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.
Highlights
The genus Ignicoccus belongs to the Desulfurococcaceae within the Crenarchaeota
Our study addresses the 3D ultrastructure of I. hospitalis cells, with a special focus on the complex membrane system, and the interaction site with cells of N. equitans
From 3D models of whole I. hospitalis cells based on focused ion beam scanning electron microscopy (FIB/SEM) and electron tomography, the volume of the inter-membrane compartment (IMC) generally makes up ∼40% of the whole cell volume
Summary
The genus Ignicoccus belongs to the Desulfurococcaceae within the Crenarchaeota. The genus comprises three species—I. hospitalis (Paper et al, 2007), I. islandicus, and I. pacificus (Huber et al, 2000). A strain was isolated from the Alvin diving expedition to the East Pacific Ridge in 2008, MEX13A. They were all isolated from submarine hydrothermal vent systems or black smokers and are anaerobic, hyperthermophilic, obligate chemolithoautotrophs with an optimal growth temperature of 90◦C. As an obligate energy source, Ignicoccus cells reduce elemental sulfur using molecular hydrogen as an electron donor. Carbon fixation is thought to occur via the dicarboxylate/4-hydroxybutyrate pathway (Jahn et al, 2007; Huber et al, 2008)
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