Tellurite Adsorption onto Bacterial Surfaces

Goff, Jennifer L.; Wang, Yuwei; Boyanov, Maxim I.; Yu, Qiang; Kemner, Kenneth M.; Fein, Jeremy B.; Yee, Nathan

doi:10.1021/acs.est.1c01001

Title: Tellurite Adsorption onto Bacterial Surfaces

Abstract

Tellurium (Te) is an emerging contaminant and its chemical transformation in the environment is strongly influenced by microbial processes. In this study, we investigated the adsorption of tellurite [Te(IV), TeO₃^2-] onto the common soil bacterium Bacillus subtilis. Thiol-blocking experiments were carried out to investigate the role of cell surface sulfhydryl sites in tellurite binding, and extended X-ray absorption fine structure (EXAFS) spectroscopy was performed to determine the chemical speciation of the adsorbed tellurite. The results indicate that tellurite reacts with sulfhydryl functional groups in the extracellular polymeric substances (EPS) produced by B. subtilis. Upon binding to sulfhydryl sites in the EPS, the Te changes from Te-O bonds to Te-S coordination. Further analysis of the surface-associated molecules shows that the EPS of B. subtilis contain proteins. Removal of the proteinaceous EPS dramatically decreases tellurite adsorption and the sulfhydryl surface site concentration. These findings indicate that sulfhydryl binding in EPS plays a key role in tellurite adsorption on bacterial surfaces.

Authors:

Goff, Jennifer L. ^[1]; Wang, Yuwei ^[2];

^[3];

^[4]; Kemner, Kenneth M. ^[5]; Fein, Jeremy B. ^[4];

^[6]

Rutgers Univ., Piscataway, NJ (United States)
Rutgers Univ., New Brunswick, NJ (United States)
Bulgarian Academy of Sciences, Sofia (Bulgaria); Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Notre Dame, IN (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)
Rutgers Univ., Piscataway, NJ (United States); Rutgers Univ., New Brunswick, NJ (United States)

Publication Date:: Mon Jul 19 00:00:00 EDT 2021

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

OSTI Identifier:: 1844541

Grant/Contract Number:: AC02-06CH11357; EAR-1530089; EAR-1904192

Resource Type:: Accepted Manuscript

Journal Name:: Environmental Science and Technology

Additional Journal Information:: Journal Volume: 55; Journal Issue: 15; Journal ID: ISSN 0013-936X

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 54 ENVIRONMENTAL SCIENCES; tellurium; metalloid; extracellular polymeric substances; CdTe; photovoltaic; sulfhydryl; toxicity; X-ray adsorption spectroscopy

Citation Formats


                    Goff, Jennifer L., Wang, Yuwei, Boyanov, Maxim I., Yu, Qiang, Kemner, Kenneth M., Fein, Jeremy B., and Yee, Nathan. Tellurite Adsorption onto Bacterial Surfaces.  United States: N. p., 2021. 
Web.  doi:10.1021/acs.est.1c01001.

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                    Goff, Jennifer L., Wang, Yuwei, Boyanov, Maxim I., Yu, Qiang, Kemner, Kenneth M., Fein, Jeremy B., & Yee, Nathan. Tellurite Adsorption onto Bacterial Surfaces.  United States.  https://doi.org/10.1021/acs.est.1c01001

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                    Goff, Jennifer L., Wang, Yuwei, Boyanov, Maxim I., Yu, Qiang, Kemner, Kenneth M., Fein, Jeremy B., and Yee, Nathan. Mon .  
"Tellurite Adsorption onto Bacterial Surfaces".  United States.  https://doi.org/10.1021/acs.est.1c01001.  https://www.osti.gov/servlets/purl/1844541.

