The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

Abstract

All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita. A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. aurita. IMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita. Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism.

Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress

“…Future laboratory work should attempt to carefully manipulate associations between different coral genotypes and microbial symbiotic partners (including Symbiodiniaceae and bacteria) to move toward the generation of gnotobiotic (i.e., known-microbiome) corals for use in functional experiments. This has been shown to be feasible in cnidarian model systems such as Hydra, Nematostella, and Aiptasia (Murillo-Rincon et al, 2017;Domin et al, 2018;Medrano et al, 2019;Costa et al, 2021;Dungan et al, 2021), but is only beginning to be explored in reefbuilding corals and other cnidarians (Lin et al, 2019;Cunning and Baker, 2020;Weiland-Bräuer et al, 2020). Experiments that apply a combination of antibiotics treatments followed by targeted probiotic delivery or "microbiome recovery" treatments will yield insights into whether disturbed coral-associated bacteria communities and host stress response phenotypes can be "rescued" by the re-introduction of one or several beneficial microbes (Peixoto et al, 2017(Peixoto et al, , 2021Rosado et al, 2018;Damjanovic et al, 2019;Assis et al, 2020;Santoro et al, 2021).…”

Holobiont Nitrogen Control and its Potential for Eutrophication Resistance in an Obligate Photosymbiotic Jellyfish

“…Other, aposymbiotic scyphozoans host largely species-specific bacterial communities that differ across body parts and life stages [66,67]. The bacterial associates are distinct from the environment, potentially selected via antimicrobial peptides, and involved in asexual reproduction, health, and fitness of the host [68,69].…”

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

“…Planulae and propagules of some scyphozoans have been successfully induced to enter metamorphosis using bacteria found in the environment of settled polyps; in particular, larvae of Cassiopea andromeda responded to a species of Vibrio alginolyticus ( Neumann, 1979 ; Hofmann et al, 1996 ), and the propagules (pedal stolons) of Aurelia aurita to a species of Micrococcaceae ( Schmahl, 1985 ). The asexual reproduction and strobilation of A. aurita was severely inhibited in the absence of the native microbiota ( Weiland-Bräuer et al, 2020 ). Moreover, Lee et al (2018) identified OTUs within Chrysaora plocamia and A. aurita most closely related to a suite of metabolically and physiologically diverse microorganisms capable of mediating the interrelated pathways of carbon, nitrogen, sulfur, and phosphorus.…”