skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metabolism, survival, and gene expression of Pseudomonas putida to hematite nanoparticles mediated by surface-bound humic acid

Abstract

Natural organic matter (NOM) is likely to coat naturally occurring nanoparticles (NNPs) in the soil environment and poses distinct effects on the interaction between NPs and soil microorganisms, however such topic has not been well investigated. This study explored the influence of nanoparticle surface-bound humic acid (HA, as a model NOM) on the toxicity of hematite NPs (i.e., nano-Fe2O3) to Pseudomonas putida (P. putida). Results showed that nano-Fe2O3 could inhibit the bacterial growth with an IC50 of 23.58 mg L-1, while nanoparticle surface-bound HA could significantly alleviate the P. putida toxicity of nano-Fe2O3. IC50 of nano-Fe2O3 increased to 4774.23 mg L-1 as a result of surface-saturation by HA. Co-precipitation experiment and transmission electron microscopy observation revealed that nanoparticle surface-bound HA prevented the adhesion of nano-Fe2O3 to the cells as well as limited cell internalization of nanoparticles due to the increased electrostatic repulsion. The generation of intracellular reactive oxygen species (ROS) was significantly limited by the nanoparticle surface-bound HA. The prevention of adhesion and inhibition of ROS generation could account for the HA-mitigated nanotoxicity. Interfacial interactions between hematite NPs and cell membrane were also evaluated on the basis of the Derjaguin–Landau–Verwey–Overbeek (DLVO) theory, and the magnitude of interaction energy barrier correlatedmore » well with the 48 h LC50 data of hematite NPs to P. putida. This result implies that metal oxide NPs with strong association with the cell surface might induce more severe cytotoxicity in microorganisms.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1];  [1]; ORCiD logo [1]
  1. State Key Laboratory of Agricultural Microbiology; College of Resources and Environment; Huazhong Agricultural University; Wuhan 430070; China
  2. Department of Chemical and Environmental Engineering; University of California; California 92521; USA
  3. Earth & Biological Sciences Directorate; Pacific Northwest National Laboratory; Richland; USA
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1439676
Report Number(s):
PNNL-SA-121317
Journal ID: ISSN 2051-8153; ESNNA4
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Environmental Science: Nano
Additional Journal Information:
Journal Volume: 5; Journal Issue: 3; Journal ID: ISSN 2051-8153
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
natural occurring nanoparticles; na; hematite; su; Pseudomonas putida; nanotoxicity

Citation Formats

Ouyang, Kai, Walker, Sharon L., Yu, Xiao-Ying, Gao, Chun-Hui, Huang, Qiaoyun, and Cai, Peng. Metabolism, survival, and gene expression of Pseudomonas putida to hematite nanoparticles mediated by surface-bound humic acid. United States: N. p., 2018. Web. doi:10.1039/C7EN01039G.
Ouyang, Kai, Walker, Sharon L., Yu, Xiao-Ying, Gao, Chun-Hui, Huang, Qiaoyun, & Cai, Peng. Metabolism, survival, and gene expression of Pseudomonas putida to hematite nanoparticles mediated by surface-bound humic acid. United States. doi:10.1039/C7EN01039G.
Ouyang, Kai, Walker, Sharon L., Yu, Xiao-Ying, Gao, Chun-Hui, Huang, Qiaoyun, and Cai, Peng. Mon . "Metabolism, survival, and gene expression of Pseudomonas putida to hematite nanoparticles mediated by surface-bound humic acid". United States. doi:10.1039/C7EN01039G.
@article{osti_1439676,
title = {Metabolism, survival, and gene expression of Pseudomonas putida to hematite nanoparticles mediated by surface-bound humic acid},
author = {Ouyang, Kai and Walker, Sharon L. and Yu, Xiao-Ying and Gao, Chun-Hui and Huang, Qiaoyun and Cai, Peng},
abstractNote = {Natural organic matter (NOM) is likely to coat naturally occurring nanoparticles (NNPs) in the soil environment and poses distinct effects on the interaction between NPs and soil microorganisms, however such topic has not been well investigated. This study explored the influence of nanoparticle surface-bound humic acid (HA, as a model NOM) on the toxicity of hematite NPs (i.e., nano-Fe2O3) to Pseudomonas putida (P. putida). Results showed that nano-Fe2O3 could inhibit the bacterial growth with an IC50 of 23.58 mg L-1, while nanoparticle surface-bound HA could significantly alleviate the P. putida toxicity of nano-Fe2O3. IC50 of nano-Fe2O3 increased to 4774.23 mg L-1 as a result of surface-saturation by HA. Co-precipitation experiment and transmission electron microscopy observation revealed that nanoparticle surface-bound HA prevented the adhesion of nano-Fe2O3 to the cells as well as limited cell internalization of nanoparticles due to the increased electrostatic repulsion. The generation of intracellular reactive oxygen species (ROS) was significantly limited by the nanoparticle surface-bound HA. The prevention of adhesion and inhibition of ROS generation could account for the HA-mitigated nanotoxicity. Interfacial interactions between hematite NPs and cell membrane were also evaluated on the basis of the Derjaguin–Landau–Verwey–Overbeek (DLVO) theory, and the magnitude of interaction energy barrier correlated well with the 48 h LC50 data of hematite NPs to P. putida. This result implies that metal oxide NPs with strong association with the cell surface might induce more severe cytotoxicity in microorganisms.},
doi = {10.1039/C7EN01039G},
journal = {Environmental Science: Nano},
issn = {2051-8153},
number = 3,
volume = 5,
place = {United States},
year = {2018},
month = {1}
}