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@article{osti_1844541,

  title        = {Tellurite Adsorption onto Bacterial Surfaces},

  author       = {Goff, Jennifer L. and Wang, Yuwei and Boyanov, Maxim I. and Yu, Qiang and Kemner, Kenneth M. and Fein, Jeremy B. and Yee, Nathan},

  abstractNote = {Tellurium (Te) is an emerging contaminant and its chemical transformation in the environment is strongly influenced by microbial processes. In this study, we investigated the adsorption of tellurite [Te(IV), TeO32-] onto the common soil bacterium Bacillus subtilis. Thiol-blocking experiments were carried out to investigate the role of cell surface sulfhydryl sites in tellurite binding, and extended X-ray absorption fine structure (EXAFS) spectroscopy was performed to determine the chemical speciation of the adsorbed tellurite. The results indicate that tellurite reacts with sulfhydryl functional groups in the extracellular polymeric substances (EPS) produced by B. subtilis. Upon binding to sulfhydryl sites in the EPS, the Te changes from Te-O bonds to Te-S coordination. Further analysis of the surface-associated molecules shows that the EPS of B. subtilis contain proteins. Removal of the proteinaceous EPS dramatically decreases tellurite adsorption and the sulfhydryl surface site concentration. These findings indicate that sulfhydryl binding in EPS plays a key role in tellurite adsorption on bacterial surfaces.},

  doi          = {10.1021/acs.est.1c01001},

  journal      = {Environmental Science and Technology},

  number       = 15,

  volume       = 55,

  place        = {United States},

  year         = {Mon Jul 19 00:00:00 EDT 2021},

  month        = {Mon Jul 19 00:00:00 EDT 2021}

}

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Title: Tellurite Adsorption onto Bacterial Surfaces

Abstract

Citation Formats

Estimation of Reactive Thiol Concentrations in Dissolved Organic Matter and Bacterial Cell Membranes in Aquatic Systems journal, August 2012

Crystal chemistry of the microporous tellurite minerals zemannite and kinichilite, Mg0.5[Me2+Fe3+(TeO3)3]-4.5H2O, (Me2+=Zn;Mn) [Crystal chemistry of the microporous tellurite minerals zemannite and kinichilite, Mg0.5[Me2+Fe3+(TeO3)3]-4.5H2O, (Me2+=Zn;Mn)] journal, May 1995

Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V journal, June 1998

Conformation versus Coordination: Synthesis and Structural Investigations of Tellurium(II) Dithiolates Derived from β-Donor-Substituted Thiols journal, August 2002

XANES−EXAFS Analysis of Se Solid-Phase Reaction Products Formed upon Contacting Se(IV) with FeS 2 and FeS journal, May 2008

An X-ray absorption spectroscopy study of Cd binding onto bacterial consortia journal, August 2009

Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis journal, December 2010

Sulfhydryl Binding Sites within Bacterial Extracellular Polymeric Substances journal, May 2016

Analysis of multiple-scattering XAFS data using theoretical standards journal, March 1995

Origin of the difference in the distribution behavior of tellurium and selenium in a soil–water system journal, March 2008

The crystal structure and absolute optical chirality of paratellurite, α-TeO 2 journal, September 1988

Preparation chimioue et structure cristalline des tellurites de sodium et d'argent: Na2TeO3, Ag2TeO3 journal, April 1980

Tellurium Distribution and Speciation in Contaminated Soils from Abandoned Mine Tailings: Comparison with Selenium journal, May 2017

Spore formation in B acillus subtilis: Bacillus subtilis sporulation journal, December 2013

Leaching of cadmium and tellurium from cadmium telluride (CdTe) thin-film solar panels under simulated landfill conditions journal, August 2017

Verfeinerung der Kristallstruktur von Tellurit, dem rhombischen TeO 2 journal, June 1967

Protein Measurement with the Folin Phenol Reagent journal, November 1951

Binding of tellurium to hepatocellular selenoproteins during incubation with inorganic tellurite: consequences for the activity of selenium-dependent glutathione peroxidase journal, February 1999

Characterization of sulfhydryl sites within bacterial cell envelopes using selective site-blocking and potentiometric titrations journal, May 2014

Stereochemical Aspects of Tellurium Complexes with Sulfur Ligands: Molecular Compounds and Supramolecular Associations journal, March 1994

Tellurium Compounds: Selective Inhibition of Cysteine Proteases and Model Reaction with Thiols journal, March 1998

Synthesis and Crystal Structure of Tellurium(II) bis(2-methoxycarbonylethanethiolate): A Novel Coordination Mode of Tellurium journal, October 2003

