Biogenic Cyanide Production Promotes Dissolution of Gold

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Environmental Processes

Biogenic cyanide production promotes dissolution of gold nanoparticles in soil Eric McGivney, Xiaoyu Gao, Yijing Liu, Gregory V. Lowry, Elizabeth A. Casman, Kelvin B. Gregory, Jeanne M. Vanbriesen, and Astrid Avellan Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b05884 • Publication Date (Web): 28 Dec 2018 Downloaded from http://pubs.acs.org on January 3, 2019

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Environmental Science & Technology

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Biogenic cyanide production promotes dissolution

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of gold nanoparticles in soil

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Eric McGivney§†‡, Xiaoyu Gao§‡, Yijing Liu§, Gregory V. Lowry§, Elizabeth Casman§, Kelvin

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B. Gregory§, Jeanne M. VanBriesen§, Astrid Avellan§*

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§Civil

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15213, United States

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*Corresponding

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†Current

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Stockholm University, Svante Arrhenius väg 8, SE-106 91 Stockholm, Sweden

and Environmental Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania

author: [email protected]

address: Department of Environmental Science and Analytical Chemistry,

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‡These authors contributed equally.

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Author Contributions: The manuscript was written through contributions of all

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authors. All authors have given approval to the final version of the

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manuscript.

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ACS Paragon Plus Environment


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ABSTRACT: Gold nanoparticles (Au NPs) are often used to study the physiochemical

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behavior and distribution of nanomaterials in natural systems because they are assumed to be

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inert under environmental conditions, even though Au can be oxidized and dissolved by a

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common environmental compound: cyanide. We used the cyanogenic soil bacterium,

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Chromobacterium violaceum, to demonstrate that quorum-sensing-regulated cyanide

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production could lead to a high rate of oxidative dissolution of Au NPs in soil. After 7 days of

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incubation in a pH 7.0 soil inoculated with C. violaceum, labile Au concentration increased

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from 0 to 15%. There was no observable dissolution when Au NPs were incubated in abiotic

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soil. In the same soil adjusted to pH 7.5, labile Au concentration increased up to 29% over the

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same time frame. Furthermore, by using a quorum-sensing-deficient mutant of C. violaceum,

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CV026, we demonstrated that Au dissolution required quorum-sensing-regulated cyanide

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production in soil. Au NP dissolution experiments in liquid media coupled with mass

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spectrometry analysis confirmed that biogenic cyanide oxidized Au NPs to soluble Au(CN)2-.

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These results demonstrate under which conditions biologically-enhanced metal dissolution

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can contribute to the overall geochemical transformation kinetics of nanoparticle in soils, even

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though the materials may be inert in abiotic environments.

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Introduction

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The dissolution of metal nanoparticles (NP), and subsequent release of ionic species,

35

modulates NP fate, transport, and environmental impact1–5. Dissolution has been identified as

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one of the most important predictors of fate in environmental models6, and toxicity in nano-

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environmental health and safety (nano-EHS)7.

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Gold nanoparticles (Au NP) are stable against oxidative dissolution under most

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environmental conditions and are used as such to study the distribution of nanomaterials in

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environmental and biological systems8–16. Au NPs are also modeled in nano-EHS modeling



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studies under the assumption that they will not undergo dissolution nor transformation13,17.

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However, the core element of Au NPs, metallic Au0, can be oxidized and solubilized by a

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common environmental constituent18, cyanide, following the reaction19,20,

44 45

Equation 1: 4𝐴𝑢 + 8𝑁𝑎𝐶𝑁 + 𝑂2 + 2𝐻2𝑂⇌4[𝑁𝑎𝐴𝑢(𝐶𝑁)2] + 4𝑁𝑎𝑂𝐻

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Cyanide is ubiquitous in the environment due to its formation in biological processes18.

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Certain bacteria, fungi, and plants produce cyanide compounds to deter pathogenic attacks

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and to regulate biochemical processes18,21. In bacteria, cyanide is a secondary metabolite,

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produced by common soil bacteria,

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Rhizobium, and Serratia genera22. Bacterially-produced cyanide plays an important ecological

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role in soils, altering plant growth22, invertebrate toxicity23, and fungal pathogenicity24.

