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Comparative metagenomics reveals the distinctive adaptive features of the Spongia officinalis endosymbiotic consortium

2017-12Journal article Open access
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dc.contributor.authorKarimi, Elham
dc.contributor.authorRamos, Miguel
dc.contributor.authorGonçalves, Jorge Manuel Santos
dc.contributor.authorXavier, Joana R.
dc.contributor.authorReis, Margarida
dc.contributor.authorCosta, Rodrigo
dc.date.accessioned2018-12-07T14:52:53Z
dc.date.available2018-12-07T14:52:53Z
dc.date.issued2017-12
dc.description.abstractCurrent knowledge of sponge microbiome functioning derives mostly from comparative analyses with bacterioplankton communities. We employed a metagenomics-centered approach to unveil the distinct features of the Spongia officinalis endosymbiotic consortium in the context of its two primary environmental vicinities. Microbial metagenomic DNA samples (n = 10) from sponges, seawater, and sediments were subjected to Hiseq Illumina sequencing (c. 15 million 100 bp reads per sample). Totals of 10,272 InterPro (IPR) predicted protein entries and 784 rRNA gene operational taxonomic units (OTUs, 97% cut-off) were uncovered from all metagenomes. Despite the large divergence in microbial community assembly between the surveyed biotopes, the S. officinalis symbiotic community shared slightly greater similarity (p < 0.05), in terms of both taxonomy and function, to sediment than to seawater communities. The vast majority of the dominant S. officinalis symbionts (i.e., OTUs), representing several, so-far uncultivable lineages in diverse bacterial phyla, displayed higher residual abundances in sediments than in seawater. CRISPR-Cas proteins and restriction endonucleases presented much higher frequencies (accompanied by lower viral abundances) in sponges than in the environment. However, several genomic features sharply enriched in the sponge specimens, including eukaryotic-like repeat motifs (ankyrins, tetratricopeptides, WD-40, and leucine-rich repeats), and genes encoding for plasmids, sulfatases, polyketide synthases, type IV secretion proteins, and terpene/terpenoid synthases presented, to varying degrees, higher frequencies in sediments than in seawater. In contrast, much higher abundances of motility and chemotaxis genes were found in sediments and seawater than in sponges. Higher cell and surface densities, sponge cell shedding and particle uptake, and putative chemical signaling processes favoring symbiont persistence in particulate matrices all may act as mechanisms underlying the observed degrees of taxonomic connectivity and functional convergence between sponges and sediments. The reduced frequency of motility and chemotaxis genes in the sponge microbiome reinforces the notion of a prevalent mutualistic mode of living inside the host. This study highlights the S. officinalis "endosymbiome" as a distinct consortium of uncultured prokaryotes displaying a likely "sit-and-wait" strategy to nutrient foraging coupled to sophisticated anti-viral defenses, unique natural product biosynthesis, nutrient utilization and detoxification capacities, and both microbe-microbe and host-microbe gene transfer amenability.
dc.description.sponsorshipPortuguese Foundation for Science and Technology (FCT) [PTDC/BIA-MIC/3865/2012, PTDC/MAR-BIO/1547/2014]; Education, Audiovisual and Culture Executive Agency (European Commission, Erasmus Mundus Programme) [EMA2 lot7/SALA1206422]
dc.description.sponsorshipEMA2 lot7/SALA1206422
dc.description.versioninfo:eu-repo/semantics/publishedVersion
dc.identifier.doi10.3389/fmicb.2017.02499
dc.identifier.issn1664-302X
dc.identifier.urihttp://hdl.handle.net/10400.1/11254
dc.language.isoeng
dc.peerreviewedyes
dc.publisherFrontiers Media
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
dc.subjectCell genomics reveals
dc.subjectMarine sponges
dc.subjectBacterial communities
dc.subjectMicrobial symbionts
dc.subjectMediterranean Sea
dc.subjectDiversity
dc.subjectGene
dc.subjectPoribacteria
dc.subjectTransmission
dc.subjectChemotaxis
dc.titleComparative metagenomics reveals the distinctive adaptive features of the Spongia officinalis endosymbiotic consortium
dc.typejournal article
dspace.entity.typePublication
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/PTDC%2FBIA-MIC%2F3865%2F2012/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/Projetos de Investigação Científica e Desenvolvimento Tecnológico - 2014/PTDC%2FMAR-BIO%2F1547%2F2014/PT
oaire.citation.startPage2499
oaire.citation.titleFrontiers In Microbiology
oaire.citation.volume8
oaire.fundingStream3599-PPCDT
oaire.fundingStreamProjetos de Investigação Científica e Desenvolvimento Tecnológico - 2014
person.familyNameKarimi
person.familyNameGonçalves
person.familyNameReis
person.familyNameda Silva Costa
person.givenNameElham
person.givenNameJorge Manuel Santos
person.givenNameMargarida
person.givenNameRodrigo
person.identifier458972
person.identifier356846
person.identifier115920
person.identifier.ciencia-id1013-ED6A-65EB
person.identifier.ciencia-id5917-D500-D251
person.identifier.orcid0000-0002-2204-0789
person.identifier.orcid0000-0001-7704-8190
person.identifier.orcid0000-0003-0552-0868
person.identifier.orcid0000-0002-5932-4101
person.identifier.ridG-5206-2011
person.identifier.ridN-7274-2013
person.identifier.scopus-author-id7103326116
person.identifier.scopus-author-id25623703900
person.identifier.scopus-author-id7203063627
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
rcaap.rightsopenAccess
rcaap.typearticle
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