Crystal structure, Raman spectrum and lattice dynamics of a new metastable form of tellurium dioxide: γ-TeO2 journal, September 2000

High- and low-affinity binding sites for Cd on the bacterial cell walls of Bacillus subtilis and Shewanella oneidensis journal, August 2010

Functionalized Tellurium(II) Thiolates: Tellurium Bis(2-hydroxyethanethiolate) Hydrate, the First H2O–TeII Complex journal, October 2000

Ochrobactrum sp. MPV1 from a dump of roasted pyrites can be exploited as bacterial catalyst for the biogenesis of selenium and tellurium nanoparticles journal, November 2017

Near-edge x-ray-absorption fine structure of Pb: A comparison of theory and experiment journal, June 1993

Tellurite enters E scherichia coli mainly through the PitA phosphate transporter journal, June 2012

Cadmium telluride (CdTe) and cadmium selenide (CdSe) leaching behavior and surface chemistry in response to pH and O2 journal, May 2015

An EXAFS and XANES Study of V, Ni, and Fe Speciation in Cokes for Anodes Used in Aluminum Production journal, September 2019

Stoichiometry of mercury-thiol complexes on bacterial cell envelopes journal, August 2017

Export of glutathione by some widely used Salmonella typhimurium and Escherichia coli strains. journal, October 1986

Bacterial cell envelope and extracellular sulfhydryl binding sites: Their roles in metal binding and bioavailability journal, September 2019

Reinvestigation of the structure of tellurium journal, June 1989

Inhibition of human squalene monooxygenase by tellurium compounds: evidence of interaction with vicinal sulfhydryls journal, February 2001

Stabilization of cell wall proteins in Bacillus subtilis: A proteomic approach journal, May 2002

The crystal structure of sonoraite, Fe3+Te4+O3(OH)�H2O journal, January 1970

Zinc Sorption to Three Gram-Negative Bacteria: Combined Titration, Modeling, and EXAFS Study journal, March 2006

The ActP acetate transporter acts prior to the PitA phosphate carrier in tellurite uptake by Escherichia coli journal, August 2015

Biological accumulation of tellurium nanorod structures via reduction of tellurite by Shewanella oneidensis MR-1 journal, December 2012

Identification of siderophores of Pseudomonas stutzeri journal, December 2006

UniProt: a worldwide hub of protein knowledge November 2018

Extreme selenium and tellurium contamination in soils — An eighty year-old industrial legacy surrounding a Ni refinery in the Swansea Valley journal, December 2011

LocateP: Genome-scale subcellular-location predictor for bacterial proteins journal, March 2008

Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite journal, April 1997

The role of intermolecular interactions: studies on model systems for bacterial biofilms journal, October 1999

Microbial Selenate Sorption and Reduction in Nutrient Limited Systems journal, May 2006

Real-space multiple-scattering calculation and interpretation of x-ray-absorption near-edge structure journal, September 1998

A Proteomic View on Genome-Based Signal Peptide Predictions journal, September 2001

The Impact of Tellurium Supply on Cadmium Telluride Photovoltaics journal, May 2010

Adsorption of Selenite onto Bacillus subtilis : The Overlooked Role of Cell Envelope Sulfhydryl Sites in the Microbial Conversion of Se(IV) journal, August 2018

Ab initio study of linear and nonlinear optical properties of mixed tellurite–chalcogenide glasses journal, April 2010

Pyridine-2,6-Bis(Thiocarboxylic Acid) Produced by Pseudomonas stutzeri KC Reduces and Precipitates Selenium and Tellurium Oxyanions journal, May 2006

Ab initio study of the nonlinear optical susceptibility of Te O 2 -based glasses journal, April 2006

The New MRCAT (Sector 10) Bending Magnet Beamline at the Advanced Photon Source conference, January 2010

Formation of Tellurium Nanocrystals during Anaerobic Growth of Bacteria That Use Te Oxyanions as Respiratory Electron Acceptors journal, February 2007

Acetate Permease (ActP) Is Responsible for Tellurite (TeO 3 2− ) Uptake and Resistance in Cells of the Facultative Phototroph Rhodobacter capsulatus journal, February 2010

