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

Sofia Sizikov, Ilia Burgsdorf, Kim Marie Handley, Matan Lahyani, Markus Haber, Laura Steindler

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish
Pages (from-to)4669-4688
Number of pages20
JournalEnvironmental Microbiology
Volume22
Issue number11
DOIs
StatePublished - Nov 2020

Bibliographical note

Funding Information:
This work was funded by the Israel Science Foundation [Grant No. 1243/16] titled ‘Identification of molecular mechanisms underlying sponge‐microbiome symbiosis’. We would like to thank Maya Britstein for assistance with the collection of sponges, and the Mediterranean Explorer team (from EcoOcean) for assistance with the collection of seawater samples. Dr. Stefan Green, director of the DNA Services Facility at the University of Illinois at Chicago (UIC) is thanked for useful comments and suggestions when planning the sequencing of the sponge microbiome for this project.

Funding Information:
This work was funded by the Israel Science Foundation [Grant No. 1243/16] titled ?Identification of molecular mechanisms underlying sponge-microbiome symbiosis?. We would like to thank Maya Britstein for assistance with the collection of sponges, and the Mediterranean Explorer team (from EcoOcean) for assistance with the collection of seawater samples. Dr. Stefan Green, director of the DNA Services Facility at the University of Illinois at Chicago (UIC) is thanked for useful comments and suggestions when planning the sequencing of the sponge microbiome for this project.

Publisher Copyright:
© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

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