Characterization of Bacterial, Archaeal and Eukaryote Symbionts from Antarctic Sponges Reveals a High Diversity at a Three-Domain Level and a Particular Signature for This Ecosystem

Abstract

Sponge-associated microbial communities include members from the three domains of life. In the case of bacteria, they are diverse, host specific and different from the surrounding seawater. However, little is known about the diversity and specificity of Eukarya and Archaea living in association with marine sponges. This knowledge gap is even greater regarding sponges from regions other than temperate and tropical environments. In Antarctica, marine sponges are abundant and important members of the benthos, structuring the Antarctic marine ecosystem. In this study, we used high throughput ribosomal gene sequencing to investigate the three-domain diversity and community composition from eight different Antarctic sponges. Taxonomic identification reveals that they belong to families Acarnidae, Chalinidae, Hymedesmiidae, Hymeniacidonidae, Leucettidae, Microcionidae, and Myxillidae. Our study indicates that there are different diversity and similarity patterns between bacterial/archaeal and eukaryote microbial symbionts from these Antarctic marine sponges, indicating inherent differences in how organisms from different domains establish symbiotic relationships. In general, when considering diversity indices and number of phyla detected, sponge-associated communities are more diverse than the planktonic communities. We conclude that three-domain microbial communities from Antarctic sponges are different from surrounding planktonic communities, expanding previous observations for Bacteria and including the Antarctic environment. Furthermore, we reveal differences in the composition of the sponge associated bacterial assemblages between Antarctic and tropical-temperate environments and the presence of a highly complex microbial eukaryote community, suggesting a particular signature for Antarctic sponges, different to that reported from other ecosystems.

Fig 1. Diversity measures.

Non-parametric Shannon and Chao1 estimator calculated with sequences rarefied to the sample with minimum sequence number (Clathria sp. with 53,038 and Myxilla (Burtonanchora) sp. with 907 sequences for Bacteria/Archaea and Eukarya, respectively). SW: surrounding seawater sample.

Fig 2. Taxonomic composition.

Taxonomic distribution of assigned tag sequences of Antarctic sponge-associated and surrounding seawater (SW) microbial communities. Bars represent relative abundance of sequences belonging to given classes superior to 0.5%. (A) Bacteria/Archaea assigned with the Silva database. (B) Eukaryotes assigned with the PR2 database. MyxB: Myxilla (Burtonanchora) sp.; Clat: Clathria sp.; uDem: undetermined Demospongiae; Kvar: Kirkpatrickia variolosa; Htor: Hymeniacidon torquata; Lant: Leucetta Antarctica; HalG: Haliclona (Gellius) sp.; Mann: Megaciella annectens; SW: surrounding seawater sample.

Fig 3. OTU distribution and clustering.

Heatmaps representing the relative abundance (50 most abundant OTUs) of bacterial/archaeal (A) and eukaryote (B) taxa associated to Antarctic sponges and the corresponding surrounding seawater microbial communities. Their most resolved taxonomic assignation is included a side each OTU. Numbers represent taxonomic resolution level of the assignation, with (2) = Phylum, (3) = Class, (4) = Order, (5) = Family and (6) = Genus. Cluster above heatmap was generated using weighted Unifrac distance and group average clustering method. Color keys represent square root of relative abundance (in percentage). MyxB: Myxilla (Burtonanchora) sp.; Clat: Clathria sp.; uDem: undetermined Demospongiae; Kvar: Kirkpatrickia variolosa; Htor: Hymeniacidon torquata; Lant: Leucetta Antarctica; HalG: Haliclona (Gellius) sp.; Mann: Megaciella annectens; SW: surrounding seawater sample.

Fig 4. NMDS analysis of bacterial microbiota of sponges from different environments.

Analysis is based on Bray-Curtis similarities of relative abundances at phylum-level. Circles indicate similarity level of 75% based on hierarchical cluster analysis. Polar: MyxB: Myxilla (Burtonanchora) sp.; Clat: Clathria sp.; uDem: undetermined Demospongiae; Kvar: Kirkpatrickia variolosa; Htor: Hymeniacidon torquata; Lant: Leucetta Antarctica; HalG: Haliclona (Gellius) sp.; Mann: Megaciella annectens. Tropical: Eform: Erylus formosus; Acra: Aiolochroia crassa; Aful: Aplysina fulva; Acauli: Aplysina cauliformis; Eferox: Ectyoplasia ferox; Pinter: Placospongia intermedia; Hvan: Haliclona vansoesti; Ccari: Chondrilla caribensis; Cmol: Chalinula molitba; Htub: Haliclona tubifera; Mlax: Mycale laxissima;Xboc: Xestospongia bocatorensis; Nere: Niphates erecta; Acomp: Amphimedon compressa; Mlae: Mycale laevis; Aerina: Amphimedon erina; Tignis:Tedania ignis; Dethe: Dysidea etheria. Warm-temperate: Rodor: Rhopaloeides odorabile; Iram: Ircinia ramosa; Herec: Hyrtios erectus; Xtest: Xestospongia testudinaria; Caus: Cinachyrella australiensis, Sdiver: Suberites diversicolor. Cold-temperate: Rram: Raspailia ramosa; Sstup: Stelligera stuposa.