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Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

2022-09-22Journal article Open access
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dc.contributor.authorKeller-Costa, Tina
dc.contributor.authorKozma, Lydia
dc.contributor.authorSilva, Sandra G.
dc.contributor.authorToscan, Rodolfo
dc.contributor.authorGonçalves, Jorge Manuel Santos
dc.contributor.authorLago-Lestón, Asunción
dc.contributor.authorKyrpides, Nikos C.
dc.contributor.authorNunes da Rocha, Ulisses
dc.contributor.authorCosta, Rodrigo
dc.date.accessioned2022-10-01T11:22:56Z
dc.date.available2022-10-01T11:22:56Z
dc.date.issued2022-09-22
dc.date.updated2022-10-01T03:32:16Z
dc.description.abstractThe role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater. Results Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity. Conclusion This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large.pt_PT
dc.description.sponsorshipVH-NG-1248 Micro ‘Big Data; FA_05_2017_032; DE-AC02-05CH11231
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationMicrobiome. 2022 Sep 22;10(1):151pt_PT
dc.identifier.doi10.1186/s40168-022-01343-7pt_PT
dc.identifier.eissn2049-2618
dc.identifier.urihttp://hdl.handle.net/10400.1/18324
dc.language.isoengpt_PT
dc.language.rfc3066eng
dc.peerreviewedyespt_PT
dc.publisherBMCpt_PT
dc.relationHarnessing the catalyst power of host-microbe interactions: a quest for novel chitinases from octocoral symbionts
dc.relationInstitute for Bioengineering and Biosciences
dc.relationInstitute for Bioengineering and Biosciences
dc.relationInstitute for Health and Bioeconomy
dc.relationNot Available
dc.relationSecondary metabolite biosynthesis by Aquimarina species: emerging properties and bioactivities from rare marine biosphere
dc.rights.holderThe Author(s)
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.titleMetagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiomept_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleHarnessing the catalyst power of host-microbe interactions: a quest for novel chitinases from octocoral symbionts
oaire.awardTitleInstitute for Bioengineering and Biosciences
oaire.awardTitleInstitute for Bioengineering and Biosciences
oaire.awardTitleInstitute for Health and Bioeconomy
oaire.awardTitleNot Available
oaire.awardTitleSecondary metabolite biosynthesis by Aquimarina species: emerging properties and bioactivities from rare marine biosphere
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/EXPL%2FMAR-EST%2F1664%2F2013/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/EXPL%2FBIA-MIC%2F0286%2F2021/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDB%2F04565%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDP%2F04565%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/LA%2FP%2F0140%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/CEEC IND 2017/CEECIND%2F00788%2F2017%2FCP1461%2FCT0008/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT//PD%2FBD%2F143029%2F2018/PT
oaire.citation.issue1pt_PT
oaire.citation.startPage151pt_PT
oaire.citation.titleMicrobiomept_PT
oaire.citation.volume10pt_PT
oaire.fundingStream3599-PPCDT
oaire.fundingStream3599-PPCDT
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStreamCEEC IND 2017
person.familyNameGonçalves
person.familyNameVieira Costa
person.givenNameJorge Manuel Santos
person.givenNameRodrigo
person.identifier356846
person.identifier.ciencia-id1013-ED6A-65EB
person.identifier.ciencia-id3615-5B1C-57FC
person.identifier.orcid0000-0001-7704-8190
person.identifier.orcid0000-0002-6400-9077
person.identifier.ridG-5206-2011
person.identifier.scopus-author-id7103326116
project.funder.identifierhttp://doi.org/10.13039/501100001871
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project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
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