Microbial degradation of jellyfish detritus promotes phytoplankton growth in coastal marine ecosystem

Gelatinous zooplankton or 'jellyfish' are present in large numbers in diverse marine ecosystems and, due to their metabolic features and life history traits, some species are capable of generating massive blooms. These blooms often collapse en masse, releasing large quantities of labile proteinaceous organic matter (jelly-OM) that is potentially readily available for microbial degradation in the water column. To test the microbial response to jelly-OM, we simulated, in a two-stage microcosm experiment, the scenario experienced by the coastal pelagic microbiome during a bloom of the invasive ctenophore Mnemiopsis leiydi. In the first stage of our experiment, jelly-OM supported rapid growth of opportunistic bacteria. The jelly-OM degradation was mostly associated with enhanced leucine aminopeptidase, several glycosyl hydrolases and alkaline phosphatase activity and resulted in the accumulation of inorganic nutrients (particularly ammonium). Accordingly, functional annotations of metagenomes recruited from the first stage of our experiment revealed enhanced microbial metabolism of amino acids, lipids and carbohydrates in jelly-OM treatments. In stage two of the experiment, we incubated the processed jelly-OM (i.e., 0.2 µm filtered end-product of microbial processing in stage one) with a fresh microbial plankton assemblage. After 3 days, we observed a significant increase in primary production and phytoplankton biomass, reaching values similar to those observed in situ during seasonal phytoplankton peaks in the region. Observed growth of the phytoplankton community, dominated by diatoms, was likely supported by accumulated ammonia. At the same time, shift in bacterial community composition towards bacterial taxa regularly associated with phytoplankton blooms was observed. Changes in organic matter pool quality and quantity also triggered different metabolic pathways in bacterial communities, in particular those associated with metabolizing carbohydrates. In situ measurements revealed that jellyfish and phytoplankton may be coupled through rapid degradation of jelly-OM by pelagic heterotrophic bacteria. Thus, jellyfish blooms seem to represent a significant source of not only OM but also inorganic nutrients, and may induce major perturbations to ecosystems (e.g., by boosting phytoplankton growth). Considering that gelatinous zooplankton are expected to thrive under projected future changes and increased exploitation of the ocean, our results highlight the necessity to include jellyfish carbon budgets in biogeochemical models of the ocean.