Bacterial Toxicity of Potassium Tellurite: Unveiling an Ancient Enigma journal, February 2007

Tellurite-mediated thiol oxidation in Escherichia coli journal, September 1999

Glutathione is a target in tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli journal, January 2001

Prediction of protein subcellular localization journal, June 2006

Microbial toxicity of ionic species leached from the II-VI semiconductor materials, cadmium telluride (CdTe) and cadmium selenide (CdSe) journal, November 2016

Tellurium: an element with great biological potency and potential journal, January 2010

Estimation of Reactive Thiol Concentrations in Dissolved Organic Matter and Bacterial Cell Membranes in Aquatic Systems
journal, August 2012

Crystal chemistry of the microporous tellurite minerals zemannite and kinichilite, Mg0.5[Me2+Fe3+(TeO3)3]-4.5H2O, (Me2+=Zn;Mn) [Crystal chemistry of the microporous tellurite minerals zemannite and kinichilite, Mg0.5[Me2+Fe3+(TeO3)3]-4.5H2O, (Me2+=Zn;Mn)]
journal, May 1995

Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V
journal, June 1998

Conformation versus Coordination: Synthesis and Structural Investigations of Tellurium(II) Dithiolates Derived from β-Donor-Substituted Thiols
journal, August 2002

XANES−EXAFS Analysis of Se Solid-Phase Reaction Products Formed upon Contacting Se(IV) with FeS ₂ and FeS
journal, May 2008

An X-ray absorption spectroscopy study of Cd binding onto bacterial consortia
journal, August 2009

Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis
journal, December 2010

Sulfhydryl Binding Sites within Bacterial Extracellular Polymeric Substances
journal, May 2016

Analysis of multiple-scattering XAFS data using theoretical standards
journal, March 1995

Origin of the difference in the distribution behavior of tellurium and selenium in a soil–water system
journal, March 2008

The crystal structure and absolute optical chirality of paratellurite, α-TeO ₂
journal, September 1988

Preparation chimioue et structure cristalline des tellurites de sodium et d'argent: Na2TeO3, Ag2TeO3
journal, April 1980

Tellurium Distribution and Speciation in Contaminated Soils from Abandoned Mine Tailings: Comparison with Selenium
journal, May 2017

Spore formation in B acillus subtilis: Bacillus subtilis sporulation
journal, December 2013

Leaching of cadmium and tellurium from cadmium telluride (CdTe) thin-film solar panels under simulated landfill conditions
journal, August 2017

Verfeinerung der Kristallstruktur von Tellurit, dem rhombischen TeO ₂
journal, June 1967

Protein Measurement with the Folin Phenol Reagent
journal, November 1951

Binding of tellurium to hepatocellular selenoproteins during incubation with inorganic tellurite: consequences for the activity of selenium-dependent glutathione peroxidase
journal, February 1999

Characterization of sulfhydryl sites within bacterial cell envelopes using selective site-blocking and potentiometric titrations
journal, May 2014

Stereochemical Aspects of Tellurium Complexes with Sulfur Ligands: Molecular Compounds and Supramolecular Associations
journal, March 1994

Tellurium Compounds: Selective Inhibition of Cysteine Proteases and Model Reaction with Thiols
journal, March 1998

Synthesis and Crystal Structure of Tellurium(II) bis(2-methoxycarbonylethanethiolate): A Novel Coordination Mode of Tellurium
journal, October 2003

Crystal structure, Raman spectrum and lattice dynamics of a new metastable form of tellurium dioxide: γ-TeO2
journal, September 2000

High- and low-affinity binding sites for Cd on the bacterial cell walls of Bacillus subtilis and Shewanella oneidensis
journal, August 2010

Functionalized Tellurium(II) Thiolates: Tellurium Bis(2-hydroxyethanethiolate) Hydrate, the First H2O–TeII Complex
journal, October 2000

Ochrobactrum sp. MPV1 from a dump of roasted pyrites can be exploited as bacterial catalyst for the biogenesis of selenium and tellurium nanoparticles
journal, November 2017

