A complex prokaryotic endomembrane system

Abstract

Compartmentation is generally considered a feature of eukaryotic cells. One exception in the “prokaryotic world” is the marine hyperthermophilic Crenarchaeon Ignicococcus that exhibits a large inter‐membrane compartment (IMC) between an inner (cytoplasmic) and an outer (cellular) membrane (CM and OCM) [1]. In addition, I. hospitalis supports the propagation of another archaeon ‐ Nanoarchaeum equitans ‐ on its surface [2]. Cryopreparation in combination with 3D methods (serial sectioning, FIB/SEM and electron tomography) enabled us to deliver a comprehensive insight into the anatomy of I. hopitalis and its contact to N. equitans . The 3D‐models obtained, reveal a highly complex and dynamic endogenous membrane system with putative secretory function: The IMC makes up ~40% of the whole cell volume on average, but in few cells, it can reach an extent much larger than the volume of the cytoplasm. In the IMC, elongated protrusions of the cytoplasm are present. Apparently, these structures can constrict from or fuse with the CM or themselves. We also observed interactions of these protrusions with the OM via macromolecular, cylindrically shaped complexes. All interacting structures are connected via thin filaments (~3‐6 nm in diameter), that span through the whole IMC and are presumably responsible for membrane dynamics. In addition, homologues in sequence and/or structure to eukaryotic proteins can be found in Ignicoccus , that are putatively involved in the system like their eukaryotic counterparts: small GTPases (Sar1/Arf like), Coatomer proteins, Sec61ß, proteins of the ESCRT‐III system, a tethering complex component (Bet3) and the ATPase CDC48/p97 [3, 4]. Since Ignicoccus belongs to the recently proposed TACK superphylum, that is considered a sister group of eukaryotes [5], it is also tempting to speculate about a prokaryotic origin of the eukaryotic endogenous membrane system. Regarding the contact of N. equitans to I. hospitalis, a fusion of cytoplasms of both organisms was revealed, providing an important complement and explanation to recent proteomic [4], transcriptomic [6] and metabolomic [7] studies on this inter‐archaeal system.