The Microbial Community Associated with Rhizostoma pulmo: Ecological Significance and Potential Consequences for Marine Organisms and Human Health

Abstract

Jellyfish blooms are frequent and widespread in coastal areas worldwide, often associated with significant ecological and socio-economic consequences. Recent studies have also suggested cnidarian jellyfish may act as vectors of bacterial pathogens. The scyphomedusa Rhizostoma pulmo is an outbreak-forming jellyfish widely occurring across the Mediterranean basin. Using combination of culture-based approaches and a high-throughput amplicon sequencing (HTS), and based on available knowledge on a warm-affinity jellyfish-associated microbiome, we compared the microbial community associated with R. pulmo adult jellyfish in the Gulf of Taranto (Ionian Sea) between summer (July 2016) and winter (February 2017) sampling periods. The jellyfish-associated microbiota was investigated in three distinct compartments, namely umbrella, oral arms, and the mucus secretion. Actinobacteria, Bacteroidetes, Chlamydiae, Cyanobacteria, Deinococcus-Thermus, Firmicutes, Fusobacteria, Planctomycetes, Proteobacteria, Rhodothermaeota, Spirochaetes, Tenericutes, and Thaumarchaeota were the phyla isolated from all the three R. pulmo compartments in the sampling times. In particular, the main genera Mycoplasma and Spiroplasma, belonging to the class Mollicutes (phylum Tenericutes), have been identified in all the three jellyfish compartments. The taxonomic microbial data were coupled with metabolic profiles resulting from the utilization of 31 different carbon sources by the BIOLOG Eco-Plate system. Microorganisms associated with mucus are characterized by great diversity. The counts of culturable heterotrophic bacteria and potential metabolic activities are also remarkable. Results are discussed in terms of R. pulmo ecology, the potential health hazard for marine and human life as well as the potential biotechnological applications related to the associated microbiome.

Bacterial Communities Associated With Four Blooming Scyphozoan Jellyfish: Potential Species-Specific Consequences for Marine Organisms and Humans Health

“…The A. coerulea -associated bacterial communities were dominated by Vibrio , as has previously been shown for the communities associated with A. aurita ( Weiland-Bräuer et al, 2015 ; Kramar et al, 2019 ; Jaspers et al, 2020 ). The bacterial communities associated with N. nomurai and R. esculentum (family Rhizostomatidae) were similarly dominated by a single genus, Mycoplasma , which was consistent with previous results for R. pulmo (family Rhizostomatidae) ( Basso et al, 2019 ; Stabili et al, 2020 ). Interestingly, three bacterial genera presented relatively similar abundances associated with C. nozakii including Shingomonas , Phyllobacterium , and Ralstonia .…”

“…Several studies found Mycoplasma to be the prevailing taxa in the microbiomes of the scyphozoans A. aurita (Weiland-Bräuer et al, 2015;Daley et al, 2016;Jaspers et al, 2020), and R. pulmo (Basso et al, 2019;Stabili et al, 2020), similar to the present study. Vibrio has previously been found to be the dominant genus in A. aurita (Weiland-Bräuer et al, 2015;Kramar et al, 2019;Jaspers et al, 2020), A. coerulea (Chen et al, 2020), R. pulmo (Basso et al, 2019;Stabili et al, 2020), Cotylorhiza tuberculata (Cortés-Lara et al, 2015), C. lamarckii (Schuett and Doepke, 2010), and C. capillata (Schuett and Doepke, 2010;Clinton et al, 2020), and was abundant in A. coerulea, N. nomurai and R. esculentum in this study. Genus Tenacibaculum was dominant in N. nomurai and R. esculentum in this study, and has been suggested as a key part of the bacterial communities of A. aurita (Jaspers et al, 2020), C. tuberculata (Cortés-Lara et al, 2015;Viver et al, 2017) and P. noctiluca (Delannoy et al, 2011).…”

“…Scyphomedusa-associated bacterial communities presented different composition and lower diversities compared with the free-living bacterial communities in the ambient seawater, consistent with previous studies ( Weiland-Bräuer et al, 2015 ; Daley et al, 2016 ; Kramar et al, 2019 ; Daniel and Ana, 2020 ). Most previous studies on scyphozoan-associated microbiomes focused on one single scyphozoan species (e.g., Cortés-Lara et al, 2015 ; Weiland-Bräuer et al, 2015 ; Viver et al, 2017 ; Lee et al, 2018 ; Basso et al, 2019 ; Kramar et al, 2019 ; Stabili et al, 2020 ), with few studies investigating the differences between the bacteria associated with various scyphozoan species. In the present study, the composition and structure of the microbiomes associated with four scyphomedusae were compared and found to be significantly different from each other, indicating that the scyphomedusa-associated bacteria were scyphozoan taxa-specific (as Cleary et al, 2016 ; Hao et al, 2019 ; and Daniel and Ana, 2020 reported).…”

“…Bacterial communities associated with jellyfish mainly consisted of Alpha- and Gammaproteobacteria, Bacteroidetes, Tenericutes, and Cyanobacteria ( Weiland-Bräuer et al, 2015 ; Daley et al, 2016 ; Basso et al, 2019 ; Kramar et al, 2019 ; Jaspers et al, 2020 ; Stabili et al, 2020 ). Certain jellyfish increase in numbers and form blooms or aggregations during certain periods, during which the population density of the pelagic medusae peaks distinctly over broad temporal and regional scales ( Purcell et al, 2007 ; Condon et al, 2012 ; Purcell, 2012 ).…”

Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans

“…These bacteria, due to their capability to synthesize antimicrobial compounds when attached to live or inert surfaces, were previously recognized as significant players in the host defense towards pathogens and fouling organisms from the surrounding environment. Rhizostoma pulmo-associated microbiota were investigated in three distinct compartments, namely umbrella, oral arms, and the mucus secretion [47,48]. Actinobacteria, Bacteroidetes, Chlamydiae, Cyanobacteria, Deinococcus-Thermus, Firmicutes, Fusobacteria, Planctomycetes, Proteobacteria, Rhodothermaeota, Spirochaetes, Tenericutes, and Thaumarchaeota were the phyla isolated from all the three R. pulmo compartments in the sampling times.…”