Metabolic reconstruction of the near complete microbiome of the model sponge Ianthella basta

Abstract

Many marine sponges host highly diverse microbiomes that contribute to various aspects of host health. Although the putative function of individual groups of sponge symbionts has been increasingly described, the extreme diversity has generally precluded in-depth characterization of entire microbiomes, including identification of syntrophic partnerships. The Indo-Pacific sponge Ianthella basta is emerging as a model organism for symbiosis research, hosting only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium and a range of other low abundance or transitory taxa. Here, we retrieved metagenome assembled genomes (MAGs) representing >90% of I. basta's microbial community, facilitating the metabolic reconstruction of the sponge's near complete microbiome. Through this analysis, we identified metabolic complementarity between microbes, including vitamin sharing, described the importance of low abundance symbionts, and characterized a novel microbe-host attachment mechanism in the Alphaproteobacterium. We further identified putative viral sequences, highlighting the role viruses can play in maintaining symbioses in I. basta through the horizontal transfer of eukaryotic-like proteins, and complemented this data with metaproteomics to identify active metabolic pathways in bacteria, archaea, and viruses. This data provide the framework to adopt I. basta as a model organism for studying host-microbe interactions and provide a basis for in-depth physiological experiments.

FIGURE 1

Relative abundance of MAGs present in ≥3 I. basta individuals after de‐replication at 95% identity. For I. basta individual 4 the average relative abundance is shown, as this individual was sequenced six times in the study Moeller et al. (2019). ‘Unmapped’ represents reads that could not be mapped to any of the six MAGs. IB: Ianthella basta followed by the replicate number. The proposed species name (dominant symbionts; Moeller et al., 2019, 2022) or the GTDB‐Tk taxonomy (low abundant symbionts) is displayed.

FIGURE 2

Metabolic reconstruction of I. basta's microbiome and virome. Arrowheads point to the hypothesized direction of transfer. Genes expressed in the metaproteomics data are indicated by a black dot. For secondary metabolite production and vitamin and amino acid biosynthesis, proteins were either not detected (secondary metabolite production) or detected for <60% of the genes in the metabolic pathway (vitamin and amino acid biosynthesis). The legend displays the proposed species name (for the dominant symbionts, Moeller et al., 2019, 2022) or the lowest resolved taxonomy as per GTDB taxonomy Release 202, with the three dominant symbionts highlighted by a star. HP‐HB cycle, hydroxypropionate‐hydroxybutyrate cycle; NPRS, non‐ribosomal peptide synthetase; PKS, polyketide synthase; RiPP, ribosomally synthesized and post‐translationally modified peptides; RRE, RiPP recognition element; TPR, tetratricopeptide repeats