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Cyanogenic bacteria also have commercial applications for Au recovery from sulfidic ores25,26

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and e-waste19,27, and have even been considered as soil supplements to enhance crop yields by

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limiting the growth of competitive plants28,29.

members of the Pseudomonas, Chromobacterium,

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Cyanogenesis in Pseudomonas aeruginosa30 and Chromobacterium violaceum22 is

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regulated by quorum sensing (QS), i.e., a threshold cell-density is required to produce

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cyanide. Cyanide is generally produced in the µM-range (1-200 µM) by planktonic bacteria22,

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but in QS-regulated biofilms of the Burkholderia cepia complex, cyanide concentrations can

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reach the mM-range (up to 19 mM)31. Thus, the size and structure of the microbial population

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affects cyanide production, which may affect the potential for Au dissolution. In several

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studies, biofilms have been identified as one of the most important sinks for Au in

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environmental tracer experiments of Au NPs8,15.

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The mechanisms and kinetics of cyanide-promoted oxidative dissolution of Au have been

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studied in laboratory settings, including with Au surfaces19,20, colloidal Au32, and Au

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nanorods33. Due to high specific surface area, nano- and colloidal-Au dissolution half-life


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kinetics in cyanide solutions are on the order of seconds32,33. Oxidative dissolution of Au NPs

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has largely been overlooked in environmental nanotechnology research altogether, with a few

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exceptions that monitored the absence of Au dissolution34–36 or oxidation34,37, or speculated

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about the possibility of dissolution38. A recent study demonstrated that a freshwater

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macrophyte biofilm induced oxidation of Au NPs, forming complexes with cyanide,

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hydroxyls, and thiol groups15.

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The potential for Au biotransformation by bacteria in soils has been studied in the past, and

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some authors proposed bio-geochemical models of Au cycling in soils39,40. One study found a

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correlation between Au solubilization in soil and the presence of microorganisms41, and

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several other studies have enhanced Au dissolution in liquid cultures of isolated cyanogenic

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soil bacteria cultivated under cyanide-forming condition25,42–44. However, to the best of our

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knowledge, no prior Au NP work has included soils containing cyanide or cyanogenic-

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bacteria, and currently, the parameters that drive cyanide-mediated Au NP dissolution in soils

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are not known.

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The physiochemical characteristics of the system may influence Au NPs dissolution.

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Bacteria produce cyanide as HCN which has a pKa of 9.21 (I=0, T= 298 K)18. Thus, pH

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controls the speciation of cyanide, which affects Au dissolution. The lower the pH, the lower

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the Au dissolution because cyanide will only promote the oxidation of Au when it is

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deprotonated, in its free ion state, CN- (Equation 1).

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In the present work, we test the ability of a cyanogenic soil bacterium, Chromobacterium

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violaceum, to oxidize and solubilize Au NPs in soils. C. violaceum has previously been used

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as a model organism in QS22,45,46 and Au-recovery research25,27. Here, we assessed how Au

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NP dissolution was affected by (i) QS-regulated cyanide production by using a QS-negative

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mutant, CV026, and looking for Au dissolution at different inoculant-cell densities (ii)

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changes in soil pH, and (iii) the type of medium (e.g. soil vs. liquid cultures and abiotic



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cyanide solutions). These last measurements allowed us to investigate the mechanism of Au

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NPs oxidation and confirm dissolution mechanisms in soil.

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Materials and Methods

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Materials

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DTPA (99%, titration), ammonium acetate, and sodium cyanide were purchased from

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Sigma-Aldrich. Calcium chloride (≥99.0%, ACS grade) was purchased from Fisher Scientific.

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12 nm citrate-stabilized Au nanoparticles (Au NPs) were provided by the Center for the

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Environmental Implications of NanoTechnology (CEINT, Durham, NC, USA); synthesized as

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previously described47. Standard soil (Lufa 2.1, sandy soil) was purchased from Lufa Speyer

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(Germany). Chromobacterium violaceum ATCC 31532 was purchased from ATCC.

