Preservation of Archaeal Surface Layer Structure During Mineralization

Abstract

Proteinaceous surface layers (S-layers) are highly ordered, crystalline structures commonly found in prokaryotic cell envelopes that augment their structural stability and modify interactions with metals in the environment. While mineral formation associated with S-layers has previously been noted, the mechanisms were unconstrained. Using Sulfolobus acidocaldarius a hyperthermophilic archaeon native to metal-enriched environments and possessing a cell envelope composed only of a S-layer and a lipid cell membrane, we describe a passive process of iron phosphate nucleation and growth within the S-layer of cells and cell-free S-layer “ghosts” during incubation in a Fe-rich medium, independently of metabolic activity. This process followed five steps: (1) initial formation of mineral patches associated with S-layer; (2) patch expansion; (3) patch connection; (4) formation of a continuous mineral encrusted layer at the cell surface; (5) early stages of S-layer fossilization via growth of the extracellular mineralized layer and the mineralization of cytosolic face of the cell membrane. At more advanced stages of encrustation, encrusted outer membrane vesicles are formed, likely in an attempt to remove damaged S-layer proteins. The S-layer structure remains strikingly well preserved even upon the final step of encrustation, offering potential biosignatures to be looked for in the fossil record.

Microbe‐Mediated Extracellular and Intracellular Mineralization: Environmental, Industrial, and Biotechnological Applications

“…B) Reproduced under the terms of the CC‐BY Creative Commons Attribution 4.0 International license ( http://creativecommons.org/licenses/by/4.0/). [ 162 ] Copyright 2016, Springer Nature.…”

“…Post‐nucleation mineralization of the hyperthermophilic archaeon, Sulfolobus acidocaldarius , for example, begins with extracellular mineralization outside the proteinaceous surface layer (S‐layer) and subsequently beneath the S‐layer within the cytosol (Figure 1b). [ 162 ] After nucleation (step #1), mineral portions in form of domes are synthesized over the initial portions of the S‐layer/mineral assemblies (step #2), which is followed by the fusion of the mineral assemblies (step #3). In this manner, the entire cell surface is eventually covered by a continuous mineral layer, leaving behind a nonmineralized layer related to the original S‐layer (step #4).…”

“…Fossilization of the S‐layer subsequently occurs through the extracellular mineralized layer and intracellular mineralization occurs on the cell membrane beneath the S‐layer (step #5). [ 162 ]…”

Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions

“…This hypothesis was, however, never fully tested. Since 57 then, S-layer nucleation of mineralization has been observed in a range of bacteria (Konhauser et al,58 1994; Phoenix et al, 2000) and archaea (Kish et al, 2016). 59 S-layer mineralization is a mechanism for metallotolerance with potential application in 60 bioremediation.…”

Revealing S-layer Functions in the Hyperthermophilic Crenarchaeon Sulfolobus islandicus

“…The current S-layer model in Sulfolobus shows a “stalk-and-cap” relationship between SlaA and SlaB, with SlaB as the stalk anchoring SlaA to the cytoplasmic membrane, forming a crystal matrix that constitutes the outermost layer covering the whole cell (22). Instability of the S-layer in Sulfolobus has been associated with changes in cell shape (24) and budding of vesicles (25, 26). It has been proposed that the archaeal S-layer assists the cell against turgor pressure (1, 9).…”