Marine bacteriophages disturb the associated microbiota of Aurelia aurita with a recoverable effect on host morphology.

The concept of the metaorganism describes a multicellular host and its diverse microbial community, which form one biological unit with a combined genetic repertoire that significantly influences health and survival of the host. The present study delved into the emerging field of bacteriophage research within metaorganisms, focusing on the moon jellyfish Aurelia aurita as a model organism. The previously isolated Pseudomonas phage BSwM KMM1 and Citrobacter phages BSwM KMM2 - KMM4 demonstrated potent infectivity on bacteria present in the A. aurita-associated microbiota. In a host-fitness experiment, Baltic Sea subpopulation polyps were exposed to individual phages and a phage cocktail, monitoring polyp survival and morphology, as well as microbiome changes. The following effects were obtained. First, phage exposure in general led to recoverable malformations in polyps without affecting their survival. Second, analyses of the community structure, using 16S rRNA amplicon sequencing, revealed alterations in the associated microbial community in response to phage exposure. Third, the native microbiota is dominated by an uncultured likely novel Mycoplasma species, potentially specific to A. aurita. Notably, this main colonizer showed resilience through the recovery after initial declines, which aligned with abundance changes in Bacteroidota and Proteobacteria, suggesting a dynamic and adaptable microbial community. Overall, this study demonstrates the resilience of the A. aurita metaorganism facing phage-induced perturbations, emphasizing the importance of understanding host-phage interactions in metaorganism biology. These findings have implications for ecological adaptation and conservation in the rapidly changing marine environment, particularly regarding the regulation of blooming species and the health of marine ecosystems during ongoing environmental changes.

Four Novel Caudoviricetes Bacteriophages Isolated from Baltic Sea Water Infect Colonizers of Aurelia aurita.

The moon jellyfish Aurelia aurita is associated with a highly diverse microbiota changing with provenance, tissue, and life stage. While the crucial relevance of bacteria to host fitness is well known, bacteriophages have often been neglected. Here, we aimed to isolate virulent phages targeting bacteria that are part of the A. aurita-associated microbiota. Four phages (Pseudomonas phage BSwM KMM1, Citrobacter phages BSwM KMM2-BSwM KMM4) were isolated from the Baltic Sea water column and characterized. Phages KMM2/3/4 infected representatives of Citrobacter, Shigella, and Escherichia (Enterobacteriaceae), whereas KMM1 showed a remarkably broad host range, infecting Gram-negative Pseudomonas as well as Gram-positive Staphylococcus. All phages showed an up to 99% adsorption to host cells within 5 min, short latent periods (around 30 min), large burst sizes (mean of 128 pfu/cell), and high efficiency of plating (EOP > 0.5), demonstrating decent virulence, efficiency, and infectivity. Transmission electron microscopy and viral genome analysis revealed that all phages are novel species and belong to the class of Caudoviricetes harboring a tail and linear double-stranded DNA (formerly known as Siphovirus-like (KMM3) and Myovirus-like (KMM1/2/4) bacteriophages) with genome sizes between 50 and 138 kbp. In the future, these isolates will allow manipulation of the A. aurita-associated microbiota and provide new insights into phage impact on the multicellular host.