Near-edge x-ray-absorption fine structure of Pb: A comparison of theory and experiment
journal, June 1993

Tellurite enters E scherichia coli mainly through the PitA phosphate transporter
journal, June 2012

Cadmium telluride (CdTe) and cadmium selenide (CdSe) leaching behavior and surface chemistry in response to pH and O2
journal, May 2015

An EXAFS and XANES Study of V, Ni, and Fe Speciation in Cokes for Anodes Used in Aluminum Production
journal, September 2019

Stoichiometry of mercury-thiol complexes on bacterial cell envelopes
journal, August 2017

Export of glutathione by some widely used Salmonella typhimurium and Escherichia coli strains.
journal, October 1986

Bacterial cell envelope and extracellular sulfhydryl binding sites: Their roles in metal binding and bioavailability
journal, September 2019

Reinvestigation of the structure of tellurium
journal, June 1989

Inhibition of human squalene monooxygenase by tellurium compounds: evidence of interaction with vicinal sulfhydryls
journal, February 2001

Stabilization of cell wall proteins in Bacillus subtilis: A proteomic approach
journal, May 2002

The crystal structure of sonoraite, Fe3+Te4+O3(OH)�H2O
journal, January 1970

Zinc Sorption to Three Gram-Negative Bacteria: Combined Titration, Modeling, and EXAFS Study
journal, March 2006

The ActP acetate transporter acts prior to the PitA phosphate carrier in tellurite uptake by Escherichia coli
journal, August 2015

Biological accumulation of tellurium nanorod structures via reduction of tellurite by Shewanella oneidensis MR-1
journal, December 2012

Identification of siderophores of Pseudomonas stutzeri
journal, December 2006

UniProt: a worldwide hub of protein knowledge
November 2018

Extreme selenium and tellurium contamination in soils — An eighty year-old industrial legacy surrounding a Ni refinery in the Swansea Valley
journal, December 2011

LocateP: Genome-scale subcellular-location predictor for bacterial proteins
journal, March 2008

Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite
journal, April 1997

The role of intermolecular interactions: studies on model systems for bacterial biofilms
journal, October 1999

Microbial Selenate Sorption and Reduction in Nutrient Limited Systems
journal, May 2006

Real-space multiple-scattering calculation and interpretation of x-ray-absorption near-edge structure
journal, September 1998

A Proteomic View on Genome-Based Signal Peptide Predictions
journal, September 2001

The Impact of Tellurium Supply on Cadmium Telluride Photovoltaics
journal, May 2010

Adsorption of Selenite onto Bacillus subtilis : The Overlooked Role of Cell Envelope Sulfhydryl Sites in the Microbial Conversion of Se(IV)
journal, August 2018

Ab initio study of linear and nonlinear optical properties of mixed tellurite–chalcogenide glasses
journal, April 2010

Pyridine-2,6-Bis(Thiocarboxylic Acid) Produced by Pseudomonas stutzeri KC Reduces and Precipitates Selenium and Tellurium Oxyanions
journal, May 2006

Ab initio study of the nonlinear optical susceptibility of $Te O_{2}$ -based glasses
journal, April 2006

The New MRCAT (Sector 10) Bending Magnet Beamline at the Advanced Photon Source
conference, January 2010

Formation of Tellurium Nanocrystals during Anaerobic Growth of Bacteria That Use Te Oxyanions as Respiratory Electron Acceptors
journal, February 2007

Acetate Permease (ActP) Is Responsible for Tellurite (TeO ₃ ²⁻ ) Uptake and Resistance in Cells of the Facultative Phototroph Rhodobacter capsulatus
journal, February 2010

Bacterial Toxicity of Potassium Tellurite: Unveiling an Ancient Enigma
journal, February 2007

Tellurite-mediated thiol oxidation in Escherichia coli
journal, September 1999

Glutathione is a target in tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli
journal, January 2001

Prediction of protein subcellular localization
journal, June 2006

Microbial toxicity of ionic species leached from the II-VI semiconductor materials, cadmium telluride (CdTe) and cadmium selenide (CdSe)
journal, November 2016

Tellurium: an element with great biological potency and potential
journal, January 2010