Phylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seeps

Handle URI:
http://hdl.handle.net/10754/622450
Title:
Phylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seeps
Authors:
Skennerton, Connor T.; Haroon, Mohamed; Briegel, Ariane; Shi, Jian; Jensen, Grant J.; Tyson, Gene W.; Orphan, Victoria J.
Abstract:
Tenericutes are a unique class of bacteria that lack a cell wall and are typically parasites or commensals of eukaryotic hosts. Environmental 16S rDNA surveys have identified a number of tenericute clades in diverse environments, introducing the possibility that these Tenericutes may represent non-host-associated, free-living microorganisms. Metagenomic sequencing of deep-sea methane seep sediments resulted in the assembly of two genomes from a Tenericutes-affiliated clade currently known as 'NB1-n' (SILVA taxonomy) or 'RF3' (Greengenes taxonomy). Metabolic reconstruction revealed that, like cultured members of the Mollicutes, these 'NB1-n' representatives lack a tricarboxylic acid cycle and instead use anaerobic fermentation of simple sugars for substrate level phosphorylation. Notably, the genomes also contained a number of unique metabolic features including hydrogenases and a simplified electron transport chain containing an RNF complex, cytochrome bd oxidase and complex I. On the basis of the metabolic potential predicted from the annotated genomes, we devised an anaerobic enrichment media that stimulated the growth of these Tenericutes at 10 °C, resulting in a mixed culture where these organisms represented ∼60% of the total cells by targeted fluorescence in situ hybridization (FISH). Visual identification by FISH confirmed these organisms were not directly associated with Eukaryotes and electron cryomicroscopy of cells in the enrichment culture confirmed an ultrastructure consistent with the defining phenotypic property of Tenericutes, with a single membrane and no cell wall. On the basis of their unique gene content, phylogenetic placement and ultrastructure, we propose these organisms represent a novel class within the Tenericutes, and suggest the names Candidatus 'Izimaplasma sp. HR1' and Candidatus 'Izimaplasma sp. HR2' for the two genome representatives.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Skennerton CT, Haroon MF, Briegel A, Shi J, Jensen GJ, et al. (2016) Phylogenomic analysis of Candidatus “Izimaplasma” species: free-living representatives from a Tenericutes clade found in methane seeps. The ISME Journal 10: 2679–2692. Available: http://dx.doi.org/10.1038/ismej.2016.55.
Publisher:
Springer Nature
Journal:
The ISME Journal
Issue Date:
8-Apr-2016
DOI:
10.1038/ismej.2016.55
Type:
Article
ISSN:
1751-7362; 1751-7370
Sponsors:
This work is funded by the Gordon and Betty Moore Foundation through Grant GBMF3780 and the US Department of Energy, Office of Science, Office of Biological Environmental Research under award numbers DESC0003940 and DE-SC0010574 (to VJO). Additional support was provided by Caltech's Center for Environmental Microbial Interactions and the Howard Hughes Medical Institute. We thank D Smith, S Scheller, S Zinder, J Hemp and D Newman for helpful discussions and M Imelfort for bioinformatics assistance. GWT was supported by an ARC Queen Elizabeth II fellowship (ARC-DP1093175)
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorSkennerton, Connor T.en
dc.contributor.authorHaroon, Mohameden
dc.contributor.authorBriegel, Arianeen
dc.contributor.authorShi, Jianen
dc.contributor.authorJensen, Grant J.en
dc.contributor.authorTyson, Gene W.en
dc.contributor.authorOrphan, Victoria J.en
dc.date.accessioned2017-01-02T09:28:32Z-
dc.date.available2017-01-02T09:28:32Z-
dc.date.issued2016-04-08en
dc.identifier.citationSkennerton CT, Haroon MF, Briegel A, Shi J, Jensen GJ, et al. (2016) Phylogenomic analysis of Candidatus “Izimaplasma” species: free-living representatives from a Tenericutes clade found in methane seeps. The ISME Journal 10: 2679–2692. Available: http://dx.doi.org/10.1038/ismej.2016.55.en
dc.identifier.issn1751-7362en
dc.identifier.issn1751-7370en
dc.identifier.doi10.1038/ismej.2016.55en
dc.identifier.urihttp://hdl.handle.net/10754/622450-
dc.description.abstractTenericutes are a unique class of bacteria that lack a cell wall and are typically parasites or commensals of eukaryotic hosts. Environmental 16S rDNA surveys have identified a number of tenericute clades in diverse environments, introducing the possibility that these Tenericutes may represent non-host-associated, free-living microorganisms. Metagenomic sequencing of deep-sea methane seep sediments resulted in the assembly of two genomes from a Tenericutes-affiliated clade currently known as 'NB1-n' (SILVA taxonomy) or 'RF3' (Greengenes taxonomy). Metabolic reconstruction revealed that, like cultured members of the Mollicutes, these 'NB1-n' representatives lack a tricarboxylic acid cycle and instead use anaerobic fermentation of simple sugars for substrate level phosphorylation. Notably, the genomes also contained a number of unique metabolic features including hydrogenases and a simplified electron transport chain containing an RNF complex, cytochrome bd oxidase and complex I. On the basis of the metabolic potential predicted from the annotated genomes, we devised an anaerobic enrichment media that stimulated the growth of these Tenericutes at 10 °C, resulting in a mixed culture where these organisms represented ∼60% of the total cells by targeted fluorescence in situ hybridization (FISH). Visual identification by FISH confirmed these organisms were not directly associated with Eukaryotes and electron cryomicroscopy of cells in the enrichment culture confirmed an ultrastructure consistent with the defining phenotypic property of Tenericutes, with a single membrane and no cell wall. On the basis of their unique gene content, phylogenetic placement and ultrastructure, we propose these organisms represent a novel class within the Tenericutes, and suggest the names Candidatus 'Izimaplasma sp. HR1' and Candidatus 'Izimaplasma sp. HR2' for the two genome representatives.en
dc.description.sponsorshipThis work is funded by the Gordon and Betty Moore Foundation through Grant GBMF3780 and the US Department of Energy, Office of Science, Office of Biological Environmental Research under award numbers DESC0003940 and DE-SC0010574 (to VJO). Additional support was provided by Caltech's Center for Environmental Microbial Interactions and the Howard Hughes Medical Institute. We thank D Smith, S Scheller, S Zinder, J Hemp and D Newman for helpful discussions and M Imelfort for bioinformatics assistance. GWT was supported by an ARC Queen Elizabeth II fellowship (ARC-DP1093175)en
dc.publisherSpringer Natureen
dc.titlePhylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seepsen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalThe ISME Journalen
dc.contributor.institutionDivision of Geological and Planetary Sciences, California Institute of Technology, 1200 East California Blvd, MC 100-23, Pasadena, CA, 91125, United Statesen
dc.contributor.institutionAustralian Center for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, QLD, Australiaen
dc.contributor.institutionDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, United Statesen
dc.contributor.institutionSylvius Laboratorium, Leiden University, Sylviusweg 72, Leiden, 23333 BE, Netherlandsen
dc.contributor.institutionHoward Hughes Medical Institute, California Institute of Technology, Pasadena, CA, United Statesen
dc.contributor.institutionAdvanced Water Management Center, University of Queensland, St Lucia, QLD, Australiaen
kaust.authorHaroon, Mohameden
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