The gill-associated symbiont microbiome is a main source of woody-plant polysaccharide hydrolase genes and secondary metabolite gene clusters in Neoteredo reynei, a unique shipworm from south Atlantic mangroves.
Teredinidae is a family of highly adapted wood-feeding and wood-boring bivalves, commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work we applied metagenomics to characterize microbiomes of the gills and digestive tract of Neoteredo reynei, a mangrove-adapted shipworm species found over a large range of the Brazilian coast. Comparative metagenomics grouped the symbiotic gammaproteobacterial community of gills of different N. reynei specimens, indicating closely related bacterial types are shared, while intestine and digestive glands presented related, and more diverse microbiomes that did not overlap with gills. Annotation of assembled metagenomic contigs revealed that the symbiotic community of N. reynei gills was a hotspot of woody-polysaccharides degrading hydrolase genes, and Biosynthetic Gene Clusters (BGCs), while in contrast, the digestive tract microbiomes seems to play little role in wood digestion and secondary metabolites biosynthesis. Metagenome binning recovered the nearly complete genome sequences of two symbiotic Teredinibacter strains from the gills, a representative of Teredinibacter turnerae \"clade I\" strain, and a yet to be cultivated Teredinibacter sp. type. These Teredinibacter genomes, as well as unbinned gill-derived gammaproteobacteria contigs, code for novelty including an endo-{beta}-1,4-xylanase/acetylxylan esterase multi-catalytic carbohydrate-active enzyme, and a trans-acyltransferase polyketide synthase (trans-AT PKS) gene cluster with the gene cassette for generating {beta}-branching on complex polyketides. Multivariate analyzes have shown that the secondary metabolome encoded on the genomes of Teredinibacter representatives, including the genomes binned from N. reynei gills metagenomes, stand out within the Cellvibrionaceae family by size, and enrichments for polyketide, nonribosomal peptide and hybrid BGCs. Results grouped here add to the growing characterization of shipworm symbiotic microbiomes and indicate that the N. reynei gill gammaproteobacterial community is a prolific source of biotechnologically relevant enzymes for wood-digestion and bioactive compounds production.