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

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    Type
    Article
    Authors
    Skennerton, Connor T.
    Haroon, Mohamed
    Briegel, Ariane
    Shi, Jian
    Jensen, Grant J.
    Tyson, Gene W.
    Orphan, Victoria J.
    KAUST Department
    Red Sea Research Center (RSRC)
    Date
    2016-04-08
    Online Publication Date
    2016-04-08
    Print Publication Date
    2016-11
    Permanent link to this record
    http://hdl.handle.net/10754/622450
    
    Metadata
    Show full item record
    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.
    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.
    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)
    Publisher
    Springer Nature
    Journal
    The ISME Journal
    DOI
    10.1038/ismej.2016.55
    ae974a485f413a2113503eed53cd6c53
    10.1038/ismej.2016.55
    Scopus Count
    Collections
    Articles; Red Sea Research Center (RSRC)

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