Abstract
BackgroundMarine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Lamellodysidea herbacea sponges obtain additional energy from abundant photosynthetic Hormoscilla cyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscilla bacteria to Lamellodysidea microbiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown.ResultsThis study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, uncultured Lamellodysidea-associated microbial populations by reconstructing near-complete metagenome-assembled genomes (MAGs) to complement 16S rRNA gene amplicon studies. Microbial community compositions aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a 3-year period, including representatives of Alphaproteobacteria, Gammaproteobacteria, Oligoflexia, and Bacteroidetes as well as Cyanobacteria (Hormoscilla). Unexpectedly, microbiomes from one host clade also included Cyanobacteria from the prolific secondary metabolite-producer genus Prochloron, a common tunicate symbiont.Two novel Alphaproteobacteria MAGs encoded pathways diagnostic for methylotrophic metabolism as well as type III secretion systems, and have been provisionally assigned to a new order, designated Candidatus Methylospongiales. MAGs from other taxonomic groups encoded light-driven energy production pathways using not only chlorophyll, but also bacteriochlorophyll and proteorhodopsin. Diverse heterotrophic capabilities favoring aerobic versus anaerobic conditions included pathways for degrading chitin, eukaryotic extracellular matrix polymers, phosphonates, dimethylsulfoniopropionate, trimethylamine, and benzoate. Genetic evidence identified an aerobic catabolic pathway for halogenated aromatics that may enable endogenous PBDEs to be used as a carbon and energy source.ConclusionsThe reconstruction of high-quality MAGs from all microbial taxa comprising greater than 0.1% of the sponge microbiome enabled species-specific assignment of unique metabolic features that could not have been predicted from taxonomic data alone. This information will promote more representative models of marine invertebrate microbiome contributions to host bioenergetics, the identification of potential new sponge parasites and pathogens based on conserved metabolic and physiological markers, and a better understanding of biosynthetic and degradative pathways for secondary metabolites and halogenated compounds in sponge-associated microbiota.Dn7znYuJ-m6v4UERxLrGDHVideo
Highlights
Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter
The reconstruction of high-quality Metagenome-assembled genome (MAG) from all microbial taxa comprising greater than 0.1% of the sponge microbiome enabled species-specific assignment of unique metabolic features that could not have been predicted from taxonomic data alone
Hormoscilla sponge symbionts have never been successfully cultured in the laboratory, two genomes of this bacterial clade have recently been assembled from trichome-enriched metagenomic samples [13]. 16S rRNA gene amplification studies have detected sponge-specific Alpha- and Gammaproteobacteria sequences associated with Lamellodysidea [14], but did not investigate how these nonHormoscilla symbionts might contribute to metabolic activities and ecological interactions in the sponge microbiome
Summary
Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Studies measuring potential contributions of photosynthetic symbionts to host energy metabolism have historically used Lamellodysidea herbacea as a prototypical model [8,9,10]. These studies have suggested that phototrophic cyanobacteria can contribute as much as 80% of the total sponge carbon budget, significant variation has been observed among individual sponges [11]. Hormoscilla sponge symbionts have never been successfully cultured in the laboratory, two genomes of this bacterial clade have recently been assembled from trichome-enriched metagenomic samples [13]. 16S rRNA gene amplification studies have detected sponge-specific Alpha- and Gammaproteobacteria sequences associated with Lamellodysidea [14], but did not investigate how these nonHormoscilla symbionts might contribute to metabolic activities and ecological interactions in the sponge microbiome
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