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 c...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01072/full
_version_ 1819157528988090368
author 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
Louie Wurch
Mircea Podar
Mircea Podar
Reinhard Rachel
author_facet 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
Louie Wurch
Mircea Podar
Mircea Podar
Reinhard Rachel
author_sort Thomas Heimerl
collection DOAJ
description 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.
first_indexed 2024-12-22T16:10:12Z
format Article
id doaj.art-e66308ba27d147eaadbd019c4688c1ba
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-22T16:10:12Z
publishDate 2017-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-e66308ba27d147eaadbd019c4688c1ba2022-12-21T18:20:30ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-06-01810.3389/fmicb.2017.01072256456A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitansThomas Heimerl0Jennifer Flechsler1Carolin Pickl2Veronika Heinz3Benjamin Salecker4Josef Zweck5Gerhard Wanner6Stefan Geimer7Rachel Y. Samson8Stephen D. Bell9Harald Huber10Reinhard Wirth11Louie Wurch12Louie Wurch13Mircea Podar14Mircea Podar15Reinhard Rachel16LOEWE Research Center for Synthetic Microbiology (SYNMIKRO), Philipps University of MarburgMarburg, GermanyPlant Development and Electron Microscopy, Biocenter LMUMunich, GermanyPlant Development and Electron Microscopy, Biocenter LMUMunich, GermanyCenter for Electron Microscopy, University of RegensburgRegensburg, GermanyCenter for Electron Microscopy, University of RegensburgRegensburg, GermanyInstitute of Experimental and Applied Physics, University of RegensburgRegensburg, GermanyPlant Development and Electron Microscopy, Biocenter LMUMunich, GermanyCell Biology and Electron Microscopy, University of BayreuthBayreuth, GermanyMolecular and Cellular Biochemistry Department, Indiana UniversityBloomington, IN, United StatesMolecular and Cellular Biochemistry Department, Indiana UniversityBloomington, IN, United StatesMicrobiology Department, University of RegensburgRegensburg, GermanyMicrobiology Department, University of RegensburgRegensburg, GermanyBiosciences Division, Oak Ridge National LaboratoryOak Ridge, TN, United StatesMicrobiology Department, University of TennesseeKnoxville, TN, United StatesBiosciences Division, Oak Ridge National LaboratoryOak Ridge, TN, United StatesMicrobiology Department, University of TennesseeKnoxville, TN, United StatesCenter for Electron Microscopy, University of RegensburgRegensburg, GermanyBased 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01072/fullArchaeaultrastructure3DeukaryogenesisFIB/SEMelectron tomography
spellingShingle 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
Louie Wurch
Mircea Podar
Mircea Podar
Reinhard Rachel
A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
Frontiers in Microbiology
Archaea
ultrastructure
3D
eukaryogenesis
FIB/SEM
electron tomography
title A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
title_full A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
title_fullStr A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
title_full_unstemmed A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
title_short A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
title_sort complex endomembrane system in the archaeon ignicoccus hospitalis tapped by nanoarchaeum equitans
topic Archaea
ultrastructure
3D
eukaryogenesis
FIB/SEM
electron tomography
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01072/full
work_keys_str_mv AT thomasheimerl acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT jenniferflechsler acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT carolinpickl acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT veronikaheinz acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT benjaminsalecker acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT josefzweck acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT gerhardwanner acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT stefangeimer acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT rachelysamson acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT stephendbell acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT haraldhuber acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT reinhardwirth acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT louiewurch acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT louiewurch acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT mirceapodar acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT mirceapodar acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT reinhardrachel acomplexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT thomasheimerl complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT jenniferflechsler complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT carolinpickl complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT veronikaheinz complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT benjaminsalecker complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT josefzweck complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT gerhardwanner complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT stefangeimer complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT rachelysamson complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT stephendbell complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT haraldhuber complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT reinhardwirth complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT louiewurch complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT louiewurch complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT mirceapodar complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT mirceapodar complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans
AT reinhardrachel complexendomembranesysteminthearchaeonignicoccushospitalistappedbynanoarchaeumequitans