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Here, we employed comparative metagenomics to uncover the distinct functional and phylogenetic features of the microbiomes of healthy <jats:italic>Eunicella gazella<\/jats:italic>, <jats:italic>Eunicella verrucosa<\/jats:italic>, and <jats:italic>Leptogorgia sarmentosa<\/jats:italic> tissues, in contrast with the microbiomes found in seawater and sediments. We further explored how the octocoral microbiome shifts to a pathobiome state in <jats:italic>E. gazella<\/jats:italic>.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Multivariate analyses based on 16S rRNA genes, Clusters of Orthologous Groups of proteins (COGs), Protein families (Pfams), and secondary metabolite-biosynthetic gene clusters annotated from 20 Illumina-sequenced metagenomes each revealed separate clustering of the prokaryotic communities of healthy tissue samples of the three octocoral species from those of necrotic <jats:italic>E. gazella<\/jats:italic> tissue and surrounding environments. While the healthy octocoral microbiome was distinguished by so-far uncultivated <jats:italic>Endozoicomonadaceae<\/jats:italic>, <jats:italic>Oceanospirillales<\/jats:italic>, and <jats:italic>Alteromonadales<\/jats:italic> phylotypes in all host species, a pronounced increase of <jats:italic>Flavobacteriaceae<\/jats:italic> and <jats:italic>Alphaproteobacteria<\/jats:italic>, originating from seawater, was observed in necrotic <jats:italic>E. gazella<\/jats:italic> tissue. Increased abundances of eukaryotic-like proteins, exonucleases, restriction endonucleases, CRISPR\/Cas proteins, and genes encoding for heat-shock proteins, inorganic ion transport, and iron storage distinguished the prokaryotic communities of healthy octocoral tissue regardless of the host species. An increase of arginase and nitric oxide reductase genes, observed in necrotic <jats:italic>E. gazella<\/jats:italic> tissues, suggests the existence of a mechanism for suppression of nitrite oxide production by which octocoral pathogens may overcome the host\u2019s immune system.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>This is the first study to employ primer-less, shotgun metagenome sequencing to unveil the taxonomic, functional, and secondary metabolism features of prokaryotic communities in octocorals. Our analyses reveal that the octocoral microbiome is distinct from those of the environmental surroundings, is host genus (but not species) specific, and undergoes large, complex structural changes in the transition to the dysbiotic state. Host-symbiont recognition, abiotic-stress response, micronutrient acquisition, and an antiviral defense arsenal comprising multiple restriction endonucleases, CRISPR\/Cas systems, and phage lysogenization regulators are signatures of prokaryotic communities in octocorals. We argue that these features collectively contribute to the stabilization of symbiosis in the octocoral holobiont and constitute beneficial traits that can guide future studies on coral reef conservation and microbiome therapy.<\/jats:p>\n                \n              <\/jats:sec>","DOI":"10.1186\/s40168-021-01031-y","type":"journal-article","created":{"date-parts":[[2021,3,25]],"date-time":"2021-03-25T16:03:08Z","timestamp":1616688188000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":70,"title":["Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals"],"prefix":"10.1186","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3702-9192","authenticated-orcid":false,"given":"T.","family":"Keller-Costa","sequence":"first","affiliation":[]},{"given":"A.","family":"Lago-Lest\u00f3n","sequence":"additional","affiliation":[]},{"given":"J. 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This study was exempt from ethical approval procedures according to the current Portuguese legislation. All procedures involving animals were in accordance with the ethical standards of the institution (Centre of Marine Sciences (CCMAR), Faro, Portugal) at which the coral samples were processed. This study did not involve endangered or protected octocoral species (according to the IUCN red list of threatened species, 02\/11\/2019: ). The sampling of octocorals did not occur within privately owned or protected areas. Sampling procedures were minimally intrusive and preserved octocoral colonies at the field site.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"72"}}