Microbiome changes through the ontogeny of the marine sponge Crambe crambe.

BACKGROUND: Poriferans (sponges) are highly adaptable organisms that can thrive in diverse marine and freshwater environments due, in part, to their close associations with internal microbial communities. This sponge microbiome can be acquired from the surrounding environment (horizontal acquisition) or obtained from the parents during the reproductive process through a variety of mechanisms (vertical transfer), typically resulting in the presence of symbiotic microbes throughout all stages of sponge development. How and to what extent the different components of the microbiome are transferred to the developmental stages remain poorly understood. Here, we investigated the microbiome composition of a common, low-microbial-abundance, Atlantic-Mediterranean sponge, Crambe crambe, throughout its ontogeny, including adult individuals, brooded larvae, lecithotrophic free-swimming larvae, newly settled juveniles still lacking osculum, and juveniles with a functional osculum for filter feeding. RESULTS: Using 16S rRNA gene analysis, we detected distinct microbiome compositions in each ontogenetic stage, with variations in composition, relative abundance, and diversity of microbial species. However, a particular dominant symbiont, Candidatus Beroebacter blanensis, previously described as the main symbiont of C. crambe, consistently occurred throughout all stages, an omnipresence that suggests vertical transmission from parents to offspring. This symbiont fluctuated in relative abundance across developmental stages, with pronounced prevalence in lecithotrophic stages. A major shift in microbial composition occurred as new settlers completed osculum formation and acquired filter-feeding capacity. Candidatus Beroebacter blanensis decreased significatively at this point. Microbial diversity peaked in filter-feeding stages, contrasting with the lower diversity of lecithotrophic stages. Furthermore, individual specific transmission patterns were detected, with greater microbial similarity between larvae and their respective parents compared to non-parental conspecifics. CONCLUSIONS: These findings suggest a putative vertical transmission of the dominant symbiont, which could provide some metabolic advantage to non-filtering developmental stages of C. crambe. The increase in microbiome diversity with the onset of filter-feeding stages likely reflects enhanced interaction with environmental microbes, facilitating horizontal transmission. Conversely, lower microbiome diversity in lecithotrophic stages, prior to filter feeding, suggests incomplete symbiont transfer or potential symbiont digestion. This research provides novel information on the dynamics of the microbiome through sponge ontogeny, on the strategies for symbiont acquisition at each ontogenetic stage, and on the potential importance of symbionts during larval development.

Fine-scale differences in eukaryotic communities inside and outside salmon aquaculture cages revealed by eDNA metabarcoding.

Aquaculture impacts on marine benthic ecosystems are widely recognized and monitored. However, little is known about the community changes occurring in the water masses surrounding aquaculture sites. In the present study, we studied the eukaryotic communities inside and outside salmonid aquaculture cages through time to assess the community changes in the neighbouring waters of the farm. Water samples were taken biweekly over five months during the production phase from inside the cages and from nearby points located North and South of the salmon farm. Eukaryotic communities were analyzed by eDNA metabarcoding of the partial COI Leray-XT fragment. The results showed that eukaryotic communities inside the cages were significantly different from those in the outside environment, with communities inside the cages having higher diversity values and more indicator species associated with them. This is likely explained by the appearance of fouling species that colonize the artificial structures, but also by other species that are attracted to the cages by other means. Moreover, these effects were highly localized inside the cages, as the communities identified outside the cages, both North and South, had very similar eukaryotic composition at each point in time. Overall, the eukaryotic communities, both inside and outside the cages, showed similar temporal fluctuations through the summer months, with diversity peaks occurring at the end of July, beginning of September, and in the beginning of November, with the latter showing the highest Shannon diversity and richness values. Hence, our study suggests that seasonality, together with salmonid aquaculture, are the main drivers of eukaryotic community structure in surface waters surrounding the farm.

Sponges and Their Microbiomes Show Similar Community Metrics Across Impacted and Well-Preserved Reefs.

Sponge diversity has been reported to decrease from well-preserved to polluted environments, but whether diversity and intra-species variation of their associated microbiomes also change as function of environmental quality remains unknown. Our study aimed to assess whether microbiome composition and structure are related to the proliferation of some sponges and not others under degraded conditions. We characterized the most frequent sponges and their associated bacteria in two close areas (impacted and well-preserved) of Nha Trang Bay (Indo-Pacific). Sponge assemblages were richer and more diverse in the well-preserved reefs, but more abundant (individuals/m. transect) in the impacted environments, where two species (Clathria reinwardti and Amphimedon paraviridis) dominated. Sponge microbiomes from the polluted zones had, in general, lower bacterial diversity and core size and consequently, higher intra-species dispersion than microbiomes of sponges from the well-preserved environments. Microbial communities reflect the reduction of diversity and richness shown by their host sponges. In this sense, sponges with less complex and more variable microbiomes proliferate under degraded environmental conditions, following the ecological paradigm that negatively correlates community diversity and environmental degradation. Thereby, the diversity and structure of sponge microbiomes might indirectly determine the presence and proliferation of sponge species in certain habitats.

Multipartner Symbiosis across Biological Domains: Looking at the Eukaryotic Associations from a Microbial Perspective.

