Nested Formation of Calcium Carbonate Polymorphs in a Bacterial Surface Membrane with a Graded Nanoconfinement: An Evolutionary Strategy to Ensure Bacterial Survival

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Paul Simon - , Max Planck Institute for Chemical Physics of Solids (Author)
  • Wolfgang Pompe - , Dresden University of Technology (Author)
  • Denise Gruner - , Dresden University of Technology (Author)
  • Elena Sturm - , Max Planck Institute for Chemical Physics of Solids (Author)
  • Kai Ostermann - , Environmental Monitoring and Endocrinology (Research Group) (Author)
  • Sabine Matys - , Helmholtz-Zentrum Dresden-Rossendorf (Author)
  • Manja Vogel - , Helmholtz-Zentrum Dresden-Rossendorf (Author)
  • Gerhard Roedel - (Author)

Abstract

It is the intention of this study to elucidate the nested formation of calcium carbonate polymorphs or polyamorphs in the different nanosized compartments. With these observations, it can be concluded how the bacteria can survive in a harsh environment with high calcium carbonate supersaturation. The mechanisms of calcium carbonate precipitation at the surface membrane and at the underlying cell wall membrane of the thermophilic soil bacterium Geobacillus stearothermophilus DSM 13240 have been revealed by high-resolution transmission electron microscopy and atomic force microscopy. In this Gram-positive bacterium, nanopores in the surface layer (S-layer) and in the supporting cell wall polymers are nucleation sites for metastable calcium carbonate polymorphs and polyamorphs. In order to observe the different metastable forms, various reaction times and a low reaction temperature (4 °C) have been chosen. Calcium carbonate polymorphs nucleate in the confinement of nanosized pores (3-5 nm) of the S-layer. The hydrous crystalline calcium carbonate (ikaite) is formed initially with [110] as the favored growth direction. It transforms into the anhydrous metastable vaterite by a solid-state transition. In a following reaction step, calcite is precipitated, caused by dissolution of vaterite in the aqueous solution. In the larger pores of the cell wall (20-50 nm), hydrated amorphous calcium carbonate is grown, which transforms into metastable monohydrocalcite, aragonite, or calcite. Due to the sequence of reaction steps via various metastable phases, the bacteria gain time for chipping the partially mineralized S-layer, and forming a fresh S-layer (characteristic growth time about 20 min). Thus, the bacteria can survive in solutions with high calcium carbonate supersaturation under the conditions of forced biomineralization.

Details

Original languageEnglish
Pages (from-to)526-539
Number of pages14
JournalACS biomaterials science & engineering
Volume8
Issue number2
Early online date7 Jan 2022
Publication statusPublished - 14 Feb 2022
Peer-reviewedYes

External IDs

Scopus 85123916142
PubMed 34995442
Mendeley 701d1937-7933-34d9-9c45-8e2eefd23975
unpaywall 10.1021/acsbiomaterials.1c01280

Keywords

ASJC Scopus subject areas

Keywords

  • S-layer, peptidoglycan layer, nanostructures, calcium carbonate, forced biomineralization, HR-TEM, GRAM-POSITIVE BACTERIA, CELL-WALL POLYMERS, S-LAYER, X-RAY, CRYSTAL-STRUCTURE, TRANSFORMATION, VATERITE, CRYSTALLIZATION, IKAITE, CACO3, Water, Calcium Carbonate/chemistry, Bacteria