Nanoscale Tungsten-MicrobialInterface of the Metal ImmobilizingThermoacidophilic ArchaeonMetallosphaera sedula CultivatedWith Tungsten Polyoxometalate

Tetyana Milojevic, Mihaela Albu, Amir Blazevic, Nadila Gumerova, Lukas Konrad, Norbert Cyran

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Inorganic systems based upon polyoxometalate (POM) clusters provide an experimentalapproach to develop artificial life. These artificial symmetric anionic macromoleculeswith oxidometalate polyhedra as building blocks were shown to be well suitedas inorganic frameworks for complex self-assembling and organizing systems withemergent properties. Analogously to mineral cells based on iron sulfides, POMs areconsidered as inorganic cells in facilitating prelife chemical processes and displaying“life-like” characteristics. However, the relevance of POMs to life-sustaining processes(e.g., microbial respiration) has not yet been addressed, while iron sulfides are verywell known as ubiquitous mineral precursors and energy sources for chemolithotrophicmetabolism. Metallosphaera sedula is an extreme metallophilic and thermoacidophilicarchaeon, which flourishes in hot acid and respires by metal oxidation. In the presentstudy we provide our observations on M. sedula cultivated on tungsten polyoxometalate(W-POM). The decomposition of W-POM macromolecular clusters and the appearanceof low molecular weight W species (e.g., WO) in the presence of M. sedula havebeen detected by electrospray ionization mass spectrometry (ESI-MS) analysis. Here,we document the presence of metalloorganic assemblages at the interface betweenM. sedula and W-POM resolved down to the nanometer scale using scanningand transmission electron microscopy (SEM and TEM) coupled to electron energyloss spectroscopy (EELS). High-resolution TEM (HR-TEM) and selected-area electrondiffraction (SAED) patterns indicated the deposition of redox heterogeneous tungstenspecies on the S-layer of M. sedula along with the accumulation of intracellulartungsten-bearing nanoparticles, i.e., clusters of tungsten atoms. These results revealthe effectiveness of the analytical spectroscopy coupled to the wet chemistry approachas a tool in the analysis of metal–microbial interactions and microbial cultivationon supramolecular self-assemblages based on inorganic metal clusters. We discussthe possible mechanism of W-POM decomposition by M. sedula in light of uniqueelectrochemical properties of POMs. The findings presented herein highlight uniquemetallophilicity in hostile environments, extending our knowledge of the relevance ofPOMs to life-sustaining processes, understanding of the transition of POMs as inorganicprebiotic model to life-sustainable material precursors and revealing biogenic signaturesobtained after the decomposition of an artificial inorganic compound, which previouslywas not associated with any living matter.
Original languageEnglish
Article number1267
Number of pages15
JournalFrontiers in Microbiology
Volume10
DOIs
Publication statusPublished - 7 Jun 2019

ASJC Scopus subject areas

  • Materials Science(all)

Fields of Expertise

  • Advanced Materials Science

Treatment code (Nähere Zuordnung)

  • Basic - Fundamental (Grundlagenforschung)

Cite this

Nanoscale Tungsten-MicrobialInterface of the Metal ImmobilizingThermoacidophilic ArchaeonMetallosphaera sedula CultivatedWith Tungsten Polyoxometalate. / Milojevic, Tetyana; Albu, Mihaela; Blazevic, Amir; Gumerova, Nadila; Konrad, Lukas; Cyran, Norbert.

In: Frontiers in Microbiology , Vol. 10, 1267, 07.06.2019.

Research output: Contribution to journalArticleResearchpeer-review

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abstract = "Inorganic systems based upon polyoxometalate (POM) clusters provide an experimentalapproach to develop artificial life. These artificial symmetric anionic macromoleculeswith oxidometalate polyhedra as building blocks were shown to be well suitedas inorganic frameworks for complex self-assembling and organizing systems withemergent properties. Analogously to mineral cells based on iron sulfides, POMs areconsidered as inorganic cells in facilitating prelife chemical processes and displaying“life-like” characteristics. However, the relevance of POMs to life-sustaining processes(e.g., microbial respiration) has not yet been addressed, while iron sulfides are verywell known as ubiquitous mineral precursors and energy sources for chemolithotrophicmetabolism. Metallosphaera sedula is an extreme metallophilic and thermoacidophilicarchaeon, which flourishes in hot acid and respires by metal oxidation. In the presentstudy we provide our observations on M. sedula cultivated on tungsten polyoxometalate(W-POM). The decomposition of W-POM macromolecular clusters and the appearanceof low molecular weight W species (e.g., WO) in the presence of M. sedula havebeen detected by electrospray ionization mass spectrometry (ESI-MS) analysis. Here,we document the presence of metalloorganic assemblages at the interface betweenM. sedula and W-POM resolved down to the nanometer scale using scanningand transmission electron microscopy (SEM and TEM) coupled to electron energyloss spectroscopy (EELS). High-resolution TEM (HR-TEM) and selected-area electrondiffraction (SAED) patterns indicated the deposition of redox heterogeneous tungstenspecies on the S-layer of M. sedula along with the accumulation of intracellulartungsten-bearing nanoparticles, i.e., clusters of tungsten atoms. These results revealthe effectiveness of the analytical spectroscopy coupled to the wet chemistry approachas a tool in the analysis of metal–microbial interactions and microbial cultivationon supramolecular self-assemblages based on inorganic metal clusters. We discussthe possible mechanism of W-POM decomposition by M. sedula in light of uniqueelectrochemical properties of POMs. The findings presented herein highlight uniquemetallophilicity in hostile environments, extending our knowledge of the relevance ofPOMs to life-sustaining processes, understanding of the transition of POMs as inorganicprebiotic model to life-sustainable material precursors and revealing biogenic signaturesobtained after the decomposition of an artificial inorganic compound, which previouslywas not associated with any living matter.",
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AU - Albu, Mihaela

AU - Blazevic, Amir

AU - Gumerova, Nadila

AU - Konrad, Lukas

AU - Cyran, Norbert

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