Bacterial degradation of ctenophoreMnemiopsis leidyiorganic matter

Abstract

AbstractBlooms 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 theM. leidyiOM was observed, characterized by elevated bacterial biomass production and respiration rates. Compared to our previous microcosm study of jellyfish (Aurelia aurita s.l.),M. leidyiOM degradation revealed that, despite the fundamental genetic and biochemical differences between the two species, a similar pattern in the bacterial community response was observed. Combined metagenomic and metaproteomic analysis indicated that the degradation activity was mainly performed byPseudoalteromonas, producing a large amount of proteolytic exoenzymes and exhibiting high metabolic activity. Interestingly, the reconstructed metagenome-assembled genome (MAG) ofPseudoalteromonas phenolicawas almost identical (average nucleotide identity >99%) to the MAG previously reconstructed in ourA. auritamicrocosm study. 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.ImportanceJellyfish blooms are increasingly becoming a recurring seasonal event in marine ecosystems, characterised by a rapid build-up of gelatinous biomass that collapses rapidly. Although these blooms have the potential to cause major perturbations, their impact on marine microbial communities is largely unknown. We conducted an incubation experiment simulating a bloom of the ctenophoreMnemiopsis leidyiin the Northern Adriatic, where we investigated the bacterial response to the gelatinous biomass. We found that the bacterial communities actively degraded the gelatinous organic matter, and overall showed a striking similarity to the dynamics previously observed after a simulated bloom of the jellyfishAurelia aurita s.l. In both cases we found that a single bacterial species,Pseudoalteromonas phenolica, was responsible for most of the degradation activity. This suggests that blooms of different jellyfish are likely to trigger a consistent response from natural bacterial communities, with specific bacterial species driving the remineralisation of gelatinous biomass.