Grappling archaea: ultrastructural analyses of an uncultivated, cold-loving archaeon, and its biofilm

Abstract

Similarly to Bacteria, Archaea are microorganisms that interact with their surrounding environment in a versatile manner. To date, interactions based on cellular structure and surface appendages have mainly been documented using model systems of cultivable archaea under laboratory conditions. Here, we report on the microbial interactions and ultrastructural features of the uncultivated SM1 Euryarchaeon, which is highly dominant in its biotope. Therefore, biofilm samples taken from the Sippenauer Moor, Germany, were investigated via transmission electron microscopy (TEM; negative staining, thin-sectioning) and scanning electron microscopy (SEM) in order to elucidate the fine structures of the microbial cells and the biofilm itself. The biofilm consisted of small archaeal cocci (0.6 μm diameter), arranged in a regular pattern (1.0–2.0 μm distance from cell to cell), whereas each archaeon was connected to 6 other archaea on average. Extracellular polymeric substances (EPS) were limited to the close vicinity of the archaeal cells, and specific cell surface appendages (hami, Moissl et al., 2005) protruded beyond the EPS matrix enabling microbial interaction by cell-cell contacts among the archaea and between archaea and bacteria. All analyzed hami revealed their previously described architecture of nano-grappling hooks and barb-wire basal structures. Considering the archaeal cell walls, the SM1 Euryarchaea exhibited a double-membrane, which has rarely been reported for members of this phylogenetic domain. Based on these findings, the current generalized picture on archaeal cell walls needs to be revisited, as archaeal cell structures are more complex and sophisticated than previously assumed, particularly when looking into the uncultivated majority.

Archaeal type IV pili and their involvement in biofilm formation

“…The archaea also express a wide variety of additional, structurally diverse adhesion filaments. These filaments include the Mth60 fimbriae of Methanothermobacter thermautotrophicus ( Thoma et al, 2008 ), 5 nm diameter filaments that adhere to organic surfaces such as chitin, the cannulae, 25 nm diameter hollow tubes that are found on the hyperthermophilic Pyrodictium , which mediate interactions between cells ( Horn et al, 1999 ), and the hami of SM1 euryarchaea, which form grappling hooks that allow attachment to surfaces in cold sulfurous marshes ( Perras et al, 2014 ).…”

S-layer and cytoplasmic membrane – exceptions from the typical archaeal cell wall with a focus on double membranes

“…In addition, the finding of an energized outermost cellular membrane in the well described Ignicoccus hospitalis and related species already indicated the possibility of an outer membrane (OM), as it is present in Gram-negative bacteria. Furthermore, recent results on the SM1 euryarchaeon, ultra-small ARMAN cells and Methanomassiliicoccus luminyensis strengthened the idea of a real archaeal OM and, besides others, will also be discussed here ( Comolli et al, 2009 ; Dridi et al, 2012 ; Perras et al, 2014 ). And in this concern, the possible functions of an OM in regard to the bacterial version as well as challenges concerning energetic problems become apparent.…”

“…Interestingly, a common feature of all archaea that posses a double membrane cell wall architecture is that they are closely interacting with other organisms (archaea, bacteria, eukaryotes), as already mentioned by Perras et al (2014) , and that they are difficult to cultivate or even not cultivatable at all. At this point, it can still be discussed if the S-layer ( Albers and Meyer, 2011 ) or an OM is the more archaic cell wall compound.…”

“…The thick transparent layer mentioned in this study might depict the periplasm of Methanomassiliicoccus luminyensis . In a recent study concerning the ultrastructure of the cold-loving archaeal isolate SM1, an outer cellular membrane in addition to the cytoplasmic membrane could be documented as well ( Perras et al, 2014 ).…”

Intra- and inter-species interactions in microbial communities

“…Perras et al (2014) examined uncultivated biofilms taken directly from a natural sulfidic marsh (Sippenauer Moor near Regensburg, Bavaria, Germany) by transmission and scanning electron microscopy (TEM and SEM). The dominant SM1 Euryarchaeon uses thin appendages to connect to other cells of the same species forming a network in which each cell has an average of six connections, but also connects to cells of other species.…”