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Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome.

ABSTRACT: All eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly linked physical interactions that characterize many macroscopic symbioses create opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between distantly related taxa. Here, we sequence the microbiomes of five species of clownfish-hosting sea anemones that co-occur on coral reefs in the Maldives. We test the importance of evolutionary history, clownfish symbiont association, and habitat on the taxonomic and predicted functional diversity of the microbiome, and explore signals of microbiome convergence in anemone taxa that have evolved symbioses with clownfishes independently. Our data indicate that host identity and clownfish association shapes the majority of the taxonomic diversity of the clownfish-hosting sea anemone microbiome, and predicted functional microbial diversity analyses demonstrate a convergence among host anemone microbiomes, which reflect increased functional diversity over individuals that do not host clownfishes. Further, we identify upregulated predicted microbial functions that are likely affected by clownfish presence. Taken together our study potentially reveals an even deeper metabolic coupling between clownfishes and their host anemones, and what could be a previously unknown mutualistic benefit to anemones that are symbiotic with clownfishes.

SUBMITTER: Titus BM

PROVIDER: S-EPMC7058955 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome.

Titus Benjamin M BM Laroche Robert R Rodríguez Estefanía E Wirshing Herman H Meyer Christopher P CP

Biology letters 20200205 2

All eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly linked physical interactions that characterize many macroscopic symbioses create opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between dista ...[more]

PMID: 32019466

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Project description:BackgroundOne of the most charismatic, and yet not completely resolved example of mutualistic interaction is the partnership of clownfish and its symbiotic sea anemone. The mechanism explaining this tolerance currently relies on the molecular mimicry of clownfish epithelial mucus, which could serve as camouflage, preventing the anemone's nematocysts' discharge. Resident bacteria are known as key drivers of epithelial mucus chemical signature in vertebrates. A recent study has proposed a restructuration of the skin microbiota in a generalist clown fish when first contacting its symbiotic anemone. We explored a novel hypothesis by testing the effect of remote interaction on epithelial microbiota restructuration in both partners.MethodsWith metataxonomics, we investigated the epithelial microbiota dynamic of 18 pairs of percula clownfish (Amphiprion percula) and their symbiotic anemone Heteractis magnifica in remote interaction, physical interaction and control groups for both partners during a 4-week trial.ResultsThe Physical and Remote Interaction groups' results evidence gradual epithelial microbiota convergence between both partners when fish and anemone were placed in the same water system. This convergence occurred preceding any physical contact between partners, and was maintained during the 2-week interaction period in both contact groups. After the interaction period, community structure of both fish and anemone's epthelial community structures maintained the interaction signature 2 weeks after fish-anemone pairs' separation. Furthermore, the interaction signature persistence was observed both in the Physical and Remote Interaction groups, thus suggesting that water-mediated chemical communication between symbiotic partners was strong enough to shift the skin microbiota durably, even after the separation of fish-anemone pairs. Finally, our results suggest that fish-anemone convergent microbiota restructuration was increasingly associated with the parallel recruitment of three Flavobacteriaceae strains closely related to a tyrosinase-producing Cellulophaga tyrosinoxydans.ConclusionsOur study shows that bacterial community restructuration, in the acclimation process, does not only rely on direct physical contact. Furthermore, our results challenge, for the first time, the traditional unidirectional chemical camouflage hypothesis, as we argue that convergence of the epithelial microbiota of both partners may play essential roles in establishing mutual acceptance. Video abstract Fish-anemone symbiotic relationship.

Project description:BACKGROUND: Coral reef ecosystems are renowned for their diversity and beauty. Their immense ecological success is due to a symbiotic association between cnidarian hosts and unicellular dinoflagellate algae, known as zooxanthellae. These algae are photosynthetic and the cnidarian-zooxanthellae association is based on nutritional exchanges. Maintenance of such an intimate cellular partnership involves many crosstalks between the partners. To better characterize symbiotic relationships between a cnidarian host and its dinoflagellate symbionts, we conducted a large-scale EST study on a symbiotic sea anemone, Anemonia viridis, in which the two tissue layers (epiderm and gastroderm) can be easily separated. RESULTS: A single cDNA library was constructed from symbiotic tissue of sea anemones A. viridis in various environmental conditions (both normal and stressed). We generated 39,939 high quality ESTs, which were assembled into 14,504 unique sequences (UniSeqs). Sequences were analysed and sorted according to their putative origin (animal, algal or bacterial). We identified many new repeated elements in the 3'UTR of most animal genes, suggesting that these elements potentially have a biological role, especially with respect to gene expression regulation. We identified genes of animal origin that have no homolog in the non-symbiotic starlet sea anemone Nematostella vectensis genome, but in other symbiotic cnidarians, and may therefore be involved in the symbiosis relationship in A. viridis. Comparison of protein domain occurrence in A. viridis with that in N. vectensis demonstrated an increase in abundance of some molecular functions, such as protein binding or antioxidant activity, suggesting that these functions are essential for the symbiotic state and may be specific adaptations. CONCLUSION: This large dataset of sequences provides a valuable resource for future studies on symbiotic interactions in Cnidaria. The comparison with the closest available genome, the sea anemone N. vectensis, as well as with EST datasets from other symbiotic cnidarians provided a set of candidate genes involved in symbiosis-related molecular crosstalks. Altogether, these results provide new molecular insights that could be used as a starting-point for further functional genomics studies.