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Chromobacterium violaceum CV026, a mini-Tn5 mutant45, was acquired through the

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Colección Española de Cultivos Tipo (CECT 5999). Prior to experimentation ATCC 31532

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was grown over night in LB media and CV026 was grown in LB media containing 50 μg/mL

104

kanamycin. All growth cultures were supplemented with glycine, an amino acid commonly

105

found in rhizosphere soil49 and the metabolic precursor in bacterial cyanide production48.

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The Au NPs used in this study were synthesized and characterized by the Center of

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Environmental Implications of NanoTechnology (CEINT, Duke University): primary particle

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size of 11.8±1.2 nm (TEM based), hydrodynamic diameter of 11.9±0.2 nm, and a zeta

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potential of -14.1±1 mV at pH 7.0 in 10-3 M of KCl.

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Au NP dissolution in soil

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Soil preparation. Prior to experimentation, a standard soil (Lufa 2.1, characterized

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previously50) was air dried for 24 hours before adjusting the pH from 4.9 (original soil pH) to

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7.0 (by adding 0.02 g CaO + 0.02 g CaCO3 per 10 g of soil) or to pH 7.5 (by adding 0.025 g

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CaO + 0.03 g CaCO3 per 10 g of soil). The pH-adjusted soil was then aged for 5 days before


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being autoclaved three times and tested for sterility via plating (LB 1.5% agar, 30°C). No

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growth was observed after plating. The total organic carbon content was 0.56±0.02% (±SD)

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and 0.53±0.02% (±SD) before and after autoclaving, respectively (InnovOx Laboratory TOC

118

Analyzer, GE Analytical Instruments).

119

Au NP dosing and bacteria inoculation. Au NP dissolution in soil was measured in the

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presence and absence of C. violaceum, and at two different soil pH values (7.0 and 7.5, see

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Table 1 and Figure S1). These pH values were chosen to simulate conditions with different

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relative concentrations of HCN and CN-.

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Air-dried soil was supplemented with a liquid medium (LB, 8 g/L glycine) containing Au

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NPs (final concentration of 1.9 mg/kg in soil, 19% moisture). The Au NP amended soil was

125

then mixed using sterile wooden sticks.

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C. violaceum was grown (30°C, 200 rpm, LB media + 8 g/L of glycine, pH 7.0) and washed

127

(centrifuged, following pellet resuspension in equivalent volume of growth media), before

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addition to soil (1.5 × 109 CFU/g soil, determined by plating). As an abiotic control, soil was

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supplemented with the sterile growth medium. The total soil moisture content in all

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experiments was 19%. All samples were prepared, in triplicate, in sterile 50 mL tubes sealed

131

with alcohol-sterilized Parafilm®, to allow for gas exchange while keeping the moisture

132

content constant, and stored in a 30°C incubator.

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As a QS-control experiment, pH 7.0 soil was inoculated with the QS-mutant CV026 (Table

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1). HCN production in C. violaceum is regulated by the hcnABC operon, and this operon is

135

upregulated via QS receptor/promoter cviR, i.e., when a quorum is reached, hcnABC activity

136

increases. The mutant strain CV026 has the hcnABC operon, but it lacks the functioning genes

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to produce QS signal N-hexanoyl homoserine lactone (cviI), meaning hcnABC is never over

138

expressed, even when cell density increases22,45,51.



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Finally, we considered the role of initial cell density on Au dissolution by evaluating

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induced Au dissolution in soil inoculated with lower cell densities of C. violaceum culture.

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Instead of inoculating the soil directly with a high cell density (1.5 × 109 CFU/g soil) liquid

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culture of C. violaceum at early stationary phase growth, we supplemented Au NP-containing

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soil with a low-cell density suspension. Specifically, 1 gram of soil incubated for 7 days with

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C. violaceum 1.5 × 109 CFU/g soil was mixed with 40 g of sterile, Au NP-containing soil

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(Table 1). The mixed soil was then incubated at 30°C, and Au dissolution was measured over

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7 days. This experiment is referred to as the ‘Aged’ sample in Table 1.

