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Title: Adsorption of selenite onto Bacillus subtilis: the overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se(IV)

Abstract

Microbial activities play a central role in the global cycling of selenium. Microorganisms can reduce, methylate and assimilate Se, controlling the transport and fate of Se in the environment. However, the mechanisms controlling these microbial activities are still poorly understood. In particular, it is unknown how the negatively-charged Se(IV) and Se(VI) oxyanions that dominate the aqueous Se speciation in oxidizing environments bind to negatively-charged microbial cell surfaces in order to become bioavailable. Here, we show that the adsorption of selenite onto Bacillus subtilis bacterial cells is controlled by cell envelope sulfhydryl sites. Once adsorbed onto the bacteria, selenite is reduced, and forms reduced organo-Se compounds (e.g., R1S-Se-SR2). Because sulfhydryl sites are present within cell envelopes of a wide range of bacterial species, sulfhydryl-controlled adsorption of selenite likely represents a general mechanism adopted by bacteria to make selenite bioavailable. Therefore, sulfhydryl binding of selenite likely occurs in a wide range of oxidized Se-bearing environments, and because it is followed by microbial conversion of selenite to other Se species, the process represents a crucial step in the global cycling of Se.

Authors:
 [1];  [2];  [1];  [3];  [1]
+ Show Author Affiliations
  1. Univ. of Notre Dame, IN (United States). Dept. of Civil and Environmental Engineering and Earth Sciences
  2. Bulgarian Academy of Sciences, Sofia (Bulgaria). Inst. of Chemical Engineering; Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1493698
Grant/Contract Number:  
AC02-06CH11357; EAR-1424950
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Volume: 52; Journal Issue: 18; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Yu, Qiang, Boyanov, Maxim I., Liu, Jinling, Kemner, Kenneth M., and Fein, Jeremy B. Adsorption of selenite onto Bacillus subtilis: the overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se(IV). United States: N. p., 2018. Web. doi:10.1021/acs.est.8b02280.
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Yu, Qiang, Boyanov, Maxim I., Liu, Jinling, Kemner, Kenneth M., & Fein, Jeremy B. Adsorption of selenite onto Bacillus subtilis: the overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se(IV). United States. https://doi.org/10.1021/acs.est.8b02280
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Yu, Qiang, Boyanov, Maxim I., Liu, Jinling, Kemner, Kenneth M., and Fein, Jeremy B. Tue . "Adsorption of selenite onto Bacillus subtilis: the overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se(IV)". United States. https://doi.org/10.1021/acs.est.8b02280. https://www.osti.gov/servlets/purl/1493698.
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@article{osti_1493698,
title = {Adsorption of selenite onto Bacillus subtilis: the overlooked role of cell envelope sulfhydryl sites in the microbial conversion of Se(IV)},
author = {Yu, Qiang and Boyanov, Maxim I. and Liu, Jinling and Kemner, Kenneth M. and Fein, Jeremy B.},
abstractNote = {Microbial activities play a central role in the global cycling of selenium. Microorganisms can reduce, methylate and assimilate Se, controlling the transport and fate of Se in the environment. However, the mechanisms controlling these microbial activities are still poorly understood. In particular, it is unknown how the negatively-charged Se(IV) and Se(VI) oxyanions that dominate the aqueous Se speciation in oxidizing environments bind to negatively-charged microbial cell surfaces in order to become bioavailable. Here, we show that the adsorption of selenite onto Bacillus subtilis bacterial cells is controlled by cell envelope sulfhydryl sites. Once adsorbed onto the bacteria, selenite is reduced, and forms reduced organo-Se compounds (e.g., R1S-Se-SR2). Because sulfhydryl sites are present within cell envelopes of a wide range of bacterial species, sulfhydryl-controlled adsorption of selenite likely represents a general mechanism adopted by bacteria to make selenite bioavailable. Therefore, sulfhydryl binding of selenite likely occurs in a wide range of oxidized Se-bearing environments, and because it is followed by microbial conversion of selenite to other Se species, the process represents a crucial step in the global cycling of Se.},
doi = {10.1021/acs.est.8b02280},
journal = {Environmental Science and Technology},
number = 18,
volume = 52,
place = {United States},
year = {2018},
month = {9}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1021/acs.est.8b02280
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Cited by: 4 works
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Figures / Tables:

Figure 1 Figure 1: Removal of aqueous Se(IV) by untreated and qBBr-treated B. subtilis biomass as a function of pH (Biomass: 20 g/L; initial Se(IV): 1 ppm; 0.1 M NaCl background electrolyte). Two replicates of the adsorption experiments were conducted using identical conditions but at different times, as denoted by #1 andmore » #2.« less
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Works referenced in this record:

Selenate Reduction to Elemental Selenium by Anaerobic Bacteria in Sediments and Culture: Biogeochemical Significance of a Novel, Sulfate-Independent Respiration
journal, September 1989

