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

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.
Authors:
 [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.
Publication Date:
Grant/Contract Number:
SC0006654; DEB-1134877; HU 703/2; 086045/Z/08/Z
Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Research Org:
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Philipps Univ. of Marburg (Germany); Univ. of Regensburg (Germany)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); German Research Foundation (DFG); Wellcome Trust (United Kingdom)
Contributing Orgs:
Ludwig Maximilian Univ., Munich (Germany); Univ. of Bayreuth (Germany); Indiana Univ., Bloomington, IN (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Archaea; ultrastructure; 3D; eukaryogenesis; FIB/SEM; electron tomography; symbiosis; membranes
OSTI Identifier:
1364327

Heimerl, Thomas, Flechsler, Jennifer, Pickl, Carolin, Heinz, Veronika, Salecker, Benjamin, Zweck, Josef, Wanner, Gerhard, Geimer, Stefan, Samson, Rachel Y., Bell, Stephen D., Huber, Harald, Wirth, Reinhard, Wurch, Louie, Podar, Mircea, and Rachel, Reinhard. A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans. United States: N. p., Web. doi:10.3389/fmicb.2017.01072.
Heimerl, Thomas, Flechsler, Jennifer, Pickl, Carolin, Heinz, Veronika, Salecker, Benjamin, Zweck, Josef, Wanner, Gerhard, Geimer, Stefan, Samson, Rachel Y., Bell, Stephen D., Huber, Harald, Wirth, Reinhard, Wurch, Louie, Podar, Mircea, & Rachel, Reinhard. A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans. United States. doi:10.3389/fmicb.2017.01072.
Heimerl, Thomas, Flechsler, Jennifer, Pickl, Carolin, Heinz, Veronika, Salecker, Benjamin, Zweck, Josef, Wanner, Gerhard, Geimer, Stefan, Samson, Rachel Y., Bell, Stephen D., Huber, Harald, Wirth, Reinhard, Wurch, Louie, Podar, Mircea, and Rachel, Reinhard. 2017. "A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans". United States. doi:10.3389/fmicb.2017.01072. https://www.osti.gov/servlets/purl/1364327.
@article{osti_1364327,
title = {A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans},
author = {Heimerl, Thomas and Flechsler, Jennifer and Pickl, Carolin and Heinz, Veronika and Salecker, Benjamin and Zweck, Josef and Wanner, Gerhard and Geimer, Stefan and Samson, Rachel Y. and Bell, Stephen D. and Huber, Harald and Wirth, Reinhard and Wurch, Louie and Podar, Mircea and Rachel, Reinhard},
abstractNote = {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.},
doi = {10.3389/fmicb.2017.01072},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {6}
}

Works referenced in this record:

A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis
journal, May 2008
  • Huber, H.; Gallenberger, M.; Jahn, U.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 22, p. 7851-7856
  • DOI: 10.1073/pnas.0801043105