriched proteins are mainly located in extracellular or membrane-associated regions, while the tissue-enriched proteins are distributed throughout intracellular compartments. Tryptamine, among 16 different metabolites, increased with the largest-fold change value of 7.8 in mucus, which is consistent with its involvement in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway ‘tryptophan metabolism’. We identified 11 metalloproteinases, four serpins, three superoxide dismutases and three complements, and their presence was speculated to be related to self-protective defense. Conclusions: Our results provide a composition profile of proteins and metabolites in stress-induced mucus and tissue homogenate of A. coerulea. This provides insight for the ongoing endeavors to discover novel bioactive compounds. The large increase of tryptamine in mucus may indicate a strong stress response when jellyfish were taken out of seawater and the active self-protective components such as enzymes, serpins and complements potentially play a key role in innate immunity of jellyfish.

Barrel Jellyfish (Rhizostoma pulmo) as Source of Antioxidant Peptides

“…In our samples, the largest sub-fraction—i.e., containing peptides with high MW—most likely includes proteinaceous components of the jellyfish mucus, which was found to have MW higher than 40 kDa in various jellyfish species and other coelenterates [ 69 , 70 , 71 ]. In agreement with this hypothesis, the mucus fraction of the jellyfish Aurelia coerulea contained proteins falling within three MW ranges, i.e., 100–250 kDa, 50–100 kDa and 37–50 kDa, while the tissue proteins were dispersed in a wider range [ 71 ]. Interestingly, hydroalcoholic extracts of the zooxanthellate jellyfish Cotylorhiza tuberculata showed only low MW proteins ranging 10–14 kDa [ 10 ].…”

Cassiosomes are stinging-cell structures in the mucus of the upside-down jellyfish Cassiopea xamachana

“…Overall, the topic of jellyfish mucus is an understudied field, despite the ecological importance of mucus in antimicrobial and environmental stress protection and chemical defense 44,45 , relevance of toxic bioactive compounds found within venom 46,47 , and the potential importance to non-cnidarian taxa. Given the recent publication of the first reference genome for Cassiopea xamachana 14 , a thorough investigation into the molecular pathways underlying the development and release of cassiosomes and comparisons with nematocyst-enriched structures in other cnidarians (e.g., nematosomes, acontia and acrorhagi) can now be undertaken.…”

The importance of jellyfish–microbe interactions for biogeochemical cycles in the ocean

“…In addition, mucus has numerous other functions such as holding moisture, has antimicrobial properties and acting as adsorbent and surfactant (Bakshani et al 2018). Besides, large quantities of the neurotransmitter/neuromodulator tryptamine were found in mucus considered an indicator of stress (Liu et al 2018). In contrast to the biochemical composition of coral mucus, jellyfish mucus is largely unexplored.…”

“…1). While having a higher C : N molar ratio than the canonical Redfield ratio (6.6 : 1), the jellyfish excreta and mucus have lower molar N : P ratios (6.9–11.4) than the Redfield ratio (16 : 1) (Pitt et al 2009; Condon et al 2010; Liu et al 2018). Jellyfish mucus and excreta are composed of dissolved organic nitrogen (DON), dissolved free amino acids (AAs) and dissolved organic phosphorus, nucleosides, and purine compounds as well as inorganic nutrients, mainly ammonia (but not urea, as in the case of crustaceous zooplankton) and phosphate (Pitt et al 2009).…”

“…However, it has been suggested to resemble that of other cnidarians and thus is composed mostly of proteins, carbohydrates, and to a lesser extent of lipids (Ducklow and Mitchell 1979; Manzari et al 2015; Stabili et al 2015). A detailed proteomics and metabolomics study of jellyfish mucus identified more than 1000 proteins ranging from 37 to 250 kDa (Liu et al 2018). A self‐protective function of mucus proteins was related to the degradation of toxic compounds and/or pathogens (Liu et al 2018).…”