Bacterial reduction of selenite to elemental selenium
journal, October 1996

Microbial Oxidation of Elemental Selenium in Soil Slurries and Bacterial Cultures
journal, December 1998

  • Dowdle, Philip R.; Oremland, Ronald S.
  • Environmental Science & Technology, Vol. 32, Issue 23
  • DOI: 10.1021/es970940s

Environmental Selenium Research: From Microscopic Processes to Global Understanding
journal, December 2011

  • Winkel, Lenny H. E.; Johnson, C. Annette; Lenz, Markus
  • Environmental Science & Technology, Vol. 46, Issue 2
  • DOI: 10.1021/es203434d

Microbial Transformations of Selenium and the Bioremediation of Seleniferous Environments
journal, July 1999

Biogenic selenium nanoparticles: current status and future prospects
journal, January 2016

  • Wadhwani, Sweety A.; Shedbalkar, Utkarsha U.; Singh, Richa
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 6
  • DOI: 10.1007/s00253-016-7300-7

Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1
journal, January 1997

  • Fujita, Masanori; Ike, Michihiko; Nishimoto, Shintaro
  • Journal of Fermentation and Bioengineering, Vol. 83, Issue 6
  • DOI: 10.1016/S0922-338X(97)81130-0

Biomineralization of selenium by the selenate-respiring bacterium Thauera selenatis
journal, November 2012

  • Butler, Clive S.; Debieux, Charles M.; Dridge, Elizabeth J.
  • Biochemical Society Transactions, Vol. 40, Issue 6
  • DOI: 10.1042/BST20120087

Transformations of selenate and selenite by Stenotrophomonas maltophilia isolated from a seleniferous agricultural drainage pond sediment
journal, April 2003

Production of selenium nanoparticles in Pseudomonas putida KT2440
journal, November 2016

  • Avendaño, Roberto; Chaves, Nefertiti; Fuentes, Paola
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep37155

Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm
journal, January 2014

  • Li, Dao-Bo; Cheng, Yuan-Yuan; Wu, Chao
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep03735

Selenite-reducing capacity of the copper-containing nitrite reductase of Rhizobium sullae
journal, April 2007

Biotransformation and detoxification of selenite by microbial biogenesis of selenium-sulfur nanoparticles
journal, February 2018

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

  • Zawadzka, Anna M.; Crawford, Ronald L.; Paszczynski, Andrzej J.
  • Applied and Environmental Microbiology, Vol. 72, Issue 5
  • DOI: 10.1128/AEM.72.5.3119-3129.2006

A critical review of thermodynamic data for selenium species at 25°C
journal, January 2001

The binding of heavy metals to algal surfaces
journal, July 1988

A chemical equilibrium model for metal adsorption onto bacterial surfaces
journal, August 1997

Sites of metal deposition in the cell wall of Bacillus subtilis.
journal, January 1980

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

  • Guiné, V.; Spadini, L.; Sarret, G.
  • Environmental Science & Technology, Vol. 40, Issue 6
  • DOI: 10.1021/es050981l

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

  • Mishra, Bhoopesh; Boyanov, Maxim; Bunker, Bruce A.
  • Geochimica et Cosmochimica Acta, Vol. 74, Issue 15
  • DOI: 10.1016/j.gca.2010.02.019

An experimental study of Au removal from solution by non-metabolizing bacterial cells and their exudates
journal, June 2012

Experimental study of humic acid adsorption onto bacteria and Al-oxide mineral surfaces
journal, November 1999

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

  • Kenward, Paul A.; Fowle, David A.; Yee, Nathan
  • Environmental Science & Technology, Vol. 40, Issue 12
  • DOI: 10.1021/es052210n

The Chemistry and Toxicity of Selenium Compounds, with Special Reference to the Selenium Problem.
journal, April 1941

Mechanism of the reaction of thiols with selenite
journal, June 1980

  • Kice, John L.; Lee, Thomas W. S.; Pan, Shu-Teh
  • Journal of the American Chemical Society, Vol. 102, Issue 13
  • DOI: 10.1021/ja00533a025

Bacillithiol, a New Player in Bacterial Redox Homeostasis
journal, July 2011

Controls on Bacterial Cell Envelope Sulfhydryl Site Concentrations: The Effect of Glucose Concentration During Growth
journal, June 2017

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

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

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

  • Joe-Wong, Claresta; Shoenfelt, Elizabeth; Hauser, Emily J.
  • Environmental Science & Technology
  • DOI: 10.1021/es301381n

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

  • Kropf, A. J.; Katsoudas, J.; Chattopadhyay, S.
  • SRI 2009, 10TH INTERNATIONAL CONFERENCE ON RADIATION INSTRUMENTATION, AIP Conference Proceedings
  • DOI: 10.1063/1.3463194

The elimination of selenium(IV) from aqueous solution by precipitation with sodium sulfide
journal, January 2011

Uptake, Distribution, and Speciation of Selenoamino Acids by Human Cancer Cells: X-ray Absorption and Fluorescence Methods
journal, March 2011

