Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium Leptothoe

Abstract

Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus Leptothoe (Synechococcales). We obtained draft genomes from Le. kymatousa TAU-MAC 1615 and Le. spongobia TAU-MAC 1115, isolated from marine sponges. We identified five additional Leptothoe genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. Le. kymatousa and Le. spongobia have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated Leptothoe genomes. The sponge-associated Leptothoe stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of Leptothoe with chemically rich cyanobacteria revealed that Leptothoe is another promising marine cyanobacterium for the biosynthesis of novel natural products.

Description and Genomic Characterization of Oceaniferula flavus sp. nov., a Novel Potential Polysaccharide-Degrading Candidate of the Difficult-to-Cultivate Phylum Verrucomicrobiota Isolated from Seaweed

“…The phylogenetic tree based on these 120 ubiquitous genes was reconstructed by IQ-TREE [ 37 ] using the LG+F+I+G4 model and 1000 bootstrap replicates. Some other analysis methods referred to the previous published articles [ 38 , 39 ].…”

Comparative genome analysis of Vagococcus fluvialis reveals abundance of mobile genetic elements in sponge-isolated strains

“…More specifically, these strains lack the bacterial chemotaxis genes present in the other V. fluvialis genomes. The loss of chemotaxis and motility genes in bacteria associated to marine sponges has previously been described and is hypothesized to be caused, and indication of, a mutualistic lifestyle and vertical transmission of symbionts [19,20]. Pangenome analysis of V. fluvialis revealed great intraspecies diversity (Supplementary Figure S3): notably, the V. fluvialis genomes shared only 28% of core genes, whereas 45.5% of orthologous genes were unique.…”

Comparative Metagenomic Analysis of Biosynthetic Diversity across Sponge Microbiomes Highlights Metabolic Novelty, Conservation, and Diversification

“…These include GCFs that are shared among all sponge species. Lassopeptides have been found in some sponge-associated microbiomes ( 86 , 87 ), but their presence together with diverse flanking enzyme-encoding genes has not been previously reported in this environmental niche. While the functions of these BGCs and their metabolic products remains elusive, this data set expands and diversifies the set of sponge-holobiont-encoded RiPPs and predicts sponge microbiomes to be prolific sources of RiPP NPs.…”