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.

Susana Rodríguez-Marconi,Beatriz Díez,Rodrigo De La Iglesia,Eduardo Hajdu,Nicole Trefault,Cássio A Fonseca,Nicole Webster

doi:10.1371/journal.pone.0138837

Susana Rodríguez-Marconi, Beatriz Díez + Show 5 more

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https://doi.org/10.1371/journal.pone.0138837

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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.

Highlights

Symbiosis, a permanent or long-lasting association between two or more different species of organisms, has played a key role in the generation of biological diversity [1,2]
The following questions were addressed: 1) How is the diversity and community composition of microorganisms at the three-domain level associated to Antarctic marine sponges, compared to the planktonic communities in the surrounding water? 2) Are bacterial, archaeal and eukaryote Antarctic sponge-microbial communities host-specific and is there a core-microbiome associated to them? 3) Are these communities similar to the ones described in sponges from other habitats? If there are differences, what are the key components supporting these differences? To this end, we comprehensively describe and compare the microbial diversity of Bacterial, Archaeal and Eukaryote microorganisms associated to eight different Antarctic sponges collected in Fildes Bay (King George Island, South Shetlands), and the surrounding seawater, using tag sequencing of hypervariable regions from 16S and 18S rRNA genes
We can suggest that symbioses between microorganisms and Antarctic sponges contributes to the nutrition of both parts, and to Antarctic marine ecosystem

Summary

Introduction

A permanent or long-lasting association between two or more different species of organisms, has played a key role in the generation of biological diversity [1,2]. Symbiotic interactions involving microorganisms are essential to the marine environment ecology, and sponges are a remarkable exponent of this kind of interaction. These sessile, filter-feeding metazoans harbor diverse microbial communities from the three domains of life [3], that accounts for up to 40% of total sponge biomass [3,4]. Sponge-associated bacterial communities have been widely studied, and some general conclusions have arisen: (i) they are host specific, (ii) they are different from planktonic communities in the surrounding water and (iii) despite being phylogenetically different, they share functional characteristics that allow them to live in symbiosis [6,7,8,9]. The majority of these studies focus on the description of one of the microbial components (i.e. bacteria, archaea, fungi and protist) of the sponge microbiome, and descriptions of whole sponge-associated microbial communities are scarce

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