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Soil extraction for Au dissolution measurements. Dissolution of Au NPs in aqueous

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suspension can be measured by separating the ions from particles via ultracentrifugation52.

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Although it is challenging to measure the dissolution of NMs in soil due to the difficulty of

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separating the dissolved ions from the solid matrix, a recent study has developed a time based

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extraction method using diethylene triamine pentaacetic acid (DTPA) to directly measure the

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dissolution kinetics of metal based ENMs in soil50. DTPA is a strong chelating agent, and was

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shown to be able to extract both the metal dissolved in pore water and metal bound to soil

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solid surfaces (e.g. soil organic matter and clay53), which also represented most of the metal

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ions released by NMs50. The DTPA extractable fraction is often referred to as potentially

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available or labile metal in soil50,54,55.

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A time-based DTPA extraction was developed to measure the dissolved fraction of Au in

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soil after 0, 1, 2, 7 days based on previous studies investing the dissolution of CuO NPs50. The

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extraction efficiency was 116.9±3.9% (±SD), as determined by adding 2000 mg/kg of Au

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(delivered as HAuCl4) and 50 mg of NaCN to 50 g of soil before extraction after 4 days.

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For each extraction point, two grams of soil were air-dried and added to 4 ml of a mixture

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containing 0.01 M CaCl2, 0.005 M diethylenetriaminepentaacetic acid (DTPA) and 0.1 M

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triethanolamine (TEA) at pH 7.6. The samples were placed on a reciprocal shaker at 180 rpm


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for 2 hours. Next, the samples were centrifuged at 3000 rpm for 10 minutes. The supernatant

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of each sample was filtered through a 10 kDa centrifugal (10 minutes at 5000 ×g) filter before

166

being diluted with nitric acid (final nitric acid concentration= 2%) and analyzed via ICP-MS

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as described below. Pore water pH was determined as described previously50: 2 g of air-dried

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soil in 20 mL of 0.01 M CaCl2, shaken (2 hours at 180 rpm), centrifuged (3000 rpm for 10

169

minutes), and measuring the pH of the supernatant (Figure S1a). Colony-forming units were

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determined by mixing 0.1 g of soil in 1 mL of sterile soil before plating on LB plates, 1.5%

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agar (Figure S1b).

172 173 174 175

First order empirical dissolution kinetics. Au NP dissolution kinetics in soil were modeled using an empirical first-order dissolution kinetics model: Equation 2 𝑌 = (𝑌0 ― 𝑌𝑚𝑎𝑥)𝑒 ―𝑘𝑡 + 𝑌𝑚𝑎𝑥

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where Y0 is the initial dissolution value (%) of Au dissolved during the 20-minute soil

177

mixing period and the 2-hour extraction period, Ymax is the maximum dissolution (%), or

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plateau, and k is the observed first-order rate constant (day-1). Modeling was done using Prism

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(Version 7.0c for Mac, GraphPad Software, www.graphpad.com).

180

Au NP dissolution mechanisms in growth media.

181

The effect of a live culture and its supernatant (metabolites without cells) on Au NP

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dissolution was studied. C. violaceum was grown to 1010 CFU/mL (30°C, 200 rpm, LB media

183

+ 0.75 g/L of glycine, pH 7.0, according to48) before being centrifuged at 5000 ×g for 10

184

minutes (4°C). The supernatant was filtered (0.22 um, PTFE) into sterile 50 mL tubes and

185

used as the ‘Supernatant’ exposure medium (Table 1). The pellets were then resuspended in

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an equivalent volume of fresh growth medium to be used as the ‘Washed culture’ treatment

187

(Table 1). Separately, sterile growth medium was used as the ‘Control’ treatment. We added

188

1.9 mg/L (final concentration) Au NPs to each medium. Initial CN- concentrations in the



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‘Supernatant’, ‘Washed culture’, and ‘Control’ samples were 41.87±0.90 mg/l (±SD),

190

4.05±0.60 mg/l (±SD), and 0 mg/l, respectively. All samples were prepared in 10 mL volumes

191

in sterile 15 mL centrifugal tubes and placed on an end-over-end rotator for 7 days. At the

192

sampling time points of 0, 1, 2, and 7 days, 1.5 mL was removed and immediately filtered for

193

dissolved fraction metal analysis. Samples were filtered through 10 kDa membranes (5,000g,

194

10 minutes). All conditions were run in triplicate.

