Microbial strategies for survival in the glass sponge Vazella pourtalesii

Bayer, Kristina, Busch, Kathrin, Kenchington, Ellen, Beazley, Lindsay, Franzenburg, Sören, Michels, Jan, Hentschel, Ute and Slaby, Beate M. (2020) Microbial strategies for survival in the glass sponge Vazella pourtalesii mSystems, 5 (4). Art.Nr. e00473-20. DOI 10.1128/mSystems.00473-20.

[img]
Preview
Text
mSystems-2020-Bayer-e00473-20.full.pdf - Published Version
Available under License Creative Commons: Attribution 4.0.

Download (7Mb) | Preview
[img]
Preview
Text
2020.05.28.122663v1.full.pdf - Submitted Version
Available under License Creative Commons: Attribution 4.0.

Download (2733Kb) | Preview

Supplementary data:

Abstract

Few studies have thus far explored the microbiomes of glass sponges (Hexactinellida). The present study seeks to elucidate the composition of the microbiota associated with the glass sponge Vazella pourtalesii and the functional strategies of the main symbionts. We combined microscopic approaches with metagenome-guided microbial genome reconstruction and amplicon community profiling towards this goal. Microscopic imaging revealed that the host and microbial cells appeared within dense biomass patches that are presumably syncytial tissue aggregates. Based on abundances in amplicon libraries and metagenomic data, SAR324 bacteria, Crenarchaeota, Patescibacteria and Nanoarchaeota were identified as abundant members of the V. pourtalesii microbiome and their genomic potentials were thus analyzed in detail. A general pattern emerged in that the V. pourtalesii symbionts had very small genome sizes in the range of 0.5-2.2 Mb and low GC contents, even below those of seawater relatives. Based on functional analyses of metagenome-assembled genomes (MAGs), we propose two major microbial strategies: the “givers”, namely Crenarchaeota and SAR324, heterotrophs and facultative anaerobes, produce and partly secrete all required amino acids and vitamins. The “takers”, Nanoarchaeota and Patescibacteria, are anaerobes with reduced genomes that tap into the microbial community for resources, e.g., lipids and DNA, likely using pili-like structures. We posit that the existence of microbial cells in sponge syncytia together with the low-oxygen conditions in the seawater environment are factors that shape the unique compositional and functional properties of the microbial community associated with V. pourtalesii .
Importance:
We investigated the microbial community of V. pourtalesii that forms globally unique, monospecific sponge grounds under low-oxygen conditions on the Scotian Shelf, where it plays a key role for its vulnerable ecosystem. The microbial community was found to be concentrated within biomass patches and is dominated by small cells (<1 μm). MAG analyses showed consistently small genome sizes and low GC contents, which is unusual in comparison to known sponge symbionts. These properties as well as the (facultatively) anaerobic metabolism and a high degree of interdependence between the dominant symbionts regarding amino acid and vitamin synthesis are likely adaptations to the unique conditions within the syncytial tissue of their hexactinellid host and the low-oxygen environment.

Document Type: Article
Keywords: Glass sponge, Porifera, Hexactinellida, symbiosis, microbiome, microbial metabolism, metagenomic binning, SAR324, Crenarchaeota, Patescibacteria, Nanoarchaeota
Research affiliation: OceanRep > GEOMAR > FB3 Marine Ecology > FB3-MS Marine Symbioses
Kiel University
Refereed: Yes
DOI etc.: 10.1128/mSystems.00473-20
ISSN: 2379-5077
Related URLs:
Projects: SponGES
Date Deposited: 04 Aug 2020 11:31
Last Modified: 12 Aug 2020 08:04
URI: http://eprints.uni-kiel.de/id/eprint/50265

Actions (login required)

View Item View Item

Document Downloads

More statistics for this item...