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A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [2];  [3];  [3];  [4];  [2];  [5];  [6];  [6];  [7];  [7];  [8];  [8];  [3]
  1. Philipps Univ. of Marburg (Germany). LOEWE Research Center for Synthetic Microbiology (SYNMIKRO)
  2. Ludwig Maximilian Univ., Munich (Germany). Biocenter LMU. Plant Development and Electron Microscopy
  3. Univ. of Regensburg (Germany). Center for Electron Microscopy
  4. Univ. of Regensburg (Germany). Inst. of Experimental and Applied Physics
  5. Univ. of Bayreuth (Germany). Cell Biology and Electron Microscopy
  6. Indiana Univ., Bloomington, IN (United States). Molecular and Cellular Biochemistry Dept.
  7. Univ. of Regensburg (Germany). Microbiology Dept.
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Microbiology Dept.
Based on serial sectioning, focused ion beam scanning electron microscopy (FIB/SEM), and electron tomography, we depict in detail the highly unusual anatomy of the marine hyperthermophilic crenarchaeon, Ignicoccus hospitalis. Our data support a complex and dynamic endomembrane system consisting of cytoplasmic protrusions, and with secretory function. Moreover, we reveal that the cytoplasm of the putative archaeal ectoparasite Nanoarchaeum equitans can get in direct contact with this endomembrane system, complementing and explaining recent proteomic, transcriptomic and metabolomic data on this inter-archaeal relationship. In addition, we identified a matrix of filamentous structures and/or tethers in the voluminous inter-membrane compartment (IMC) of I. hospitalis, which might be responsible for membrane dynamics. Overall, this unusual cellular compartmentalization, ultrastructure and dynamics in an archaeon that belongs to the recently proposed TACK superphylum prompts speculation that the eukaryotic endomembrane system might originate from Archaea.
Research Organization:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Philipps Univ. of Marburg (Germany); Univ. of Regensburg (Germany); Univ. of Tennessee, Knoxville, TN (United States)
Sponsoring Organization:
German Research Foundation (DFG) (Germany); National Science Foundation (NSF) (United States); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Wellcome Trust (United Kingdom)
Contributing Organization:
Indiana Univ., Bloomington, IN (United States); Ludwig Maximilian Univ., Munich (Germany); Univ. of Bayreuth (Germany)
Grant/Contract Number:
SC0006654
OSTI ID:
1364327
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 8; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (79)

