Membrane Alterations in Pseudomonas putida F1 Exposed to Nanoscale Zerovalent Iron: Effects of Short-Term and Repetitive nZVI Exposure.

In this study, we report the effect of the commercial nanoscale zerovalent iron (nZVI) on environmental bacteria, emphasizing the importance of nZVI-bacterial membrane interaction on nZVI toxicity as well as the adaptability of bacteria to nZVI. Exposure of Pseudomonas putida F1 to 0.1, 1.0, and 5.0 g/L of nZVI caused the reduction in colony forming units (CFUs) substantially for almost 3 orders of magnitude. However, a rebound in the cell number was observed after the prolonged exposure except for 5.0 g/L nZVI at which bacterial viability was completely inhibited. Upon exposure, nZVI accumulated on and penetrated into the bacterial cell membrane. Cell membrane composition analysis revealed the conversion of the cis to trans isomer of unsaturated fatty acid upon short-term nZVI exposure, resulting in a more rigid membrane counteracting the membrane-fluidizing effect of nZVI. Several cycles of repetitive exposure of cells to 0.1 g/L nZVI induced a persistent phenotype of P. putida F1 as indicated by smaller colony morphology, a more rigid membrane, and higher tolerance to nZVI. A low interaction between nZVI particles and the surface of the nZVI-persistent phenotypic cells reduced the nZVI-induced membrane damage. This study unveils the significance of nZVI-membrane interaction on toxicity of nZVI toward bacteria.

[1]  S. French,et al.  The dynamic nature of bacterial surfaces: Implications for metal–membrane interaction , 2013, Critical reviews in microbiology.

[2]  J. Gottfries,et al.  Effect of Low Temperature on Growth and UltraStructure of Staphylococcus spp , 2012 .

[3]  Amy Pruden,et al.  Microbial community response of nitrifying sequencing batch reactors to silver, zero-valent iron, titanium dioxide and cerium dioxide nanomaterials. , 2015, Water research.

[4]  A. McBain,et al.  Altered Competitive Fitness, Antimicrobial Susceptibility, and Cellular Morphology in a Triclosan-Induced Small-Colony Variant of Staphylococcus aureus , 2015, Antimicrobial Agents and Chemotherapy.

[5]  C. Fajardo,et al.  Molecular Stress Responses to Nano-Sized Zero-Valent Iron (nZVI) Particles in the Soil Bacterium Pseudomonas stutzeri , 2014, PloS one.

[6]  Ho-Wen Chen,et al.  Monitoring of ORP, pH and DO in heterogeneous Fenton oxidation using nZVI as a catalyst for the treatment of azo-dye textile wastewater , 2014 .

[7]  D. Sedlak,et al.  Inactivation of Escherichia coli by Nanoparticulate Zerovalent Iron and Ferrous Ion , 2010, Applied and Environmental Microbiology.

[8]  Bernd Nowack,et al.  Application of nanoscale zero valent iron (NZVI) for groundwater remediation in Europe , 2012, Environmental Science and Pollution Research.

[9]  Arturo A. Keller,et al.  Toxicity of Nano-Zero Valent Iron to Freshwater and Marine Organisms , 2012, PloS one.

[10]  J. Ramos,et al.  Mechanisms of solvent resistance mediated by interplay of cellular factors in Pseudomonas putida. , 2015, FEMS microbiology reviews.

[11]  V. H. Liao,et al.  Nanoscale zerovalent iron (nZVI) at environmentally relevant concentrations induced multigenerational reproductive toxicity in Caenorhabditis elegans. , 2016, Chemosphere.

[12]  F. Bai,et al.  Real-Time Visualization of Perylene Nanoclusters in Water and Their Partitioning to Graphene Surface and Macrophage Cells. , 2015, Environmental science & technology.

[13]  C. Fajardo,et al.  Effects of Nano Zero-Valent Iron on Klebsiella oxytoca and Stress Response , 2013, Microbial Ecology.