Works referenced in this record:

The effect of humic acids on the cytotoxicity of silver nanoparticles to a natural aquatic bacterial assemblage
journal, November 2010


Electrostatic Interactions Affect Nanoparticle-Mediated Toxicity to Gram-Negative Bacterium Pseudomonas aeruginosa PAO1
journal, March 2010

  • Feris, Kevin; Otto, Caitlin; Tinker, Juliette
  • Langmuir, Vol. 26, Issue 6
  • DOI: 10.1021/la903491z

Quantification of c60 Fullerene Concentrations in Water
journal, January 2008

  • Chen, Zhuo; Westerhoff, Paul; Herckes, Pierre
  • Environmental Toxicology and Chemistry, Vol. 27, Issue 9
  • DOI: 10.1897/07-560.1

Deposition and Survival of Escherichia coli O157:H7 on Clay Minerals in a Parallel Plate Flow System
journal, February 2013

  • Cai, Peng; Huang, Qiaoyun; Walker, Sharon L.
  • Environmental Science & Technology, Vol. 47, Issue 4
  • DOI: 10.1021/es304686a

Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi
journal, May 2008


Fate and Transport of Engineered Nanomaterials in the Environment
journal, January 2010

  • Lin, Daohui; Tian, Xiaoli; Wu, Fengchang
  • Journal of Environment Quality, Vol. 39, Issue 6
  • DOI: 10.2134/jeq2009.0423

Aggregation and Deposition Kinetics of Fullerene (C 60 ) Nanoparticles
journal, December 2006

  • Chen, Kai Loon; Elimelech, Menachem
  • Langmuir, Vol. 22, Issue 26
  • DOI: 10.1021/la062072v

Different, overlapping mechanisms for colonization of abiotic and plant surfaces by Pseudomonas putida
journal, November 2008


Toxic Effects of Single-Walled Carbon Nanotubes in the Development of E. coli Biofilm
journal, June 2010

  • Rodrigues, Debora F.; Elimelech, Menachem
  • Environmental Science & Technology, Vol. 44, Issue 12
  • DOI: 10.1021/es1005785

Influence of Humic Acid on Titanium Dioxide Nanoparticle Toxicity to Developing Zebrafish
journal, March 2013

  • Yang, Sarah P.; Bar-Ilan, Ofek; Peterson, Richard E.
  • Environmental Science & Technology, Vol. 47, Issue 9
  • DOI: 10.1021/es3047334

Toxicity of Gold Nanoparticles Functionalized with Cationic and Anionic Side Chains
journal, July 2004

  • Goodman, Catherine M.; McCusker, Catherine D.; Yilmaz, Tuna
  • Bioconjugate Chemistry, Vol. 15, Issue 4
  • DOI: 10.1021/bc049951i

Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells
journal, September 2005


Toxic Potential of Materials at the Nanolevel
journal, February 2006


Nanopesticides: State of Knowledge, Environmental Fate, and Exposure Modeling
journal, January 2013

  • Kah, M.; Beulke, S.; Tiede, K.
  • Critical Reviews in Environmental Science and Technology, Vol. 43, Issue 16
  • DOI: 10.1080/10643389.2012.671750

Silver Nanoparticle Impact on Bacterial Growth: Effect of pH, Concentration, and Organic Matter
journal, October 2009

