Functional characterization and taxonomic classification of novel gammaproteobacterial diversity in sponges

Sponges (phylum Porifera) arose over 500 million years ago and have since diversified into at least 8,500 extant species (Van Soest et al., 2012). Sponges often harbour microbial communities that are exceptionally diverse, yet also frequently species-specific (Taylor et al., 2013). For example, a recent study of 81 sponge species identified almost 40,000 genetically unique bacterial lineages, yet there was little overlap between the microbial communities of different sponge species or with those present in the surrounding seawater or sediment (Thomas et al., 2016). Members of the phylum Proteobacteria, Chloroflexota (previously Chloroflexi (Whitman et al., 2018), Cyanobacteria, and Thermoproteota (previously TACK superphylum (Rinke et al., 2020) are often abundant in sponges. Of particular interest is the class Gammaproteobacteria, which based on 16S rRNA gene amplicon sequence data, has the highest estimated relative abundances across all sponge species examined to date (Thomas et al., 2016). Indeed, sponge-associated Gammaproteobacteria can comprise on average 25%, and in some cases more than 80%, of the relative abundance of the sponge-associated microbiota (Thomas et al., 2016, Webster and Taylor, 2012, Schmitt et al., 2012, Graeber et al., 2004, Tian et al., 2017). The vast majority of sponge-associated gammaproteobacterial species are uncultured and remain poorly assigned to taxonomic ranks below the order level (Hentschel et al., 2002, Webster et al., 2001).

Previous studies, largely based on cultured isolates, have found sponge-associated Gammaproteobacteria to be highly diverse in terms of their metabolic, functional, and ecological properties, reflected by the diversity of pathways for energy, carbon, nitrogen, and sulfur metabolism; biosynthesis of essential compounds and secondary metabolites; adaptations to varying oxic conditions; and uptake and metabolism of sponge-derived compounds (Tian et al., 2017, Tian et al., 2014, Kennedy et al., 2008, Gauthier et al., 2016, Lavy et al., 2017, Off et al., 2010, Bultel-Poncé et al., 1999, Cervino et al., 2006, Keller-Costa et al., 2014, Robbins et al., 2021). This metabolic flexibility is suggested to underpin why different Gammaproteobacteria are capable of niche partitioning and co-habitation within the same sponge host (Tian et al., 2017, Keller-Costa et al., 2014, Hardoim et al., 2009).

Here we aimed to expand our understanding of the phylogenetic diversity, metabolic versatility, and potential ecological and symbiotic roles of sponge-associated Gammaproteobacteria through the functional characterization and taxonomic classification of metagenome-assembled genomes (MAGs) from the microbial communities of three sponge species: Stylissa flabelliformis, Carteriospongia foliascens, and Petrosia ficiformis, which have previously been shown to contain an abundant population of uncharacterised Gammaproteobacteria (Burgsdorf et al., 2014, Luter et al., 2015, Glasl et al., 2018).

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