Archaea S‐layer nanotube from a “black smoker” in complex with cyclo‐octasulfur (S₈) rings

Abstract

Elemental sulfur exists primarily as an S80 ring and serves as terminal electron acceptor for a variety of sulfur-fermenting bacteria. Hyperthermophilic archaea from black smoker vents are an exciting research tool to advance our knowledge of sulfur respiration under extreme conditions. Here, we use a hybrid method approach to demonstrate that the proteinaceous cavities of the S-layer nanotube of the hyperthermophilic archaeon Staphylothermus marinus act as a storage reservoir for cyclo-octasulfur S8. Fully atomistic molecular dynamics (MD) simulations were performed and the method of multiconfigurational thermodynamic integration was employed to compute the absolute free energy for transferring a ring of elemental sulfur S8 from an aqueous bath into the largest hydrophobic cavity of a fragment of archaeal tetrabrachion. Comparisons with earlier MD studies of the free energy of hydration as a function of water occupancy in the same cavity of archaeal tetrabrachion show that the sulfur ring is energetically favored over water.

Energetics of Storage and Diffusion of Water and Cyclo-Octasulfur for a Nonpolar Cavity of RHCC Tetrabrachion by Molecular Dynamics Simulations

“…All molecular dynamics simulations of RHCC − water complexes were based on a higher pressure structure PDB 1YBK which was crystallized at P = 15 atm and T = 273 K , and which contained clusters of 13 water molecules in cavity 2 and 8 water molecules in cavity 3. All simulations of the RHCC − cyclo − octasulfur complex were based on the structure PDB 5JR5 [ 11 ] which was crystallized at T = 277 K and which contained a single crown-shaped S 8 ring in cavity 2 with a geometry similar to crystalline α − S 8 and two competing equal-occupancy conformations in cavity 3, one similar to the twisted-ring S 8 arrangement and one in the exo − endo − S 8 arrangement. For both complexes, this investigation was focused exclusively on cavity 3 and its contents and the twisted-ring conformation of S 8 was selected for analysis.…”

“…(1) by setting n = 1. In order to obtain a calculated solvation free energy for S 8 which matched the measured solvation free energy Δ G sol exp ( S 8 ) = + 15.5 kJ / mol [ 11 ], it was necessary to increase the repulsive van der Waals parameter C 12 for atomic sulfur by a factor of 1.25, leading to a modified set of non-bonded LJ parameters σ = (1.25) 1/6 σ 0 and ε = (1.25) −1 ε 0 relative to the values ( σ 0 = 0.356359 nm , ε 0 = 1.04600 kJ / mol ) generated by ACPYPE. This yielded a calculated solvation free energy for S 8 of Δ G sol cal ( S 8 ) = − Δ G sol 1→0 ( S 8 ) = + 13.4 ± 1.4 kJ / mol .…”

“…However, the extreme hydrophobicity and poor solubility of sulfur in water (5 μg L −1 at T = 25 0 C ) make it a poor substrate for bacterial sulfur respiration. Recent X-ray crystallography, dynamic light scattering and molecular dynamic simulations [ 11 ] performed on crystallized RHCC tetrabrachion after immersing it in a sulfur-rich environment for an extended period of time at an elevated temperature T = 353 K (PDB structure 5JR5) have indicated that it is highly likely that the larger cavities 2 and 3 of RHCC tetrabrachion in its native environment do not contain water clusters but instead contain crowns of cyclooctasulfur S 8 , the most common allotrope of sulfur. This expectation is further reinforced by the remarkable similarity between the geometries of the clathrate water ring and the α − S 8 sulfur crown.…”

Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins

“…Slayer proteins (SLPs) are generally 40-200 kDa and represent up to 15% of total cellular protein production [4]. S-layers serve as the first selective barrier between the cell and its environment, which includes interactions with predators, symbionts, proteins, nutrients, and energy sources [5]. Bacterial S-layers have been linked to diverse functions, including protection from large macromolecules and predators, biofilm formation, adhesion, and pathogenesis [6].…”

CRISPR-mediated gene silencing reveals involvement of the archaeal S-layer in cell division and virus infection

“…Correspondingly, it represents a first docking site for a number of extracellular molecules such as nutrients, vesicles, cells, and viruses 3,5 . Indeed, only recently, S-layer glycoproteins of hyperthermophilic archaea have been shown to accumulate iron and sulfur from the environment 27,28 . Also, recent studies revealed S-layer glycosylation to be crucial for cell-to-cell interactions during the mating process of the archaeon Haloferax 29 and comparative genomics suggest a within-niche variation of glycosylation enabling Haloferax to discriminate between such mating partners and also viruses 30 .…”