  • Fabrega, Julia; Fawcett, Shona R.; Renshaw, Joanna C.
  • Environmental Science & Technology, Vol. 43, Issue 19
  • DOI: 10.1021/es803259g

Bacterial toxicity comparison between nano- and micro-scaled oxide particles
journal, May 2009


Quantum Dot Weathering Results in Microbial Toxicity
journal, December 2008

  • Mahendra, Shaily; Zhu, Huiguang; Colvin, Vicki L.
  • Environmental Science & Technology, Vol. 42, Issue 24
  • DOI: 10.1021/es8023385

Visible spectroscopy of aerosol particles collected on filters: iron-oxide minerals
journal, January 2002


Nanocrystals as Stoichiometric Reagents with Unique Surface Chemistry
journal, January 1996

  • Klabunde, Kenneth J.; Stark, Jane; Koper, Olga
  • The Journal of Physical Chemistry, Vol. 100, Issue 30
  • DOI: 10.1021/jp960224x

Approximate expressions for retarded van der waals interaction
journal, September 1981


Functional Genomics of Stress Response in Pseudomonas putida KT2440
journal, May 2006

  • Reva, O. N.; Weinel, C.; Weinel, M.
  • Journal of Bacteriology, Vol. 188, Issue 11
  • DOI: 10.1128/JB.00101-06

Surfactive stabilization of multi-walled carbon nanotube dispersions with dissolved humic substances
journal, April 2009


Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria
journal, July 2004


Effect of Nanoparticle Surface Charge at the Plasma Membrane and Beyond
journal, July 2010

  • Arvizo, Rochelle R.; Miranda, Oscar R.; Thompson, Michael A.
  • Nano Letters, Vol. 10, Issue 7
  • DOI: 10.1021/nl101140t

Nanominerals, Mineral Nanoparticles, and Earth Systems
journal, March 2008


Dispersion and Toxicity of Selected Manufactured Nanomaterials in Natural River Water Samples: Effects of Water Chemical Composition
journal, May 2009

  • Gao, Jie; Youn, Sejin; Hovsepyan, Anna
  • Environmental Science & Technology, Vol. 43, Issue 9
  • DOI: 10.1021/es803315v

Soil Colloids and Minerals Modulate Metabolic Activity of Pseudomonas putida Measured Using Microcalorimetry
journal, July 2014


Titanium dioxide nanoparticles induce oxidative stress and DNA-adduct formation but not DNA-breakage in human lung cells
journal, January 2009

  • Bhattacharya, Kunal; Davoren, Maria; Boertz, Jens
  • Particle and Fibre Toxicology, Vol. 6, Issue 1
  • DOI: 10.1186/1743-8977-6-17

Insights into the genomic basis of niche specificity of Pseudomonas putida KT2440
journal, December 2004


Natural Genetic Transformation of Streptococcus mutans Growing in Biofilms
journal, February 2001


Mutual coagulation of colloidal dispersions
journal, January 1966

  • Hogg, R.; Healy, T. W.; Fuerstenau, D. W.
  • Transactions of the Faraday Society, Vol. 62
  • DOI: 10.1039/tf9666201638

Effect of natural organic matter on toxicity and reactivity of nano-scale zero-valent iron
journal, February 2011


Impacts of Hematite Nanoparticle Exposure on Biomechanical, Adhesive, and Surface Electrical Properties of Escherichia coli Cells
journal, March 2012

  • Zhang, Wen; Hughes, Joseph; Chen, Yongsheng
  • Applied and Environmental Microbiology, Vol. 78, Issue 11
  • DOI: 10.1128/AEM.00193-12

Bacterial Identification by Microcalorimetry
journal, February 1973

  • Boling, E. A.; Blanchard, G. C.; Russell, W. J.
  • Nature, Vol. 241, Issue 5390
  • DOI: 10.1038/241472a0

Relating Colloidal Stability of Fullerene (C 60 ) Nanoparticles to Nanoparticle Charge and Electrokinetic Properties
journal, October 2009

  • Chen, Kai Loon; Elimelech, Menachem
  • Environmental Science & Technology, Vol. 43, Issue 19
  • DOI: 10.1021/es900185p

Aggregation and ecotoxicity of CeO2 nanoparticles in synthetic and natural waters with variable pH, organic matter concentration and ionic strength
journal, April 2011

