Characterization of sponge‐associated Verrucomicrobia: microcompartment‐based sugar utilization and enhanced toxin–antitoxin modules as features of host‐associated Opitutales

Abstract

Summary Bacteria of the phylum Verrucomicrobia are ubiquitous in marine environments and can be found as free‐living organisms or as symbionts of eukaryotic hosts. Little is known about host‐associated Verrucomicrobia in the marine environment. Here we reconstructed two genomes of symbiotic Verrucomicrobia from bacterial metagenomes derived from the Atlanto‐Mediterranean sponge Petrosia ficiformis and three genomes from strains that we isolated from offshore seawater of the Eastern Mediterranean Sea. Phylogenomic analysis of these five strains indicated that they are all members of Verrucomicrobia subdivision 4, order Opitutales. We compared these novel sponge‐associated and seawater‐isolated genomes to closely related Verrucomicrobia. Genomic analysis revealed that Planctomycetes‐Verrucomicrobia microcompartment gene clusters are enriched in the genomes of symbiotic Opitutales including sponge symbionts but not in free‐living ones. We hypothesize that in sponge symbionts these microcompartments are used for degradation of l‐fucose and l‐rhamnose, which are components of algal and bacterial cell walls and therefore may be found at high concentrations in the sponge tissue. Furthermore, we observed an enrichment of toxin–antitoxin modules in symbiotic Opitutales. We suggest that, in sponges, verrucomicrobial symbionts utilize these modules as a defence mechanism against antimicrobial activity deriving from the abundant microbial community co‐inhabiting the host.

Impact of Marine Aquaculture on the Microbiome Associated with Nearby Holobionts: The Case of Patella caerulea Living in Proximity of Sea Bream Aquaculture Cages

“…Frequently in cooperation with Planctomycetes [64], members of Verrucomicrobia are capable of processing decaying organic materials and polysaccharides [65,66]. Several studies have highlighted their symbiotic lifestyle in marine invertebrates with recent findings showing metabolic adaptations enabling a more efficient utilization of specific carbon sources present in the host [22,64,67]. However, we observed that the proximity to the aquaculture site was associated with the reduction of the Verrucomicrobia uncultured family DEV007 in the limpet microbiome of limpets.…”

“…Such difference was already evident when looking at the microbiome phylogenetic structure at the phylum level, with Tenericutes largely abundant in samples collected on the cages, whereas samples from the rocky shores were enriched in Verrucomicrobia. Frequently in cooperation with Planctomycetes [64], members of Verrucomicrobia are capable of processing decaying organic materials and polysaccharides [65,66]. Several studies have highlighted their symbiotic lifestyle in marine invertebrates with recent findings showing metabolic adaptations enabling a more efficient utilization of specific carbon sources present in the host [22,64,67].…”

A Catalog of the Diversity and Ubiquity of Metabolic Organelles in Bacteria

“…Another functional type that has substantially increased in membership are the PVMs [24] now with 285 representatives (Figure 2), as compared to seven found in 2014 [4]. This reflects the increased attention to Verrucomicrobia species for their role in the global carbon cycle as degraders of complex algal and bacterial cell wall polysaccharides [25, 26]. For example, Lentimonas species devote 4% of their proteome to the degradation of fucoidan, the major cell wall polysaccharide of brown algae into fucose, which is catabolized in the PVM BMC [26].…”

Antibiotic Modulation of Capsular Exopolysaccharide in Pelagicoccus enzymogenes sp. nov. Isolated From Marine Sediment

“…Bacteria belonging to the phylum Verrucomicrobia are commonly studied in the soil and gut environments. It has been shown that Verrucomicrobia is nearly ubiquitous in the marine environment (Freitas et al, 2012;Thomas et al, 2019;Sizikov et al, 2020), but little is known about the function and cellular features of this phylum in the marine environment. Besides, detailed studies on cellular and biochemical features of the phylum Verrucomicrobia necessitate axenic cultures.…”