The archaeome in metaorganism research, with a focus on marine models and their bacteria-archaea interactions.

Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of Nitrosopumilaceae and Nanoarchaeota, which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.

Experimental mining plumes and ocean warming trigger stress in a deep pelagic jellyfish.

The deep pelagic ocean is increasingly subjected to human-induced environmental change. While pelagic animals provide important ecosystem functions including climate regulation, species-specific responses to stressors remain poorly documented. Here, we investigate the effects of simulated ocean warming and sediment plumes on the cosmopolitan deep-sea jellyfish Periphylla periphylla, combining insights gained from physiology, gene expression and changes in associated microbiota. Metabolic demand was elevated following a 4 °C rise in temperature, promoting genes related to innate immunity but suppressing aerobic respiration. Suspended sediment plumes provoked the most acute and energetically costly response through the production of excess mucus (at ≥17 mg L-1), while inducing genes related to aerobic respiration and wound repair (at ≥167 mg L-1). Microbial symbionts appeared to be unaffected by both stressors, with mucus production maintaining microbial community composition. If these responses are representative for other gelatinous fauna, an abundant component of pelagic ecosystems, the effects of planned exploitation of seafloor resources may impair deep pelagic biodiversity and ecosystem functioning.

Maternal provisioning of an obligate symbiont in a sponge.

The transmission of microbes from mother to offspring is an ancient, advantageous, and widespread feature of metazoan life history. Despite this, little is known about the quantitative strategies taken to maintain symbioses across generations. The quantity of maternal microbes that is provided to each offspring through vertical transmission could theoretically be stochastic (no trend), consistent (an optimal range is allocated), or provisioned (a trade-off with fecundity). Examples currently come from animals that release free-living eggs (oviparous) and suggest that offspring are provided a consistent quantity of symbionts. The quantity of maternal microbes that is vertically transmitted in other major reproductive strategies has yet to be assessed. We used the brooding (viviparous) sponge Halichondria panicea to test whether offspring receive quantitatively similar numbers of maternal microbes. We observed that H. panicea has a maternal pool of the obligate symbiont Candidatus Halichondribacter symbioticus and that this maternal pool is provisioned proportionally to reproductive output and allometrically by offspring size. This pattern was not observed for the total bacterial community. Experimental perturbation by antibiotics could not reduce the abundance of Ca. H. symbioticus in larvae, while the total bacterial community could be reduced without affecting the ability of larvae to undergo metamorphosis. A trade-off between offspring size and number is, by definition, maternal provisioning and parallel differences in Ca. H. symbioticus abundance would suggest that this obligate symbiont is also provisioned.

Stability of a dominant sponge-symbiont in spite of antibiotic-induced microbiome disturbance.

Marine sponges are known for their complex and stable microbiomes. However, the lack of a gnotobiotic sponge-model and experimental methods to manipulate both the host and the microbial symbionts currently limit our mechanistic understanding of sponge-microbial symbioses. We have used the North Atlantic sponge species Halichondria panicea to evaluate the use of antibiotics to generate gnotobiotic sponges. We further asked whether the microbiome can be reestablished via recolonization with the natural microbiome. Experiments were performed in marine gnotobiotic facilities equipped with a custom-made, sterile, flow-through aquarium system. Bacterial abundance dynamics were monitored qualitatively and quantitatively by 16 S rRNA gene amplicon sequencing and qPCR, respectively. Antibiotics induced dysbiosis by favouring an increase of opportunistic, antibiotic-resistant bacteria, resulting in more complex, but less specific bacteria-bacteria interactions than in untreated sponges. The abundance of the dominant symbiont, Candidatus Halichondribacter symbioticus, remained overall unchanged, reflecting its obligately symbiotic nature. Recolonization with the natural microbiome could not reverse antibiotic-induced dysbiosis. However, single bacterial taxa that were transferred, successfully recolonized the sponge and affected bacteria-bacteria interactions. By experimentally manipulating microbiome composition, we could show the stability of a sponge-symbiont clade despite microbiome dysbiosis. This study contributes to understanding both host-bacteria and bacteria-bacteria interactions in the sponge holobiont.

Symbiont transmission in marine sponges: reproduction, development, and metamorphosis.

Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are transmitted in this early-diverging lineage. We describe that vertical transmission is widespread but not universal, that microbes are vertically transmitted during a select developmental window, and that properties of the developmental microbiome depends on whether a species is a high or low microbial abundance sponge. Reproduction, development, and symbiosis are thus deeply rooted, but why these partnerships form remains the central and elusive tenet of these developmental symbioses.

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea.

The animal immune system mediates host-microbe interactions from the host perspective. Pattern recognition receptors (PRRs) and the downstream signaling cascades they induce are a central part of animal innate immunity. These molecular immune mechanisms are still not fully understood, particularly in terms of baseline immunity vs induced specific responses regulated upon microbial signals. Early-divergent phyla like sponges (Porifera) can help to identify the evolutionarily conserved mechanisms of immune signaling. We characterized both the expressed immune gene repertoire and the induced response to lipopolysaccharides (LPS) in Halichondria panicea, a promising model for sponge symbioses. We exposed sponges under controlled experimental conditions to bacterial LPS and performed RNA-seq on samples taken 1h and 6h after exposure. H. panicea possesses a diverse array of putative PRRs. While part of those PRRs was constitutively expressed in all analyzed sponges, the majority was expressed individual-specific and regardless of LPS treatment or timepoint. The induced immune response by LPS involved differential regulation of genes related to signaling and recognition, more specifically GTPases and post-translational regulation mechanisms like ubiquitination and phosphorylation. We have discovered individuality in both the immune receptor repertoire and the response to LPS, which may translate into holobiont fitness and susceptibility to stress. The three different layers of immune gene control observed in this study, - namely constitutive expression, individual-specific expression, and induced genes -, draw a complex picture of the innate immune gene regulation in H. panicea. Most likely this reflects synergistic interactions among the different components of immunity in their role to control and respond to a stable microbiome, seawater bacteria, and potential pathogens.