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

Despoina Konstantinou,Kaarina Sivonen,Rafael V Popin,David P Fewer,Spyros Gkelis

doi:10.3390/md19060298

Despoina Konstantinou, Kaarina Sivonen + Show 3 more

Open Access

https://doi.org/10.3390/md19060298

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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.

Highlights

Sponges host abundant and remarkable diverse microbial communities [1] that exhibit biological complexity similar to the human microbiome [2,3]
Cyanobacteria are an ancient lineage of photosynthetic prokaryotes demonstrating ecological key roles in a broad range of habitats, including sponges [4,5], with which they are often found in symbiosis
Two new sponge-associated cyanobacterial draft genomes belonging to the newly described Leptothoe genus were recovered from the isolates TAU-MAC 1615 and 1115 (Figure S1, Table 1)

Summary

Introduction

Sponges host abundant and remarkable diverse microbial communities [1] that exhibit biological complexity similar to the human microbiome [2,3]. Cyanobacteria are an ancient lineage of photosynthetic prokaryotes demonstrating ecological key roles (e.g., oxygen production, nitrogen fixation, carbon flux) in a broad range of habitats, including sponges [4,5], with which they are often found in symbiosis (cyanobionts). It has been shown that across sponge-associated bacteria taxa there are pathways involved in carbon fixation, B-vitamin synthesis, taurine metabolism, sulfite oxidation, and most steps of nitrogen metabolism [7,8]. Candidatus Synechococcus spongiarum, a widespread (yet uncultivated) sponge symbiont, has specific adaptations to life inside sponges [9]. This obligate cyanobiont showed extreme genome reduction [9], to other bacterial sponge symbionts such as Candidatus Endohaliclona renieramycinifaciens [10]. Genome reduction is the major genomic feature of bacterial symbionts [11] and is thought to be a process that reduces the cost of genome replication [12]

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