Distribution and diversity of Candidatus Tectomicrobia harbouring rich producers of bioactive metabolites

Genomic and functional analyses of bacteria belonging to the candidate genus ‘Entotheonella’ have revealed them as the producers of diverse bioactive compounds previously identified from their sponge hosts. Based on genetic distance to other taxa, ‘Candidatus Entotheonella’ has been proposed as the first member of a new candidate phylum, ‘Tectomicrobia’. Here, we analysed environmental samples and publicly available 16S ribosomal RNA (rRNA) gene sequences to assess the phylogenetic structure and environmental distribution of this as-yet sparsely populated lineage. The data showed that ‘Ca. Entotheonella’ and other 'Ca. Tectomicrobia' were not restricted to marine habitats but also widely distributed among terrestrial locations. Environmental factors, such as water depth and host association were identified to correlate with the phylogenetic patterns of marine phylotypes. The previously described ‘Ca. Entotheonella’ lineage could be more accurately divided into at least three different candidate genera with the terrestrial 'Candidatus Prasianella', the marine 'Candidatus Thalassonella' and the more widely distributed 'Ca. Entotheonella' of mixed origin. This first metagenomic and microscopic characterization of 'Ca. Thalassonella' from a range of sponge hosts did not suggest a role for its members as providers of natural products, despite clear similarities in genome-based predictions of primary metabolism and implied lifestyle with ‘Ca. Entotheonella’. In contrast, within the revised ‘Ca. Entotheonella’, the analysis revealed a correlation between the 16S rRNA gene phylogeny and a specific association with sponges and their chemistry, suggesting that this feature might serve as a discovery method to accelerate the identification of new ‘Ca. Entotheonella’ producers of bioactive compounds. Application of this strategy led to the identification of the first ‘Ca. Entotheonella’ symbiont in a non-lithistid sponge, Psammocinia sp., thus indicating a wider host distribution of ‘Ca. Entotheonella’-based chemical symbiosis.