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

Skennerton, Connor T. and Haroon, Mohamed F. and Briegel, Ariane and Shi, Jian and Jensen, Grant J. and Tyson, Gene W. and Orphan, Victoria J. (2016) Phylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seeps. ISME Journal, 10 (11). pp. 2679-2692. ISSN 1751-7362. PMCID PMC5113845. http://resolver.caltech.edu/CaltechAUTHORS:20160418-080655842

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1038/ismej.2016.55DOIArticle
http://www.nature.com/ismej/journal/v10/n11/full/ismej201655a.htmlPublisherArticle
http://www.nature.com/ismej/journal/v10/n11/suppinfo/ismej201655s1.htmlPublisherSupplementary Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5113845/PubMed CentralArticle
ORCID:
AuthorORCID
Skennerton, Connor T.0000-0003-1320-4873
Briegel, Ariane0000-0003-3733-3725
Jensen, Grant J.0000-0003-1556-4864
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2016 International Society for Microbial Ecology. Received 13 January 2016; Revised 29 February 2016; Accepted 4 March 2016; Advance online publication 8 April 2016. 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 DE-SC0003940 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). The authors declare no conflict of interest.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationGBMF3780
Department of Energy (DOE)DE-SC0003940
Department of Energy (DOE)DE-SC0010574
CaltechUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Australian Research CouncilDP1093175
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
PubMed Central ID:PMC5113845
Record Number:CaltechAUTHORS:20160418-080655842
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160418-080655842
Official Citation:Phylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seeps Connor T Skennerton, Mohamed F Haroon, Ariane Briegel, Jian Shi, Grant J Jensen, Gene W Tyson, and Victoria J Orphan The ISME Journal (2016) 10, 2679–2692; doi:10.1038/ismej.2016.55
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:66226
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:18 Apr 2016 15:35
Last Modified:23 Apr 2019 22:02

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