[14]  M. Yao,et al.  Use of zero-valent iron nanoparticles in inactivating microbes. , 2009, Water research.

[15]  L. Wackett,et al.  Degradation of trichloroethylene by toluene dioxygenase in whole-cell studies with Pseudomonas putida F1 , 1988, Applied and environmental microbiology.

[16]  Leen Bastiaens,et al.  Inhibition of sulfate reducing bacteria in aquifer sediment by iron nanoparticles. , 2014, Water research.

[17]  J. Gottfries,et al.  Effect of Low Temperature on Growth and Ultra-Structure of Staphylococcus spp , 2012, PloS one.

[18]  C. Fajardo,et al.  Transcriptional and proteomic stress responses of a soil bacterium Bacillus cereus to nanosized zero-valent iron (nZVI) particles. , 2013, Chemosphere.

[19]  J. Trevors,et al.  Cytoplasmic membrane response to copper and nickel in Acidithiobacillus ferrooxidans. , 2011, Microbiological research.

[20]  Q. Huang,et al.  Adhesion of bacterial pathogens to soil colloidal particles: influences of cell type, natural organic matter, and solution chemistry. , 2014, Water research.

[21]  D. Elliott,et al.  Field assessment of nanoscale bimetallic particles for groundwater treatment. , 2001, Environmental science & technology.

[22]  M. Černík,et al.  Oxidative stress induced in microorganisms by zero-valent iron nanoparticles. , 2011, Microbes and environments.

[23]  Mark R Wiesner,et al.  Effect of a fullerene water suspension on bacterial phospholipids and membrane phase behavior. , 2007, Environmental science & technology.

[24]  Heterogeneity as an adaptive trait of microbial populations , 2013, Microbiology.

[25]  H. Heipieper,et al.  Adaptation of the Hydrocarbonoclastic Bacterium Alcanivorax borkumensis SK2 to Alkanes and Toxic Organic Compounds: a Physiological and Transcriptomic Approach , 2013, Applied and Environmental Microbiology.

[26]  C. Rock,et al.  Membrane lipid homeostasis in bacteria , 2008, Nature Reviews Microbiology.

[27]  Pedro J J Alvarez,et al.  Adsorbed polymer and NOM limits adhesion and toxicity of nano scale zerovalent iron to E. coli. , 2010, Environmental science & technology.

[28]  Thomas Kuhlbusch,et al.  Fate and Bioavailability of Engineered Nanoparticles in Soils: A Review , 2014 .

[29]  A. Mukherjee,et al.  Toxic behavior of silver and zinc oxide nanoparticles on environmental microorganisms , 2014, Journal of basic microbiology.

[30]  Kara L Nelson,et al.  Bactericidal effect of zero-valent iron nanoparticles on Escherichia coli. , 2008, Environmental science & technology.

[31]  Mark R Wiesner,et al.  A review of the environmental implications of in situ remediation by nanoscale zero valent iron (nZVI): Behavior, transport and impacts on microbial communities. , 2016, The Science of the total environment.

[32]  Eakalak Khan,et al.  Role of oxidative stress in inactivation of Escherichia coli BW25113 by nanoscale zero-valent iron. , 2016, The Science of the total environment.

[33]  Christer S. Ejsing,et al.  Homeoviscous Adaptation and the Regulation of Membrane Lipids. , 2016, Journal of molecular biology.

[34]  S. Leibler,et al.  Bacterial Persistence as a Phenotypic Switch , 2004, Science.

[35]  O. Kuipers,et al.  Bistability, epigenetics, and bet-hedging in bacteria. , 2008, Annual review of microbiology.

[36]  Milica Velimirovic,et al.  Use of CAH-degrading bacteria as test-organisms for evaluating the impact of fine zerovalent iron particles on the anaerobic subsurface environment. , 2015, Chemosphere.

[37]  Ilkeun Lee,et al.  Surface characteristics and adhesion behavior of Escherichia coli O157:H7: role of extracellular macromolecules. , 2009, Biomacromolecules.

