Jellyfish detritus supports niche partitioning and metabolic interactions among marine bacteria

Abstract

Abstract Background Jellyfish blooms represent a significant but largely overlooked source of labile organic matter (jelly-OM) in the ocean, characterized by a high protein content. Decaying jellyfish are important vehicles for carbon export to the ocean’s interior. To accurately incorporate them into biogeochemical models, the interactions between microbes and jelly-OM have yet to be fully characterized. We conducted jelly-OM enrichment experiments to simulate the scenario experienced by the coastal microbiome after the decay of a jellyfish bloom. We combined metagenomics, endo- and exo-metaproteomic approaches to obtain a mechanistic understanding on the metabolic network operated by the jelly-OM degrading bacterial consortium. Results Our analysis revealed that OM released during the decay of jellyfish blooms triggers a rapid shuffling of the taxonomic and functional profile of the bacterial community, resulting in a significant enrichment of protein/amino-acid catabolism-related enzymes in the jelly-OM degrading community dominated by Pseudoalteromonadaceae, Alteromonadaceae and Vibrionaceae, compared to unamended control treatments. In accordance with the proteinaceous character of jelly-OM, Pseudoalteromonadaceae synthesized and excreted enzymes associated with proteolysis, while Alteromonadaceae contributed to extracellular hydrolysis of complex carbohydrates and organophosphorus compounds. In contrast, Vibrionaceae synthesized transporter proteins for peptides, amino acids and carbohydrates, exhibiting a cheater-type lifestyle. In the late stage of jelly-OM degradation, Rhodobacteraceae and Alteromonadaceae became dominant, growing on jelly-OM left-overs or bacterial debris, potentially contributing to the accumulation of dissolved organic nitrogen compounds and inorganic nutrients, following the decay of jellyfish blooms. Conclusions Our findings indicate that specific chemical and metabolic fingerprints associated with decaying jellyfish blooms are substantially different to those associated with decaying phytoplankton blooms, potentially altering the functioning and biogeochemistry of marine systems. In particular, the enrichment in extracellular collagenolytic proteases associated with the decay of jellyfish blooms represents an important aspect, with possible implications for marine ecosystem services as virulence factors in human and marine organisms’ disease. Our study also provides novel insights into niche partitioning and metabolic interactions among key jelly-OM degraders operating a complex metabolic network in a temporal cascade of biochemical reactions to degrade pulses of jellyfish-bloom specific compounds.