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Macroalgal microbiomes unveil a valuable genetic resource for halogen metabolism

2024-03-07Journal article Open access
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dc.contributor.authorLavecchia, Anna
dc.contributor.authorFosso, Bruno
dc.contributor.authorEngelen, Aschwin
dc.contributor.authorBorin, Sara
dc.contributor.authorManzari, Caterina
dc.contributor.authorPicardi, Ernesto
dc.contributor.authorPesole, Graziano
dc.contributor.authorPlacido, Antonio
dc.date.accessioned2024-04-02T11:03:34Z
dc.date.available2024-04-02T11:03:34Z
dc.date.issued2024-03-07
dc.date.updated2024-04-01T06:25:29Z
dc.description.abstractBackground Macroalgae, especially reds (Rhodophyta Division) and browns (Phaeophyta Division), are known for producing various halogenated compounds. Yet, the reasons underlying their production and the fate of these metabolites remain largely unknown. Some theories suggest their potential antimicrobial activity and involvement in interactions between macroalgae and prokaryotes. However, detailed investigations are currently missing on how the genetic information of prokaryotic communities associated with macroalgae may influence the fate of organohalogenated molecules. Results To address this challenge, we created a specialized dataset containing 161 enzymes, each with a complete enzyme commission number, known to be involved in halogen metabolism. This dataset served as a reference to annotate the corresponding genes encoded in both the metagenomic contigs and 98 metagenome-assembled genomes (MAGs) obtained from the microbiome of 2 red (Sphaerococcus coronopifolius and Asparagopsis taxiformis) and 1 brown (Halopteris scoparia) macroalgae. We detected many dehalogenation-related genes, particularly those with hydrolytic functions, suggesting their potential involvement in the degradation of a wide spectrum of halocarbons and haloaromatic molecules, including anthropogenic compounds. We uncovered an array of degradative gene functions within MAGs, spanning various bacterial orders such as Rhodobacterales, Rhizobiales, Caulobacterales, Geminicoccales, Sphingomonadales, Granulosicoccales, Microtrichales, and Pseudomonadales. Less abundant than degradative functions, we also uncovered genes associated with the biosynthesis of halogenated antimicrobial compounds and metabolites. Conclusion The functional data provided here contribute to understanding the still largely unexplored role of unknown prokaryotes. These findings support the hypothesis that macroalgae function as holobionts, where the metabolism of halogenated compounds might play a role in symbiogenesis and act as a possible defense mechanism against environmental chemical stressors. Furthermore, bacterial groups, previously never connected with organohalogen metabolism, e.g., Caulobacterales, Geminicoccales, Granulosicoccales, and Microtrichales, functionally characterized through MAGs reconstruction, revealed a biotechnologically relevant gene content, useful in synthetic biology, and bioprospecting applications.pt_PT
dc.description.sponsorshipINMARE (H2020-BG-04-2014, GA 634486); ELIXIR FOE (CUP B53C22000690005); e Blue Bioeconomy Pact with the project Algae Vertical N° C6449 5664-00000026;pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationMicrobiome. 2024 Mar 07;12(1):47pt_PT
dc.identifier.doi10.1186/s40168-023-01740-6pt_PT
dc.identifier.eissn2049-2618
dc.identifier.urihttp://hdl.handle.net/10400.1/20556
dc.language.isoengpt_PT
dc.language.rfc3066en
dc.peerreviewedyespt_PT
dc.publisherBMCpt_PT
dc.relationAlgarve Centre for Marine Sciences
dc.relationAlgarve Centre for Marine Sciences
dc.relationCentre for Marine and Environmental Research
dc.relationNot Available
dc.rights.holderThe Author(s)
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.subjectHolobiontpt_PT
dc.subjectMacroalgaept_PT
dc.subjectSphaerococcus coronopifoliuspt_PT
dc.subjectAsparagopsis taxiformispt_PT
dc.subjectHalopteris scopariapt_PT
dc.subjectMicrobiomept_PT
dc.subjectMetagenome-assembled genomes (MAGs)pt_PT
dc.subjectOrganohalogenspt_PT
dc.subjectHalogenationpt_PT
dc.subjectDehalogenationpt_PT
dc.titleMacroalgal microbiomes unveil a valuable genetic resource for halogen metabolismpt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleAlgarve Centre for Marine Sciences
oaire.awardTitleAlgarve Centre for Marine Sciences
oaire.awardTitleCentre for Marine and Environmental Research
oaire.awardTitleNot Available
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDB%2F04326%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDP%2F04326%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/LA%2FP%2F0101%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/CEEC INST 2018/CEECINST%2F00114%2F2018%2FCP1492%2FCT0001/PT
oaire.citation.issue1pt_PT
oaire.citation.startPage47pt_PT
oaire.citation.titleMicrobiomept_PT
oaire.citation.volume12pt_PT
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStreamCEEC INST 2018
person.familyNameEngelen
person.givenNameAschwin
person.identifier.ciencia-id911A-9A0C-744D
person.identifier.orcid0000-0002-9579-9606
person.identifier.ridM-3432-2013
person.identifier.scopus-author-id6701622770
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
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
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
relation.isAuthorOfPublication33d5a223-f2c9-4c68-984f-9213f15a05b0
relation.isAuthorOfPublication.latestForDiscovery33d5a223-f2c9-4c68-984f-9213f15a05b0
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relation.isProjectOfPublication.latestForDiscovery794d4c77-c731-471e-bc96-5a41dcd3d872

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