195

Au NP dissolution in cyanide solution

196

We studied Au NP dissolution in a simple aqueous buffer. Au NPs (1.9 mg/L) were placed

197

in autoclaved 20 mM ammonium acetate buffer (pH 7.0) in the presence of either 9.8 mg/L

198

NaCN (‘NaCN’, Table 1), or in the absence of NaCN (‘Control’, Table 1). All samples were

199

prepared in 10 mL volumes within sterile 15 mL centrifugal tubes and placed on an end-over-

200

end rotator for 7 days. At the sampling time points of 0, 1, 2, and 7 days, 1.5 mL was removed

201

and immediately filtered for dissolved fraction metal analysis through a 10 kDa membrane

202

(5,000g, 10 minutes). All samples were run in triplicate.

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Au and cyanide detection

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To measure Au, samples were diluted and acidified with nitric acid (final concentration of

205

2%) before being measured via inductively coupled plasma mass spectrometry (ICP-MS,

206

Agilent 7700 Series) under Hydrogen and High Energy Helium (HEHe) acquisition mode.

207

The calibration curve ranged from 25 nmol/l to 2.5 μmol/l. All diluted samples were within

208

the range of the calibration curve. Calibration samples were prepared prior to each

209

measurement.

210

Free cyanide concentration was determined by potentiometry with a cyanide-ion-selective

211

electrode according to the manufacturer’s protocol (Orion cyanide electrode, Thermo

212

Scientific). All standards and samples were stabilized with alkaline ionic strength adjustor

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solution (Orion, Thermo Scientific). The method detection limit was 5 µg/L.


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Detection of dicyanogold, Au(CN)2-, was determined via ESI-MS/MS, using a method

215

described previously56. Samples were filtered (0.22 µm) and analyzed on an LC-MS/MS

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(Agilent 6430 Triple Quad LC/MS/MS, Agilent 1100 Series). 10 µL of sample was delivered

217

to the MS using a 1:1 isocratic mixture of H2O (18 MΩcm):Methanol at a flow rate of 0.2

218

mL/min. The MS was run in negative polarity mode scanning (MS2 Scan) with a fragmentor

219

energy of 80 V and cell accelerator voltage of 7 V. Nitrogen was used as the sheath gas.

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Identification of Au(CN2)- was determined by monitoring the product ion at m/z 26, derived

221

from the parent ion at m/z 249 using Agilent MassHunter Qualitative Analysis Workstation

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Software (Agilent Technologies).

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SAFETY PRECAUTIONS

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HCN is highly toxic. Safety measures were taken to avoid the release of gaseous HCN

225

during lab work. All samples containing cyanide were handled under a fume hood to prevent

226

inhalation. Furthermore, extra care was taken to keep acidic solutions away from cyanide-

227

containing materials to avoid accidental mixing. Cyanide-containing waste was disposed of in

228

dedicated waste containers with excess NaOH to keep the solution basic and to avoid HCN

229

release.