Project description:BACKGROUND:Coral reef ecosystems are declining in response to global climate change and anthropogenic impacts. Yet patterns of standing genetic variation within cnidarian species, a major determinant of adaptive potential, are virtually unknown at genome-scale resolution. We explore patterns of genome-wide polymorphism and identify candidate loci under selection in the sea anemone Aiptasia, an important laboratory model system for studying the symbiosis between corals and dinoflagellate algae of the genus Symbiodinium. RESULTS:Low coverage genome sequencing revealed large genetic distances among globally widespread lineages, novel candidate targets of selection, and considerably higher heterozygosity than previously reported for Aiptasia. More than 670,000 single nucleotide polymorphisms were identified among 10 Aiptasia individuals including two pairs of genetic clones. Evolutionary relationships based on genome-wide polymorphism supported the current paradigm of a genetically distinct population from the US South Atlantic that harbors diverse Symbiodinium clades. However, anemones from the US South Atlantic demonstrated a striking lack of shared derived polymorphism. Heterozygosity was an important feature shaping nucleotide diversity patterns: at any given SNP site, more than a third of individuals genotyped were heterozygotes, and heterozygosity within individual genomes ranged from 0.37-0.58%. Analysis of nonsynonymous and synonymous sites suggested that highly heterozygous regions are evolving under relaxed purifying selection compared to the rest of the Aiptasia genome. Genes previously identified as having elevated evolutionary rates in Aiptasia compared to other cnidarians were found in our study to be under strong purifying selection within Aiptasia. Candidate targets of selection, including lectins and genes involved in Rho GTPase signalling, were identified based on unusual signatures of nucleotide diversity, Tajima's D, and heterozygosity compared to genome-wide averages. CONCLUSIONS:This study represents the first genome-wide analysis of Tajima's D in a cnidarian. Our results shed light on patterns of intraspecific genome-wide polymorphism in a model for studies of coral-algae symbiosis and present genetic targets for future research on evolutionary and cellular processes in early-diverging metazoans.

Project description:The size and structure of social groups of animals can be governed by a range of ecological factors and behavioral interactions. In small, highly site-attached coral reef fishes, group size is often constrained by the size of the habitat patch they are restricted to. However, group size may also be influenced by changes in abundance along important environmental gradients, such as depth or distance offshore. In addition, the body size and sex structure within social groups can be determined by the size of the habitat patch and the dominance relationships among group members. Here we examined the roles of ecological factors and behavioral interactions in governing group size and structure in the orange clownfish, Amphiprion percula, on inshore reefs in Kimbe Bay, Papua New Guinea. We quantified relationships between ecological variables (anemone size, depth, and distance from shore) and social group variables (group size, and total body length of the three largest individuals (ranks 1, 2, and 3)). Anemone size explained the greatest amount of variation in group variables, with strong, positive relationships between anemone surface area and group size, and total length of individuals ranked 1, 2, and 3. Group structure was also weakly correlated with increasing depth and distance from shore, most likely through the indirect effects of these environmental gradients on anemone size. Variation in group size and the lengths of ranks 2 and 3 were all closely related to the length of rank 1. Path analysis indicated that anemone size has a strong direct effect on the length of rank 1. In turn, the length of rank 1 directly affects the size of the subordinate individuals and indirectly affects the group size through its influence on subordinates. Hence, anemone size directly and indirectly controls social group size and structure in this space-limited fish species. It is also likely that anemonefish have feedback effects on anemone size, although this could not be differentiated in the path analysis.

Dataset Information

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome.

Publications

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome.

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