[38]  Yong Sik Ok,et al.  Review on nano zerovalent iron (nZVI): From synthesis to environmental applications , 2016 .

[39]  Marie Simonin,et al.  Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review , 2015, Environmental Science and Pollution Research.

[40]  Pedro J J Alvarez,et al.  Effects of nano-scale zero-valent iron particles on a mixed culture dechlorinating trichloroethylene. , 2010, Bioresource technology.

[41]  S. Klumpp,et al.  Population Dynamics of Bacterial Persistence , 2013, PloS one.

[42]  R. Naidu,et al.  Nanoscale zero-valent iron as a catalyst for heterogeneous Fenton oxidation of amoxicillin , 2014 .

[43]  G. Lowry,et al.  Effect of particle age (Fe0 content) and solution pH on NZVI reactivity: H2 evolution and TCE dechlorination. , 2006, Environmental science & technology.

[44]  J. Trevors,et al.  Cytoplasmic membrane fluidity and fatty acid composition of Acidithiobacillus ferrooxidans in response to pH stress , 2010, Extremophiles.

[45]  Arturo A. Keller,et al.  Persistence of commercial nanoscaled zero-valent iron (nZVI) and by-products , 2013, Journal of Nanoparticle Research.

[46]  H. Heipieper,et al.  Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes , 1994, Applied and environmental microbiology.

[47]  K. Dercová,et al.  Response Mechanisms of Bacterial Degraders to Environmental Contaminants on the Level of Cell Walls and Cytoplasmic Membrane , 2014, International journal of microbiology.

[48]  H. Heipieper,et al.  The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. , 2003, FEMS microbiology letters.

[49]  J. Modak,et al.  Soft-particle model analysis of effect of LPS on electrophoretic softness of Acidithiobacillus ferrooxidans grown in presence of different metal ions. , 2009, Colloids and surfaces. B, Biointerfaces.

[50]  O. B. Popova,et al.  Effects of copper and cadmium ions on the physicochemical properties of lipids of the marine bacterium Pseudomonas putida IB28 at different growth temperatures , 2008, Russian Journal of Marine Biology.

[51]  F. Champlin,et al.  Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. , 2001, Journal of microbiological methods.

[52]  C. Pagnout,et al.  Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward Escherichia coli. , 2012, Colloids and surfaces. B, Biointerfaces.

[53]  C. Haynes,et al.  Toxicity of engineered nanoparticles in the environment. , 2013, Analytical chemistry.

[54]  H. Heipieper,et al.  Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity , 1992, Applied and environmental microbiology.

[55]  Damià Barceló,et al.  Considerations of Environmentally Relevant Test Conditions for Improved Evaluation of Ecological Hazards of Engineered Nanomaterials. , 2016, Environmental science & technology.

[56]  X. Xia,et al.  Modification of Fatty acids in membranes of bacteria: implication for an adaptive mechanism to the toxicity of carbon nanotubes. , 2014, Environmental science & technology.

[57]  Z. Tong,et al.  Response of soil microorganisms to As-produced and functionalized single-wall carbon nanotubes (SWNTs). , 2012, Environmental science & technology.

[58]  M. Elimelech,et al.  Relevance of electrokinetic theory for "soft" particles to bacterial cells: implications for bacterial adhesion. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[59]  Baikun Li,et al.  Bacterial adhesion to glass and metal-oxide surfaces. , 2004, Colloids and surfaces. B, Biointerfaces.

[60]  K. Henn,et al.  Utilization of nanoscale zero‐valent iron for source remediation—A case study , 2006 .

[61]  Ranjit T Koodali,et al.  Size-dependent bacterial growth inhibition and mechanism of antibacterial activity of zinc oxide nanoparticles. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[62]  A. D. Syakti,et al.  Use of electrospray ionization mass spectrometry for profiling of crude oil effects on the phospholipid molecular species of two marine bacteria. , 2005, Rapid communications in mass spectrometry : RCM.

[63]  Magdalena Kwolek-Mirek,et al.  Comparison of methods used for assessing the viability and vitality of yeast cells. , 2014, FEMS yeast research.