  • Van Hoecke, Karen; De Schamphelaere, Karel A. C.; Van der Meeren, Paul
  • Environmental Pollution, Vol. 159, Issue 4
  • DOI: 10.1016/j.envpol.2010.12.010

The influence of dissolved and surface-bound humic acid on the toxicity of TiO2 nanoparticles to Chlorella sp.
journal, September 2012


Effect of soil Sorption and Aquatic Natural Organic Matter on the Antibacterial Activity of a Fullerene Water Suspension
journal, January 2008

  • Li, Dong; Lyon, Delina Y.; Li, Qilin
  • Environmental Toxicology and Chemistry, Vol. 27, Issue 9
  • DOI: 10.1897/07-548.1

Do nanoparticles present ecotoxicological risks for the health of the aquatic environment?
journal, December 2006


Interaction force measurement between E. coli cells and nanoparticles immobilized surfaces by using AFM
journal, February 2011


Antimicrobial Activity of Single-Walled Carbon Nanotubes: Length Effect
journal, October 2010

  • Yang, Cheenou; Mamouni, Jaouad; Tang, Yongan
  • Langmuir, Vol. 26, Issue 20
  • DOI: 10.1021/la103110g

Biotoxicity of nanoparticles: effect of natural organic matter
journal, January 2011


Safe handling of nanotechnology
journal, November 2006

  • Maynard, Andrew D.; Aitken, Robert J.; Butz, Tilman
  • Nature, Vol. 444, Issue 7117
  • DOI: 10.1038/444267a

Surface Charge-Dependent Toxicity of Silver Nanoparticles
journal, January 2011

  • El Badawy, Amro M.; Silva, Rendahandi G.; Morris, Brian
  • Environmental Science & Technology, Vol. 45, Issue 1
  • DOI: 10.1021/es1034188

Cell Density-Dependent Gene Contributes to Efficient Seed Colonization by Pseudomonas putida KT2440
journal, September 2004


A little knowledge...
journal, July 2003


Interaction of Fullerene (C 60 ) Nanoparticles with Humic Acid and Alginate Coated Silica Surfaces: Measurements, Mechanisms, and Environmental Implications
journal, October 2008

  • Chen, Kai Loon; Elimelech, Menachem
  • Environmental Science & Technology, Vol. 42, Issue 20
  • DOI: 10.1021/es8012062

Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili
journal, October 1998


Toxicity and Internalization of CuO Nanoparticles to Prokaryotic Alga Microcystis aeruginosa as Affected by Dissolved Organic Matter
journal, July 2011

  • Wang, Zhenyu; Li, Jing; Zhao, Jian
  • Environmental Science & Technology, Vol. 45, Issue 14
  • DOI: 10.1021/es2010573

Adsorbed Polymer and NOM Limits Adhesion and Toxicity of Nano Scale Zerovalent Iron to E. coli
journal, May 2010

  • Li, Zhiqiang; Greden, Karl; Alvarez, Pedro J. J.
  • Environmental Science & Technology, Vol. 44, Issue 9
  • DOI: 10.1021/es9031198

Toxicity of ZnO Nanoparticles to Escherichia coli : Mechanism and the Influence of Medium Components
journal, March 2011

  • Li, Mei; Zhu, Lizhong; Lin, Daohui
  • Environmental Science & Technology, Vol. 45, Issue 5
  • DOI: 10.1021/es102624t

Combined Factors Influencing the Aggregation and Deposition of nano-TiO 2 in the Presence of Humic Acid and Bacteria
journal, April 2012

  • Chowdhury, Indranil; Cwiertny, David M.; Walker, Sharon L.
  • Environmental Science & Technology, Vol. 46, Issue 13
  • DOI: 10.1021/es2034747

Sorption of Organic Contaminants by Carbon Nanotubes: Influence of Adsorbed Organic Matter
journal, May 2008

  • Wang, Xilong; Lu, Jialong; Xing, Baoshan
  • Environmental Science & Technology, Vol. 42, Issue 9
  • DOI: 10.1021/es702971g

Comparative Toxicity of Nanoparticulate ZnO, Bulk ZnO, and ZnCl 2 to a Freshwater Microalga (Pseudokirchneriella subcapitata): The Importance of Particle Solubility
journal, December 2007

  • Franklin, Natasha M.; Rogers, Nicola J.; Apte, Simon C.
  • Environmental Science & Technology, Vol. 41, Issue 24
  • DOI: 10.1021/es071445r

Influence of Dissolved Organic Matter on the Environmental Fate of Metals, Nanoparticles, and Colloids
journal, April 2011

