A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans

Thomas Heimerl; Jennifer Flechsler; Carolin Pickl; Veronika Heinz; Benjamin Salecker; Josef Zweck; Gerhard Wanner; Stefan Geimer; Rachel Y. Samson; Stephen D. Bell; Harald Huber; Reinhard Wirth; Louie Wurch; Mircea Podar; Reinhard Rachel

doi:10.3389/fmicb.2017.01072

A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans

Thomas Heimerl, Jennifer Flechsler, Carolin Pickl, Veronika Heinz, Benjamin Salecker, Josef Zweck, Gerhard Wanner, Stefan Geimer, Rachel Y. Samson, Stephen D. Bell, Harald Huber, Reinhard Wirth, Louie Wurch, Mircea Podar, Reinhard Rachel

Integrative Microbiomics

Research output: Contribution to journal › Article › peer-review

47 Scopus citations

Abstract

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.

Original language	English
Article number	1072
Journal	Frontiers in Microbiology
Volume	8
Issue number	JUN
DOIs	https://doi.org/10.3389/fmicb.2017.01072
State	Published - Jun 13 2017

Funding

This project was partially funded by the DFG grant HU 703/2, by the U.S. Department of Energy grant DE-SC0006654, by the National Science Foundation grant DEB1134877 and by the Wellcome Trust (Programme Grant 086045/Z/08/Z). The excellent technical support by M. Lange, K. Eichinger, T. Hader, C. Meese, and A. Foith from Regensburg; C. Niemann from Munich; and the continuous support by R. Witzgall, M. Thomm, and W. Minuth from Regensburg; M. Keller from Oak Ridge; and U. Maier from Marburg is gratefully acknowledged.

Keywords

3D
Archaea
Electron tomography
Eukaryogenesis
FIB/SEM
Membranes
Symbiosis
Ultrastructure

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10.3389/fmicb.2017.01072

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Heimerl, T., Flechsler, J., Pickl, C., Heinz, V., Salecker, B., Zweck, J., Wanner, G., Geimer, S., Samson, R. Y., Bell, S. D., Huber, H., Wirth, R., Wurch, L., Podar, M., & Rachel, R. (2017). A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Frontiers in Microbiology, 8(JUN), Article 1072. https://doi.org/10.3389/fmicb.2017.01072

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abstract = "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.",

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AB - 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.

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A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans

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