[64]  J. Shim,et al.  Changes in Membrane Fluidity and Fatty Acid Composition of Pseudomonas putida CN-T19 in Response to Toluene , 2002, Bioscience, biotechnology, and biochemistry.

[65]  Tanapon Phenrat,et al.  Partial oxidation ("aging") and surface modification decrease the toxicity of nanosized zerovalent iron. , 2009, Environmental science & technology.

[66]  Y. Hwang,et al.  Potential environmental implications of nanoscale zero-valent iron particles for environmental remediation , 2014, Environmental health and toxicology.

[67]  Christopher M. Hessler,et al.  The influence of capsular extracellular polymeric substances on the interaction between TiO₂ nanoparticles and planktonic bacteria. , 2012, Water research.

[68]  N. Joshi,et al.  Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances. , 2012, Journal of hazardous materials.

[69]  Wei Wang,et al.  Nanoscale zero-valent iron (nZVI) for the treatment of concentrated Cu(II) wastewater: a field demonstration. , 2014, Environmental science. Processes & impacts.

[70]  Xingzai Chen,et al.  Review on Nano zerovalent Iron (nZVI): From Modification to Environmental Applications , 2017 .

[71]  H. Heipieper,et al.  Effect of silver nanoparticles and silver ions on growth and adaptive response mechanisms of Pseudomonas putida mt-2. , 2014, FEMS microbiology letters.

[72]  P. Bremer,et al.  Mechanisms of Cation Exchange by Pseudomonas aeruginosa PAO1 and PAO1 wbpL, a Strain with a Truncated Lipopolysaccharide , 2008, Applied and Environmental Microbiology.

[73]  R. Nogueira,et al.  2,4-Dichlorophenoxyacetic acid (2,4-D) degradation promoted by nanoparticulate zerovalent iron (nZVI) in aerobic suspensions , 2013 .

[74]  J. Giddings,et al.  Effects analysis of time‐varying or repeated exposures in aquatic ecological risk assessment of agrochemicals , 2002, Environmental toxicology and chemistry.

[75]  Marie Simonin,et al.  Combined Study of Titanium Dioxide Nanoparticle Transport and Toxicity on Microbial Nitrifying Communities under Single and Repeated Exposures in Soil Columns. , 2016, Environmental science & technology.

[76]  J. Lead,et al.  Transformations of nanomaterials in the environment. , 2012, Environmental science & technology.

[77]  G. Zeng,et al.  The interactions between nanoscale zero-valent iron and microbes in the subsurface environment: A review. , 2017, Journal of hazardous materials.

[78]  Armand Masion,et al.  Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli. , 2008, Environmental science & technology.

[79]  Khara D Grieger,et al.  Environmental benefits and risks of zero-valent iron nanoparticles (nZVI) for in situ remediation: risk mitigation or trade-off? , 2010, Journal of contaminant hydrology.

[80]  Guanjun Chen,et al.  Physiological and transcriptomic analyses reveal mechanistic insight into the adaption of marine Bacillus subtilis C01 to alumina nanoparticles , 2016, Scientific Reports.

[81]  Mallavarapu Megharaj,et al.  Inhibition or promotion of biodegradation of nitrate by Paracoccus sp. in the presence of nanoscale zero-valent iron. , 2015, The Science of the total environment.

[82]  Pedro J J Alvarez,et al.  Effect of natural organic matter on toxicity and reactivity of nano-scale zero-valent iron. , 2011, Water research.

[83]  D. O’Carroll,et al.  Nanoscale zero valent iron and bimetallic particles for contaminated site remediation , 2013 .

[84]  Eakalak Khan,et al.  Impact of nanoscale zero valent iron on bacteria is growth phase dependent. , 2016, Chemosphere.

[85]  C. Fajardo,et al.  Integrating classical and molecular approaches to evaluate the impact of nanosized zero-valent iron (nZVI) on soil organisms. , 2014, Chemosphere.