  • Aiken, George R.; Hsu-Kim, Heileen; Ryan, Joseph N.
  • Environmental Science & Technology, Vol. 45, Issue 8
  • DOI: 10.1021/es103992s

Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective
journal, September 2009

  • Auffan, Mélanie; Rose, Jérôme; Bottero, Jean-Yves
  • Nature Nanotechnology, Vol. 4, Issue 10
  • DOI: 10.1038/nnano.2009.242

Aggregation Kinetics of Alginate-Coated Hematite Nanoparticles in Monovalent and Divalent Electrolytes
journal, March 2006

  • Chen, Kai Loon; Mylon, Steven E.; Elimelech, Menachem
  • Environmental Science & Technology, Vol. 40, Issue 5
  • DOI: 10.1021/es0518068

Impact of Silica Nanoparticle Design on Cellular Toxicity and Hemolytic Activity
journal, June 2011

  • Yu, Tian; Malugin, Alexander; Ghandehari, Hamidreza
  • ACS Nano, Vol. 5, Issue 7
  • DOI: 10.1021/nn2013904

Adsorption of hematite nanoparticles onto Caco-2 cells and the cellular impairments: effect of particle size
journal, August 2010


A Comparative Study of Fe(II) and Fe(III) Interactions with DNA Duplex: Major and Minor Grooves Bindings
journal, June 2005


Effects of humic acid on the interactions between zinc oxide nanoparticles and bacterial biofilms
journal, December 2017


Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability: Exopolysaccharide genes and P. putida biofilm formation
journal, March 2011


Cytotoxicity of CeO 2 Nanoparticles for Escherichia coli. Physico-Chemical Insight of the Cytotoxicity Mechanism
journal, October 2006

  • Thill, Antoine; Zeyons, Ophélie; Spalla, Olivier
  • Environmental Science & Technology, Vol. 40, Issue 19
  • DOI: 10.1021/es060999b

A study of the mechanism of in vitro cytotoxicity of metal oxide nanoparticles using catfish primary hepatocytes and human HepG2 cells
journal, October 2011


Coating Fe 3 O 4 Magnetic Nanoparticles with Humic Acid for High Efficient Removal of Heavy Metals in Water
journal, September 2008

  • Liu, Jing-fu; Zhao, Zong-shan; Jiang, Gui-bin
  • Environmental Science & Technology, Vol. 42, Issue 18
  • DOI: 10.1021/es800924c

Physicochemical Determinants of Multiwalled Carbon Nanotube Bacterial Cytotoxicity
journal, October 2008

  • Kang, Seoktae; Mauter, Meagan S.; Elimelech, Menachem
  • Environmental Science & Technology, Vol. 42, Issue 19
  • DOI: 10.1021/es8010173

Enhanced Aggregation of Alginate-Coated Iron Oxide (Hematite) Nanoparticles in the Presence of Calcium, Strontium, and Barium Cations
journal, May 2007

  • Chen, Kai Loon; Mylon, Steven E.; Elimelech, Menachem
  • Langmuir, Vol. 23, Issue 11
  • DOI: 10.1021/la063744k

Comparison of Micro- and Nanoscale Fe+3–Containing (Hematite) Particles for Their Toxicological Properties in Human Lung Cells In Vitro
journal, January 2012

  • Bhattacharya, Kunal; Hoffmann, Eik; Schins, Roel F. P.
  • Toxicological Sciences, Vol. 126, Issue 1
  • DOI: 10.1093/toxsci/kfs014

AMERICAN CHEMICAL SOCIETY MEETING: Nanomaterials Show Signs of Toxicity
journal, April 2003


Aggregation of Titanium Dioxide Nanoparticles: Role of a Fulvic Acid
journal, March 2009

  • Domingos, Rute F.; Tufenkji, Nathalie; Wilkinson, Kevin J.
  • Environmental Science & Technology, Vol. 43, Issue 5
  • DOI: 10.1021/es8023594

Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward Escherichia coli
journal, April 2012


Engineered nanomaterials in soils and water: how do they behave and could they pose a risk to human health?
journal, December 2007


Surface Interactions Affect the Toxicity of Engineered Metal Oxide Nanoparticles toward Paramecium
journal, July 2012

  • Li, Kungang; Chen, Ying; Zhang, Wen
  • Chemical Research in Toxicology, Vol. 25, Issue 8
  • DOI: 10.1021/tx300151y