Whole-Genome Comparisons Among the Genus Shewanella Reveal the Enrichment of Genes Encoding Ankyrin-Repeats Containing Proteins in Sponge-Associated Bacteria

Abstract

The bacterial members of the genus Shewanella are widely distributed and inhabit both freshwater and marine environments. Some members of Shewanella have gained considerable attention due to its ability to survive in redox-stratified environments. However, a gap of knowledge exists on the key genomic features of the sponge-associated Shewanella sp. involving the successful host-bacteria interaction, as sponge-symbiotic Shewanella are largely underrepresented in the public repositories. With the aim of identifying the genomic signatures of sponge-Shewanella association, we generated a high-quality genome data of a sponge-associated, Shewanella sp. OPT22, isolated from the intertidal marine sponge Ophlitaspongia papilla and performed comprehensive comparative analyses of 68 genome strains of the genus Shewanella including two previously reported genomes of sponge-associated bacteria, Shewanella spongiae KCTC 22492 and Shewanella sp. Alg231_23. The 16S rRNA-based phylogenetic reconstruction showed the well-supported affiliation of OPT22 and KCTC 22492 with previously reported sponge-associated bacteria, affirming the “sponge-specific” nature of these two bacterial strains isolated from different marine sponge species from the Atlantic and Pacific (East Sea) Oceans, respectively. The genome comparison of the 68 strains of Shewanella inhabiting different habitats revealed the unusual/previously unreported abundance of genes encoding for ankyrin-repeat containing proteins (ANKs) in the genomes of the two sponge-associated strains, OPT22 (ANKs; n = 45) and KCTC 22492 (ANKs; n = 52), which might be involved in sponge-Shewanella interactions. Focused analyses detected the syntenic organization of the gene cluster encoding major secretion system (type III/IV/VI) components and the presence of effector homologs in OPT22 and KCTC 22492 that seem to play a role in the virulence of the sponge bacteria. The genomic island (GI) of Shewanella sp. OPT22 was identified to localize a gene cluster encoding T4SS components and ANK (n = 1), whereas S. spongiae KCTC 22492 harbored a total of seven ANKs within multiple GIs. GIs may play a pivotal role in the dissemination of symbioses-related genes (ANKs) through the horizontal gene transfer, contributing to the diversification and adaptation of sponge-associated Shewanella. Overall, the genome analyses of Shewanella isolates from marine sponges revealed genomic repertoires that might be involved in establishing successful symbiotic relationships with the sponge hosts.

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

“…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 ). To date, most microbial isolates derived from sponges have been mainly affiliated with Proteobacteria [ 7 , 25 , 26 ]. A limited number of cyanobacterial strains have been isolated from sponges [ 24 ].…”

“…Genes encoding eukaryotic-like proteins (ELPs) such as ankyrin-like domains (ANKs), tetratricopeptide repeats (TPRs), Leucine-rich repeat (LRR) protein, and pyrroloquinoline quinone (PQQ) were detected in the two sponge-associated Leptothoe strains (Table 2); ELPs are often detected in facultative or obligate symbionts and play a key role in the modulation of cellular protein-protein interactions [37,38]. In particular, abundance of ANKs seems to be a major genomic feature of sponge symbionts [6,26] as they have The sponge-associated strains possess biosynthetic gene clusters (BGCs) encoding for natural products despite undergoing genome reduction (Figure 4a,b). It has been proposed that maintenance of such clusters sustains the symbiotic interaction [35].…”

Comparative Genomics Reveals Metabolic Specificity of Endozoicomonas Isolated from a Marine Sponge and the Genomic Repertoire for Host-Bacteria Symbioses

“…Furthermore, the protein sequences of the Endozoicomonas genomes were scanned against local InterPro's proteins signature database using InterProScan v5.32-71.0 [42]. The output files were screened for the protein domains using InterPro entries-ANKs (IPR020683 and IPR002110), TPRs (IPR011990, IPR019734, IPR013105, IPR001440, and IPR011717), and Sel1 (IPR006597) as previously reported [7,43]. In order to avoid false prediction due to high similarity of proteins containing TPRs and Sel1 repeat, TPRpred v10.3-a profile-based tool was used to classify TPRs and Sel1 repeats within a protein using E-value cutoffs of 10 −3 and 10 −2 [44].…”

“…Our recent study reported that the genome of Shewanella sp. OPT22 and S. spongiae KCTC 22492 isolated from sponges are enriched with genes coding for ANKs when compared to other Shewanella strains inhabiting other niches [7]. The role of ANKs from sponge symbionts in modulating the amoebal phagocytosis was experimentally validated [81].…”

“…Studies using whole-genome sequencing of microbes isolated from sponges and metagenomic binning approaches have shown the genomic and molecular mechanisms involved in the successful association between the sponges and symbiotic microbes. For instance, genome streamlining [2], evolution of bacterial genome through transposable insertion elements [3], presence of adhesion-related genes, the genes encoding eukaryotic-like protein, effector/virulence factors [4][5][6][7] were reported among several sponge-associated bacteria.…”