  • Weekley, Claire M.; Aitken, Jade B.; Vogt, Stefan
  • Biochemistry, Vol. 50, Issue 10
  • DOI: 10.1021/bi101678a

Chemical Forms of Selenium in the Metal-Resistant Bacterium Ralstonia metallidurans CH34 Exposed to Selenite and Selenate
journal, May 2005

Quantitative Speciation of Selenium in Soils Using X-ray Absorption Spectroscopy
journal, September 1995

  • Pickering, Ingrid J.; Brown, Gordon E.; Tokunaga, Tetsu K.
  • Environmental Science & Technology, Vol. 29, Issue 9
  • DOI: 10.1021/es00009a043

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

Selenite removal and reduction by growing Aspergillus sp. J2
journal, November 2017

Characterizing Heterogeneous Bacterial Surface Functional Groups Using Discrete Affinity Spectra for Proton Binding
journal, December 1999

  • Cox, Jenny S.; Smith, D. Scott; Warren, Lesley A.
  • Environmental Science & Technology, Vol. 33, Issue 24
  • DOI: 10.1021/es990627l

Delayed formation of zero-valent selenium nanoparticles by Bacillus mycoides SeITE01 as a consequence of selenite reduction under aerobic conditions
journal, January 2014

  • Lampis, Silvia; Zonaro, Emanuele; Bertolini, Cristina
  • Microbial Cell Factories, Vol. 13, Issue 1
  • DOI: 10.1186/1475-2859-13-35

Microbial transformations of selenite by methane-oxidizing bacteria
journal, June 2017

  • Eswayah, Abdurrahman S.; Smith, Thomas J.; Scheinost, Andreas C.
  • Applied Microbiology and Biotechnology, Vol. 101, Issue 17
  • DOI: 10.1007/s00253-017-8380-8

Selenium (IV,VI) reduction and tolerance by fungi in an oxic environment
journal, January 2017

  • Rosenfeld, C. E.; Kenyon, J. A.; James, B. R.
  • Geobiology, Vol. 15, Issue 3
  • DOI: 10.1111/gbi.12224

Experimental measurements of the reversibility of metal–bacteria adsorption reactions
journal, July 2000

Micro-spectroscopic investigation of selenium-bearing minerals from the Western US Phosphate Resource Area
journal, January 2005

  • Ryser, Amy L.; Strawn, Daniel G.; Marcus, Matthew A.
  • Geochemical Transactions, Vol. 6, Issue 1
  • DOI: 10.1186/1467-4866-6-1

Fate of Selenate and Selenite Metabolized by Rhodobacter sphaeroides
journal, November 2000

  • Van Fleet-Stalder, Verena; Chasteen, Thomas G.; Pickering, Ingrid J.
  • Applied and Environmental Microbiology, Vol. 66, Issue 11
  • DOI: 10.1128/AEM.66.11.4849-4853.2000

Correlative Cryogenic Spectromicroscopy to Investigate Selenium Bioreduction Products
journal, December 2017

  • Fakra, Sirine C.; Luef, Birgit; Castelle, Cindy J.
  • Environmental Science & Technology, Vol. 52, Issue 2
  • DOI: 10.1021/acs.est.5b01409

Zum redoxsensitiven Verhalten von Selenit in Gegenwart reaktiver Sauerstoffspezies
journal, October 1999

  • Albrecht, Steffen; Zimmermann, Thomas; Grützmann, Robert
  • Medizinische Klinik, Vol. 94, Issue S3
  • DOI: 10.1007/BF03042197

NO-mediated cytoprotection: Instant adaptation to oxidative stress in bacteria
journal, September 2005

  • Gusarov, I.; Nudler, E.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 39
  • DOI: 10.1073/pnas.0504307102

Kinetics of Oxidation of Selenite to Selenate in the Presence of Oxygen, Titania, and Light
journal, March 1995

  • Gruebel, Karen A.; Davis, James A.; Leckie, James O.
  • Environmental Science & Technology, Vol. 29, Issue 3
  • DOI: 10.1021/es00003a005

Elucidation of the Mechanism of Reaction between S 2 O 8 2– , Selenite and Mn 2+ in Aqueous Solution and Limestone-Gypsum FGD Liquor
journal, September 2013

  • Akiho, Hiroyuki; Ito, Shigeo; Matsuda, Hiromitsu
  • Environmental Science & Technology, Vol. 47, Issue 19
  • DOI: 10.1021/es3042302

Biomimetic Synthesis of Selenium Nanospheres by Bacterial Strain JS-11 and Its Role as a Biosensor for Nanotoxicity Assessment: A Novel Se-Bioassay
journal, March 2013

Influence of pH, salinity, and selenium on the growth of Aeromonas veronii in evaporation agricultural drainage water
journal, February 1996

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    • Critical Reviews in Environmental Science and Technology, Vol. 49, Issue 19
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    • Regulatory Mechanisms in Biosystems, Vol. 10, Issue 4
    • DOI: 10.15421/021980
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