Comparative genomic analysis reveals a diverse repertoire of genes involved in prokaryote-eukaryote interactions within the Pseudovibrio Genus

dc.contributor.authorRomano, Stefano
dc.contributor.authorFernàndez-Guerra, Antonio
dc.contributor.authorReen, F. Jerry
dc.contributor.authorGlöckner, Frank O.
dc.contributor.authorCrowley, Susan P.
dc.contributor.authorO'Sullivan, Orla
dc.contributor.authorCotter, Paul D.
dc.contributor.authorAdams, Claire
dc.contributor.authorDobson, Alan D. W.
dc.contributor.authorO'Gara, Fergal
dc.contributor.funderEuropean Commission
dc.contributor.funderScience Foundation Ireland
dc.contributor.funderDepartment of Agriculture, Food and the Marine
dc.contributor.funderIrish Research Council for Science, Engineering and Technology
dc.contributor.funderHealth Research Board
dc.contributor.funderIrish Thoracic Society
dc.contributor.funderMarine Institute
dc.contributor.funderTeagasc
dc.date.accessioned2017-06-20T11:39:46Z
dc.date.available2017-06-20T11:39:46Z
dc.date.issued2016-03-30
dc.description.abstractStrains of the Pseudovibrio genus have been detected worldwide, mainly as part of bacterial communities associated with marine invertebrates, particularly sponges. This recurrent association has been considered as an indication of a symbiotic relationship between these microbes and their host. Until recently, the availability of only two genomes, belonging to closely related strains, has limited the knowledge on the genomic and physiological features of the genus to a single phylogenetic lineage. Here we present 10 newly sequenced genomes of Pseudovibrio strains isolated from marine sponges from the west coast of Ireland, and including the other two publicly available genomes we performed an extensive comparative genomic analysis. Homogeneity was apparent in terms of both the orthologous genes and the metabolic features shared amongst the 12 strains. At the genomic level, a key physiological difference observed amongst the isolates was the presence only in strain P. axinellae AD2 of genes encoding proteins involved in assimilatory nitrate reduction, which was then proved experimentally. We then focused on studying those systems known to be involved in the interactions with eukaryotic and prokaryotic cells. This analysis revealed that the genus harbors a large diversity of toxin-like proteins, secretion systems and their potential effectors. Their distribution in the genus was not always consistent with the phylogenetic relationship of the strains. Finally, our analyses identified new genomic islands encoding potential toxin-immunity systems, previously unknown in the genus. Our analyses shed new light on the Pseudovibrio genus, indicating a large diversity of both metabolic features and systems for interacting with the host. The diversity in both distribution and abundance of these systems amongst the strains underlines how metabolically and phylogenetically similar bacteria may use different strategies to interact with the host and find a niche within its microbiota. Our data suggest the presence of a sponge-specific lineage of Pseudovibrio. The reduction in genome size and the loss of some systems potentially used to successfully enter the host, leads to the hypothesis that P. axinellae strain AD2 may be a lineage that presents an ancient association with the host and that may be vertically transmitted to the progeny.en
dc.description.sponsorshipScience Foundation Ireland (SSPC-2, 12/RC/2275; 13/TIDA/B2625; 12/TIDA/B2411; 12/TIDA/B2405; 14/TIDA/2438); Department of Agriculture, Food and the Marine (FIRM/RSF/CoFoRD; FIRM 08/RDC/629; FIRM 1/F009/MabS; FIRM 13/F/516); Irish Research Council for Science, Engineering and Technology (PD/2011/2414;<s></s>GOIPG/2014/647); Health Research Board/Irish Thoracic Society (MRCG-2014-6); Marine Institute (Beaufort award C2CRA 2007/082); Teagasc (Walsh Fellowship 2013)en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.articleid387
dc.identifier.citationRomano, S., Fernàndez-Guerra, A., Reen, F. J., Glöckner, F. O., Crowley, S. P., O'Sullivan, O., Cotter, P. D., Adams, C., Dobson, A. D. W. and O'Gara, F. (2016) 'Comparative genomic analysis reveals a diverse repertoire of genes involved in prokaryote-eukaryote interactions within the Pseudovibrio Genus', Frontiers in Microbiology, 7, 387 (20pp.). doi: 10.3389/fmicb.2016.00387en
dc.identifier.doi10.3389/fmicb.2016.00387
dc.identifier.endpage20
dc.identifier.issn1664-302X
dc.identifier.journaltitleFrontiers in Microbiologyen
dc.identifier.startpage1
dc.identifier.urihttps://hdl.handle.net/10468/4114
dc.identifier.volume7
dc.language.isoenen
dc.publisherFrontiers Mediaen
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP3::PEOPLE/607786/EU/BluePharmTrain/BLUEPHARMTRAIN
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP1::KBBE/312184/EU/Increasing Value and Flow in the Marine Biodiscovery Pipeline/PHARMASEA
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP1::KBBE/311975/EU/Marine Microorganisms: Cultivation Methods for Improving their Biotechnological Applications/MACUMBA
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP1::KBBE/287589/EU/Marine Microbial Biodiversity, Bioinformatics and Biotechnology/MICRO B3
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP3::PEOPLE/256596/EU/Dissecting the role of a novel transcriptional regulator in microbial-host interactomes./MEXT REGULATION
dc.relation.projectinfo:eu-repo/grantAgreement/EC/H2020::IA/634486/EU/Industrial Applications of Marine Enzymes: Innovative screening and expression platforms to discover and use the functional protein diversity from the sea/INMARE
dc.relation.urihttp://journal.frontiersin.org/article/10.3389/fmicb.2016.00387/full
dc.rights© 2016, Romano, Fernàndez-Guerra, Reen, Glöckner, Crowley, O'Sullivan, Cotter, Adams, Dobson and O'Gara. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these termsen
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/en
dc.subjectPseudovibrioen
dc.subjectComparative genomicsen
dc.subjectSymbiosisen
dc.subjectSecretion systemsen
dc.subjectToxinsen
dc.subjectCore-genomeen
dc.subjectPhylogenesisen
dc.titleComparative genomic analysis reveals a diverse repertoire of genes involved in prokaryote-eukaryote interactions within the Pseudovibrio Genusen
dc.typeArticle (peer-reviewed)en
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