Publication in mSystems

Bacterial degradation of ctenophore Mnemiopsis leidyi organic matter

Blooms of gelatinous zooplankton, an important source of protein-rich biomass in coastal waters, often collapse rapidly, releasing large amounts of labile detrital organic matter (OM) into the surrounding water. Although these blooms have the potential to cause major perturbations in the marine ecosystem, their effects on the microbial community and hence on the biogeochemical cycles have yet to be elucidated. We conducted microcosm experiments simulating the scenario experienced by coastal bacterial communities after the decay of a ctenophore (Mnemiopsis leidyi) bloom in the northern Adriatic Sea. Within 24 h, a rapid response of bacterial communities to the M. leidyi OM was observed, characterized by elevated bacterial biomass production and respiration rates. However, compared to our previous microcosm study of jellyfish (Aurelia aurita s.l.), M. leidyi OM degradation was characterized by significantly lower bacterial growth efficiency, meaning that the carbon stored in the OM was mostly respired. Combined metagenomic and metaproteomic analysis indicated that the degradation activity was mainly performed by Pseudoalteromonas, producing a large amount of proteolytic extracellular enzymes and exhibiting high metabolic activity. Interestingly, the reconstructed metagenome-assembled genome (MAG) of Pseudoalteromonas phenolica was almost identical (average nucleotide identity >99%) to the MAG previously reconstructed in our A. aurita microcosm study, despite the fundamental genetic and biochemical differences of the two gelatinous zooplankton species. Taken together, our data suggest that blooms of different gelatinous zooplankton are likely triggering a consistent response from natural bacterial communities, with specific bacterial lineages driving the remineralization of the gelatinous OM.