Archaeal Cells book January 2013
Localization of gold in biological tissue: A photochemical method for light and electronmicroscopy journal January 1981
Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I journal September 2004
Insight into the proteome of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis: the major cytosolic and membrane proteins journal June 2008
Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography journal July 2008
Cultivation of hyperthermophilic archaea in capillary tubes resulting in improved preservation of fine structures journal October 1997
Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis journal November 2014
Coats, Tethers, Rabs, and SNAREs Work Together to Mediate the Intracellular Destination of a Transport Vesicle journal May 2007
Automated electron microscope tomography using robust prediction of specimen movements journal October 2005
The archaeal ‘TACK’ superphylum and the origin of eukaryotes journal December 2011
Bacterial Vesicle Secretion and the Evolutionary Origin of the Eukaryotic Endomembrane System journal July 2016
The effects of model choice and mitigating bias on the ribosomal tree of life journal October 2013
Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans journal July 2014
Asgard archaea illuminate the origin of eukaryotic cellular complexity journal January 2017
Evolution of diverse cell division and vesicle formation systems in Archaea journal September 2010
Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons journal August 2019
The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure and composition journal April 2004
The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells journal January 2009
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell journal January 2013
A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis journal May 2008
A unique cell division machinery in the Archaea journal November 2008
The archaebacterial origin of eukaryotes journal December 2008
Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis journal February 2010
Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. journal June 1984
Globally optimal stitching of tiled 3D microscopic image acquisitions journal April 2009
Archaeal “Dark Matter” and the Origin of Eukaryotes journal February 2014
Extending the Conserved Phylogenetic Core of Archaea Disentangles the Evolution of the Third Domain of Life journal February 2015
Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes journal September 2010
A congruent phylogenomic signal places eukaryotes within the Archaea journal October 2012
The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods journal August 2009
Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov journal November 2000
Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans' journal April 2007
The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes journal April 2014
A pyramid approach to subpixel registration based on intensity journal January 1998
The dominating outer membrane protein of the hyperthermophilic Archaeum Ignicoccus hospitalis: a novel pore-forming complex journal January 2007
A Role for the ESCRT System in Cell Division in Archaea journal December 2008
Insights into the Autotrophic CO2 Fixation Pathway of the Archaeon Ignicoccus hospitalis: Comprehensive Analysis of the Central Carbon Metabolism journal March 2007
Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea journal December 2007
The Iho670 Fibers of Ignicoccus hospitalis Are Anchored in the Cell by a Spherical Structure Located beneath the Inner Membrane journal August 2014
AMP-Forming Acetyl Coenzyme A Synthetase in the Outermost Membrane of the Hyperthermophilic Crenarchaeon Ignicoccus hospitalis journal January 2012
Overproduction of fumarate reductase in Escherichia coli induces a novel intracellular lipid-protein organelle. journal January 1984
Anaerobic Expression of Escherichia coli Succinate Dehydrogenase: Functional Replacement of Fumarate Reductase in the Respiratory Chain during Anaerobic Growth journal November 1998
In Vivo Observation of Cell Division of Anaerobic Hyperthermophiles by Using a High-Intensity Dark-Field Microscope journal August 1999
Three-Dimensional Electron Microscopic Imaging of Membrane Invaginations in Escherichia coli Overproducing the Chemotaxis Receptor Tsr journal July 2004
The ultrastructure of Ignicoccus : Evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon journal January 2002
Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer journal January 2012
A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans journal January 2008
A bacterial tubulovesicular network journal November 2013
Phylogenomics of Prokaryotic Ribosomal Proteins journal May 2012
"Parasitoid" Species and Assemblages: Convenient Definitions or Misleading Compromises? journal December 1990
S-layer and cytoplasmic membrane – exceptions from the typical archaeal cell wall with a focus on double membranes journal November 2014
Data from: The effects of model choice and mitigating bias on the ribosomal tree of life dataset January 2013
Computer Visualization of Three-Dimensional Image Data Using IMOD journal January 1996
Localization of gold in biological tissue: A photochemical method for light and electronmicroscopy journal January 1981
Complex Evolution of the Mismatch Repair System in Eukaryotes is Illuminated by Novel Archaeal Genomes journal January 2021
Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components journal October 2008
The unusual cell biology of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis journal June 2012
Analysis of the Ultrastructure of Archaea by Electron Microscopy book January 2010
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont journal May 2002
An archaeal origin of eukaryotes supports only two primary domains of life journal December 2013
The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells journal January 2009
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell journal January 2013
The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure and composition journal October 2004
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism journal October 2003
Insights into the Autotrophic CO2 Fixation Pathway of the Archaeon Ignicoccus hospitalis: Comprehensive Analysis of the Central Carbon Metabolism journal March 2007
Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea journal December 2007
The Iho670 Fibers of Ignicoccus hospitalis Are Anchored in the Cell by a Spherical Structure Located beneath the Inner Membrane journal August 2014
AMP-Forming Acetyl Coenzyme A Synthetase in the Outermost Membrane of the Hyperthermophilic Crenarchaeon Ignicoccus hospitalis journal January 2012
Overproduction of fumarate reductase in Escherichia coli induces a novel intracellular lipid-protein organelle. journal January 1984
Anaerobic Expression of Escherichia coli Succinate Dehydrogenase: Functional Replacement of Fumarate Reductase in the Respiratory Chain during Anaerobic Growth journal November 1998
In Vivo Observation of Cell Division of Anaerobic Hyperthermophiles by Using a High-Intensity Dark-Field Microscope journal August 1999
Three-Dimensional Electron Microscopic Imaging of Membrane Invaginations in Escherichia coli Overproducing the Chemotaxis Receptor Tsr journal July 2004
The prokaryotic V4R domain is the likely ancestor of a key component of the eukaryotic vesicle transport system journal January 2008
Phylogenomics of prokaryotic ribosomal proteins journal January 2011
Three-Dimensional Reconstruction of Bacteria with a Complex Endomembrane System journal May 2013
Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship journal August 2011
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. text January 2019
Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon "Ignicoccus hospitalis" text January 2010
Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship text January 2011

Cited By (9)

Unexpected host dependency of Antarctic Nanohaloarchaeota journal June 2019
Genomic diversity, lifestyles and evolutionary origins of DPANN archaea journal January 2019
Extracellular membrane vesicles in the three domains of life and beyond journal November 2018
Are Antarctic Nanohaloarchaeota Emerging Viral Lineages? preprint November 2019
Two or three domains: a new view of tree of life in the genomics era journal February 2018
An archaeal symbiont-host association from the deep terrestrial subsurface journal May 2019
Targeted isolation and cultivation of uncultivated bacteria by reverse genomics journal September 2019
FIB-SEM imaging properties of Drosophila melanogaster tissues embedded in Lowicryl HM20: FIB-SEM OF DROSOPHILA TISSUES journal November 2018
Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis journal September 2018

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