230 231

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Results and Discussion

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Au NP dissolution in soil. The dissolution of Au NPs in environmental systems is often

234

considered to be negligible8–10,16. Indeed, we did not detect Au dissolution while monitoring

235

the dissolution of Au NPs in sterile soil (Figure 1a). However, when soil was supplemented

236

with a culture of early stationary-phase C. violaceum (1.5 × 109 CFU/g soil, Table1),

237

14.84±2.27% (±SD) of Au NPs dissolved after 7 days. Our results support the expected



238

cyanide-promoted oxidative-dissolution pathway (Equation 1). The expected dissolution

239

pathway is also supported by the effect of pH: when the pH was raised by 0.5 unit, from 7.0 to

240

7.5, in soil containing C. violaceum, there was a two-fold increase in dissolved Au, with a

241

maximum dissolution plateau of 30.76±3.32% (±SD) (Figure 1a). The increase in Au NP

242

dissolution in response to an increase in pH is explained by pKa value of HCN, so a higher

243

pH would result in higher concentration of free CN-, which is required for the oxidative

244

dissolution and mobility of Au. Modeled cyanide speciation in water at pH 7.0 is 0.61% ionic

245

form, CN-, while at pH 7.5, 1.91% of cyanide would exist as CN-, about a 3-fold increase. The

246

higher CN- concentration would be expected to lead to higher Au dissolution at higher pH.

247

According to equation 1, the dissolution process should also increase the pH of the system.

248

However, soil has the buffering capacity to neutralize the pH changes57 resulting from

249

dissolution. The stability of pH measured over time is evidence of this buffering capacity

250

(Figure S1).

251

The pH 7.5 treatment resulted in higher initial dissolution values, Y0, but similar first-order

252

rate constants to pH 7.0 soils (Table 2). The similar dissolution rate between the two

253

treatments (pH 7.0 and pH 7.5) suggests that the oxidative dissolution of Au was not the rate-

254

limiting step resulting in the slow increase of dissolved Au over time. Rather, the rate of CN-

255

production in soil likely controls the overall kinetics of Au NP dissolution.

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The relation between cell density and Au NP dissolution was studied by mixing 40 g of

257

sterile Au NP-containing soil with 1 gram of soil inoculated with C. violaceum, at pH 7.0 and

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aged 7 days—which gave an initial CN- concentration of 0.05 mmol CN-/g soil and cell

259

concentration of 4 x 104 CFU/g soil. The onset of dissolution was delayed by a day, but the

260

dissolution plateau reached after 7 days, 13.93±0.86% (±SD), was nearly identical to the

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maximum dissolution plateau reached when soil was inoculated with the early stationary-

262

phase liquid culture of C. violaceum (Figure 1b). The fact that similar dissolution plateaus


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were reached when the soil was inoculated with different cell densities at the same pH

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suggests that maximum dissolution is limited by free CN-, which is limited by pH.

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Quorum sensing regulates HCN production in C. violaceum, i.e., the cell concentration

266

must reach a certain density before cyanide synthesis begins22. The observation that both

267

experimental designs resulted in about ~13% Au dissolution after 7 days at pH 7.0 suggests

268

that even at different inoculum concentrations, C. violaceum reached cell densities to support

269

QS-regulated cyanide production. The requirement of QS-regulated cyanide production was

270

further assessed by inoculating Au NP-containing soil with the QS-mutant CV026 (1.5 × 108

271

CFU/g soil, Figure 1), and no Au dissolution was detected over 7 days.

272 273

Table 1. Au NP dissolution experimental matrices Soil

Sample identification

Au

NP, Initial CN-, pH Inoculum

mg/L

mg/L

C. violaceum, pH 7.0

1.9

41.8

7.0 1.5 × 109

C. violaceum, pH 7.5

1.9

41.8

7.5 1.5 × 109

Abiotic

1.9

0

7.0 0

CV026

1.9

0

7.0 1.5 × 109

Aged

1.9

R2, Figure 3b), meaning Au NP dissolution increased after a cell

302

density threshold was achieved, characteristic of the delay associated with a cell

303

concentration-based quorum response.

304



305

Figure 2. (a) Dissolution of Au NP after 24 hours in sterile LB media, early-stationary phase

306

cultures of C. violaceum that had been rinsed in LB media, or the supernatant of an early-

307

stationary stage culture of C. violaceum. (b) Detection of Au(CN)2- using an ESI-MS/MS

308

procedure by monitoring the produced cyanide ion, m/z 26, from the dicyanogold parent ion,

309

m/z 249.

