Microbial Strategies for Survival in the Glass Sponge Vazella pourtalesii

Abstract

Few studies have 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 toward 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; thus, their genomic potentials were analyzed in detail. A general pattern emerged in that the V. pourtalesii symbionts had very small genome sizes, in the range of 0.5 to 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 pilus-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 in 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 compared 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.

Genomic Insights Into the Lifestyles of Thaumarchaeota Inside Sponges

“…The inclusion of the here generated genome of the thaumarchaeal symbiont from the deep-sea sponge Hymedesmia ( Stylopus ) methanophila suggests that low GC content is a general feature among deep-sea sponge-associated Thaumarchaeota. This is further supported by the recently published thaumarchaeal genomes from the deep-sea glass sponge Vazella pourtalesii , which had GC content between 31.8 and 40.4% ( Bayer et al, 2020 ). The general features of the analyzed genomes are summarized in Supplementary Table S1 .…”

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

“…Sponges are common, cosmopolitan filter feeders that pump water through their bodies to filter and ingest nutrients and microorganisms (13,14). Previous ex situ experiments have shown that sponges, including Geodia barretti (15), Tethya wilhelma (16), Halichondria panicea (17), Haliclona pigmentifera (18), and Vazella pourtalesii (19), have a high tolerance of hypoxia. For instance, T. wilhelma can maintain normal transcription at ;0.5 mM O 2 (16), despite lacking key components of the hypoxia-inducible factor (HIF) pathway, which regulates hypoxic responses in other invertebrates (16).…”

“…Many sponge species form symbioses with Nitrosopumilus-like ammonia-oxidizing Archaea (AOA) and/or Nitrospira spp. nitrite-oxidizing Bacteria (NOB) (19,(40)(41)(42)(43)(44). Each of these prokaryotic groups utilizes sponge waste ammonia for nitrification.…”

“…Also, Nitrosopumilaceae, a widespread and dominant AOA in many OMZs, plays a significant role in ammonium oxidation therein (47,48). Thus, many of these common sponge symbionts might be adapted to hypoxia, and it has been suggested that the presence of AOA symbionts, and other facultative anaerobes, within a glass sponge signified holobiont adaptation to mild, persistent environmental hypoxia (19). Furthermore, some symbionts have anaerobic metabolisms, including sulfate reducers (49), denitrifiers, and anaerobic ammonium oxidizers (anammox bacteria) (50).…”

Data_Sheet_1.PDF

“…The inclusion of the here generated genome of the thaumarchaeal symbiont from the deep-sea sponge Hymedesmia (Stylopus) methanophila suggests that low GC content is a general feature among deep-sea sponge-associated Thaumarchaeota. This is further supported by the recently published thaumarchaeal genomes from the deep-sea glass sponge Vazella pourtalesii, which had GC content between 5 https://img.jgi.doe.gov/cgi-bin/mer/main.cgi 31.8 and 40.4% (Bayer et al, 2020). The general features of the analyzed genomes are summarized in Supplementary Table S1.…”