Sponges establish tight associations with both micro- and macroorganisms. However, while studies on sponge microbiomes are numerous, nothing is currently known about the microbiomes of sponge-associated polychaetes and their relationships with those of their host sponges. We analyzed the bacterial communities of symbiotic polychaetes (Haplosyllis spp.) and their host sponges (Clathria reinwardti, Amphimedon paraviridis, Neofibularia hartmani, and Aaptos suberitoides) to assess the influence of the sponges on the polychaete microbiomes. We identified both eukaryote partners by molecular (16S and COI genes) and morphological features, and we identified their microbial communities by high-throughput sequencing of the 16S rRNA gene (V4 region). We unravel the existence of six Haplosyllis species (five likely undescribed) associated at very high densities with the study sponge species in Nha Trang Bay (central Vietnam). A single polychaete species inhabited A. paraviridis and was different from the single species that inhabited A. suberitoides Conversely, two different polychaete species were found in C. reinwardti and N. hartmani, depending on the two host locations. Regardless of the host sponge, polychaete microbiomes were species specific, which is a widespread feature in marine invertebrates. More than half of the polychaete bacteria were also found in the host sponge microbiome but at contrasting abundances. Thus, the associated polychaetes seemed to be able to select, incorporate, and enrich part of the sponge microbiome, a selection that appears to be polychaete species specific. Moreover, the bacterial diversity is similar in both eukaryotic partners, which additionally confirms the influence of food (host sponge) on the structure of the polychaete microbiome.IMPORTANCE The symbiotic lifestyle represents a fundamental cryptic contribution to the diversity of marine ecosystems. Sponges are ideal targets to improve understanding the symbiotic relationships from evolutionary and ecological points of view, because they are the most ancient metazoans on earth, are ubiquitous in the marine benthos, and establish complex symbiosis with both prokaryotes and animals, which in turn also harbor their own bacterial communities. Here, we study the microbiomes of sponge-polychaete associations and confirm that polychaetes feed on their host sponges. The study worms select and enrich part of the sponge microbiome to shape their own species-specific bacterial communities. Moreover, worm microbiome diversity runs parallel to that of its food host sponge. Considering our results on symbiotic polychaetes and previous studies on fishes and mammals, diet appears to be an important source of bacteria for animals to shape their species-specific microbiomes.

Showcasing the role of seawater in bacteria recruitment and microbiome stability in sponges.

We studied the core bacterial communities of 19 sponge species from Nha Trang Bay (Central Vietnam), with particular emphasis on the contribution of planktonic seawater bacteria to the sponge core microbiomes. To ensure consistent sponge-microbe associations and accurate identification of planktonic bacteria transmitted from seawater, we were very restrictive with the definition of the sponge core microbiomes (present in all the replicates), and with the identification of valid biological 16S rRNA gene sequences (100% sequence identity) that belonged to potentially different bacterial taxa. We found a high overlap (>50% relative abundance) between the sponge species core microbiome and the seawater bacterial core in ca. a half of the studied species, including representatives of both, HMA and LMA sponges. From our restrictive analysis, we point to horizontal transmission as a relevant way of symbiont acquisition in sponges. Some species-specific recognition mechanisms may act in sponges to enrich specific seawater bacteria in their tissues. These mechanisms would allow the maintenance of bacterial communities in a species across geographical ranges. Moreover, besides contrasting preferences in bacteria selection from seawater, divergent physiological traits may also account for the different microbiomes in species of HMA and LMA sponges.

A Game of Russian Roulette for a Generalist Dinoflagellate Parasitoid: Host Susceptibility Is the Key to Success.

Marine microbial interactions involving eukaryotes and their parasites play an important role in shaping the structure of phytoplankton communities. These interactions may alter population densities of the main host, which in turn may have consequences for the other concurrent species. The effect generalist parasitoids exert on a community is strongly dependent on the degree of host specificity. Parvilucifera sinerae is a generalist parasitoid able to infect a wide range of dinoflagellates, including toxic-bloom-forming species. A density-dependent chemical cue has been identified as the trigger for the activation of the infective stage. Together these traits make Parvilucifera-dinoflagellate hosts a good model to investigate the degree of specificity of a generalist parasitoid, and the potential effects that it could have at the community level. Here, we present for the first time, the strategy by which a generalist dinoflagellate parasitoid seeks out its host and determine whether it exhibits host preferences, highlighting key factors in determining infection. Our results demonstrate that in its infective stage, P. sinerae is able to sense potential hosts, but does not actively select among them. Instead, the parasitoids contact the host at random, governed by the encounter probability rate and once encountered, the chance to penetrate inside the host cell and develop the infection strongly depends on the degree of host susceptibility. As such, their strategy for persistence is more of a game of Russian roulette, where the chance of survival is dependent on the susceptibility of the host. Our study identifies P. sinerae as a potential key player in community ecology, where in mixed dinoflagellate communities consisting of hosts that are highly susceptible to infection, parasitoid preferences may mediate coexistence between host species, reducing the dominance of the superior competitor. Alternatively, it may increase competition, leading to species exclusion. If, however, highly susceptible hosts are absent from the community, the parasitoid population could suffer a dilution effect maintaining a lower parasitoid density. Therefore, both host community structure and host susceptibility will determine infectivity in the field.