310

311 312

Figure 3. (a) Au NP dissolution (%) and cyanide production (mg/L, secondary y-axis) over

313

time with an inlay that plots Au dissolution versus CN-. (b) Au dissolution (%) and cell


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growth (OD600, secondary y-axis) over time with an inlay that plots Au dissolution versus

315

OD600. The legends of the inlays report the R2 and Spearman’s rho (ρ).

316

Au NP dissolution in abiotic cyanide solution. In the abiotic buffer experiments (Figure

317

S2), 9.8 mg/L (0.20 mM) of NaCN (pH 7.0) dissolved 80.02±2.03% (±SD) of Au NPs and

318

dicyanogold complexes were detected (Figure S2). No Au dissolution nor dicyanogold was

319

detected in the control. In the abiotic cyanide solutions, Au dissolution was fast: 23.70%

320

dissolution within seconds of starting the experiment (Figure S3). In biological systems,

321

cyanide production, driven by quorum sensing, and thus, cell density, is likely to be the rate-

322

limiting step controlling the overall observed dissolution kinetics. This is in agreement with

323

our speculation explaining the similar half-life observed for Au NP dissolution in soils with

324

different pH (Table 2), and with the observation of the one-day delay of Au-dissolution in the

325

aged treatment (Figure 1a). Au NP dissolution was much higher in cyanide solutions

326

compared to soil, despite having less total CN- in the system. This is likely due to the

327

competitive complexing agents, both metals and organics, commonly found in soils

328

(reviewed18).

329

Implications. Au NPs were oxidized and solubilized to Au(CN)2- by C. violaceum in soil

330

within days. Au NP dissolution was limited by QS-regulated CN- production and the pH of

331

the soil. These results highlight the importance of microorganisms on metal NPs

332

transformation for materials, such as Au, that are inert in abiotic systems.

333

Importantly, C. violaceum is just one cyanogenic organism among many. Species of

334

Pseudomonas, Rhizobium, and several cyanobacteria are also cyanogenic28, as well as many

335

plants58 and some species of fungi18. Over 2650 species of plants, including several

336

industrially important crops (corn, lima beans, cassava, sorghum, and alfalfa) generate

337

cyanide as part of their metabolism18. Cyanide can be found in both leaf and root tissue,

338

ranging from 0-8000 mgHCN per kg of freshweight depending on the plant species. Several



339

species of funghi are cyanogenic, e.g., Actinomycetes, Basidiomycetes, Clitocybe, Marasmius,

340

Pholiota, Polyporus, and Tricholoma21.

341

Environmental cyanide concentrations are generally low in surface waters (ppb-level18).

342

However, bacteria are capable of forming dense biofilms where cyanide concentrations can

343

reach mg/Kg-levels31, potentially inducing a significant NPs transformation in these

344

biologically active compartments15. In addition to cyanogensis, sufficient oxygen (at least

345

pO2 > 0.01) is needed for Au to undergo oxidative-dissolution, so anaerobic systems are less

346

likely to observe AuNP dissolution59.

347

Biotransformations are likely to drive NP fate in NPs-accumulating compartments. Indeed,

348

Au NPs were found to significantly accumulate in biofilms8,9,15, from where Au has been

349

shown to enter the food chain60. A study on NP distribution in estuarine environments found

350

that uncharacterized biofilms were a major sink for Au nanorods8, with a water chemistry of

351

high pH values (7.9–8.5) and dissolved oxygen levels between 4–12 mg/L. These conditions

352

would be favorable to cyanide-induced oxidative dissolution15.

353

Soil pH is an important parameter driving the potential for cyanide-driven dissolution,

354

where a change in pH of 0.5 unit doubled the amount of dissolved Au. At lower pH, however,

355

such dissolution processes might not be as important due to the high pKa HCN. The

356

properties of the soil matrix can thus significantly change the observed biotransformations.

357

There are other parameters that have not been studied that are likely to influence biologically-

358

enhanced dissolution of Au NPs as well. For instance, the concentration glycine, a metabolic

359

precursor of HCN production in bacteria and fungi48, would likely influence cyanide-

360

dissolution. In this work, the organic matter in soil did not include any dissolution of AuNP.

361

This is likely due to the weak complexation between Au3+ and organic matter compared to

362

other metal-organic matter complexes. However, high sulfur functional groups containing

363

OM might have higher binding capacity to Au3+. The soil used in this study is a sandy soil


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with low clay content and did not affect the dissolution of AuNPs. However, higher clay

365

content may also affect the dissolution of Au NP by changing the aggregation state of Au NPs

366

and providing more surface to adsorb Au3+. Additionally, the homo- and hetero-aggregation states

367

of Au NPs in soils may influence dissolution kinetics61. Furthermore, the presence of other

368

cyanide-metabolizing organisms62–64 or quorum-quenching enzymes65,66 could decrease the

369

overall CN concentrations. There are also other metabolites, such as siderophores67,68 and

370

quorum sensing signals69,70, which can complex metal ions, potentially contributing to metal

371

NP dissolution. These could be interesting topics for further dissolution studies.

372

The fate and transport of cyanide in the environment is a factor of biotic (e.g., microbial

373

degradation, plant uptake) and abiotic (e.g., UV irradiation, volatilization, advection,

374

dispersion, adsorption) processes. However, cyanide does not generally accumulate in nature.

375

There are biotic processes, such as microbial degradation and plant uptake that incorporate

376

cyanide into natural nitrogen cycling. There are some sinks of HCN, such as adsorption and

377

complexation with metals (e.g., Ag, Co, Ni, Cu, or Fe) and sorption to organic matter or

378

minerals (e.g., iron oxides). The stability constant of Au(CN)2- (logK at 25°C = 126) is

379

significantly higher compared to that of other metals74,75, and the complexing reaction would

380

be the dominant reaction rather than oxidation-precipitation process. But for other metals (e.g.

381

logK for Fe(CN)63+ is 39.6, with 6 coordinates), at pH 7, precipitation would be important

382

(logKsp=-38.2 for Fe((OH)3) rather than complexation. At a lower pH, however, the effect of

383

iron on Au dissolution would be more significant because complexation of iron with CN-

384

would occur rather than participation.

385

Gold tracer studies that make no distinction between dissolved and particulate Au may

386

overstate the persistence of the particulate form if the biological conditions for cyanide-

387

enabled dissolution are met. Furthermore, the results presented here suggest that Au NPs

388

released to the environment could solubilize and enter the biogeochemical cycle of Au. In



389

geochemical fate models71,72, instead of assuming that there is no Au NP transformation,

390

appropriate dissolution rates should be included based on the properties of the environment

391

and the expected presence of key organisms. Future studies that use Au NPs in soils as a

392

tracer to investigate aggregation behavior or NP uptake should rule out the possibility of

393

cyanogenic organisms, or consider them. Although extensive efforts have been made to

394

standardize the methods to characterize engineered NP properties in environmental media73,

395

including the dissolution of NPs in different environmental matrices, the role of

396

(micro)organisms and their released metabolites on these properties has been neglected. Our

397

study illustrates the potential consequences of this omission in the case of Au NPs.

398

Cyanide-driven dissolution of metals is an important factor in environmental NP

399

transformations, and one that has been overlooked in the field of environmental

400

nanotechnology. These transformations are the result of a complex interplay between

401

microorganisms in soil, bacterial communication networks (quorum sensing), released

402

metabolites, and matrix chemistry.

403

Supporting information (SI)

404

The Supporting Information contains details on: soil pH and colony-forming units of C.

405

violcaeum in soil; Au NP dissolution and Au(CN)2- detection in a cyanide solution. The

406

Supporting Information is available free of charge on the ACS publication website.

407

Acknowledgment

408

This work was supported by the National Science Foundation (NSF) and the Environmental

409

Protection Agency (EPA) under NSF Cooperative Agreement EF-0830093 and DBI-1266252,

410

Center for the Environmental Implications of NanoTechnology (CEINT).


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Biogenic Cyanide Production Promotes Dissolution of Gold

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