Amino acid secretion influences the size and composition of copper carbonate nanoparticles synthesized by ureolytic fungi
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The ureolytic activity of Neurospora crassa results in an alkaline carbonate-rich culture medium which can precipitate soluble metals as insoluble carbonates. Such carbonates are smaller, often of nanoscale dimensions, than metal carbonates synthesized abiotically which infers that fungal excreted products can markedly affect particle size. In this work, it was found that amino acid excretion was a significant factor in affecting the particle size of copper carbonate. Eleven different amino acids were found to be secreted by Neurospora crassa, and l-glutamic acid, l-aspartic acid and l-cysteine were chosen to examine the impact of amino acids on the morphology and chemical composition of copper carbonate minerals. X-ray powder diffraction (XRPD), scanning electron microscopy (SEM), Fourier-transform infrared (FTIR) spectroscopy, thermogravimetric analysis (TGA) and X-ray photoelectron spectroscopy (XPS) were used to characterize the obtained copper carbonate samples. Copper carbonate nanoparticles with a diameter of 100–200 nm were produced with l-glutamic acid, and the presence of l-glutamic acid was found to stabilize these particles in the early phase of crystal growth and prevent them from aggregation. FTIR and TG analysis revealed that the amino acid moieties were intimately associated with the copper mineral particles. Component analysis of the final products of TG analysis of the copper minerals synthesized under various conditions showed the ultimate formation of Cu, Cu2O and Cu2S, suggesting a novel synthesis method for producing these useful Cu-containing materials.
KeywordsFungi Biomineralization Copper carbonate Nanoparticles Amino acids
Copper nanoparticles have been considered as a viable alternative to gold and silver nanoparticles due to lower cost, higher natural abundance and comparable electrical and thermal conductivity (Dabera et al. 2017; Kimber et al. 2018). Malachite (Cu2(OH)2CO3) is an important semi-precious mineral which has attracted extensive recent interest in various applications, for example, as coatings and catalysts (Gawande et al. 2016), and as an important precursor for the production of other Cu-bearing compounds such as CuO as well as Cu (Zhang et al. 2016). Malachite, in various morphologies, has been obtained by various synthetic routes, including spherical (RodrIguez-Clemente et al. 1994), hierarchical (where the structure is different at different length scales) (Xu and Xue 2005) and nanoscale (Saikia et al. 2013). The chemical and/or physical properties of such materials vary significantly as a function of crystal size, morphology and structure, even though these materials consist of the same chemical components (Hochella et al. 2008). The development of reliable and environmentally friendly technologies for the synthesis of malachite with controlled size and structure has therefore been attracting growing interest.
The use of filamentous fungi for nanoparticle synthesis represents a promising approach since fungi are able to secrete large amounts of chemical substances, for example, organic acids, amino acids and enzymes that may be involved in nanomaterial synthesis. The impact of such biological organic material on the biomineralization of carbonate minerals has been observed with both natural environmental samples and in laboratory studies (Braissant et al. 2003). Minerals frequently show a different ultrastructure and physico-chemical features in the presence of an organic matrix which can affect key events in mineral formation like nucleation and crystal growth stages (Briegel and Seto 2012; Jack et al. 2007; Jiang et al. 2017; Ngwenya et al. 2014). For example, Jiang et al. (2017) found that vaterite nanoparticles having a counterclockwise spiralling morphology could be induced by l-enantiomers of aspartic acid and glutamic acid, whereas a clockwise morphology was induced by d-enantiomers. However, there are very few reports on the impact of amino acids excreted by microorganisms on biomineralization of copper carbonate minerals and their potential industrial applications. The filamentous fungal growth form may also provide a template or scaffold for biomineral production that can be used to investigate the physical, chemical and biological properties of novel nanoparticles.
In this study, the influence of three amino acids (l-glutamic acid, l-aspartic acid and l-cysteine), which can be secreted by fungi, on biomineral formation was investigated. The chemical composition, morphology and thermal stability of copper carbonate synthesized by biomineralization, chemical synthesis in the presence of various amino acids, and inorganically synthesized minerals were investigated in order to characterize the mechanisms involved.
Materials and methods
Organism and media
The experimental fungus used in this study was Neurospora crassa (FGSC: 2489, Fungal Genetics Stock Centre (FGSC), Kansas, USA). It was routinely maintained on malt extract agar (MEA, Lab M limited, Bury, Lancashire, UK) in 90-mm diameter Petri dishes and grown at 25 °C in the dark. A urea-modified AP1 medium was used as the liquid media consisting of 2% (w/v) d-glucose (Merck, Readington Township, NJ, USA), 40 mM urea (Sigma-Aldrich, St. Louis, MO, USA), 4 mM K2HPO4∙3H2O (Sigma-Aldrich, USA), 0.8 mM MgSO4∙7H2O (Sigma-Aldrich, USA), 0.2 mM CaCl2∙6H2O (Sigma-Aldrich, USA), 1.7 mM NaCl (Sigma-Aldrich, USA), 9 × 10−3 mM FeCl3∙6H2O (Sigma-Aldrich, USA) and trace metals 0.014 mM ZnSO4∙7H2O (VWR, Radnor, PA, USA), 0.018 mM MnSO4∙4H2O (Sigma-Aldrich, USA) and 1.6 × 10−3 mM CuSO4∙5H2O (VWR, USA) (Li et al. 2014). After 3 days growth in the full AP1 medium, fungal biomass was collected and washed twice in sterile MilliQ water after centrifugation (× 4000g, 30 min), and continued to be incubated in a sterile phosphate-free AP1 medium for 12 days. The initial pH of AP1 medium was adjusted to pH 5.5 using 1 M HCl after autoclaving. All experiments were conducted at least in triplicate.
Determination of amino acid concentrations
One millimolar single amino acid (aspartic acid, glutamic acid, alanine, proline and cysteine, respectively) solutions and Dulbecco’s modified Eagle’s medium (DMEM) (Sigma-Aldrich, USA) were prepared separately as standards. Fifty microlitres of samples and standards was collected and analysed for the free amino acid concentration by high-performance liquid chromatography (HPLC) after derivatization. Protein was precipitated from each sample by adding 200 μl trifluoroacetic acid (TFA) and methanol solution (volume ratio = 1:10) and centrifuged at × 20,000g for 10 min. The free amino acids were then eluted and concentrated from sample supernatants by sodium acetate, methanol, triethanolamine (TEA) solution (volume ratio = 2∶2:1), methanol, MilliQ water, TEA, phenylisothiocyanate (PITC) solution (volume ratio = 7∶1:1∶1) and methanol. Samples were dried thoroughly between each step at 46 °C in a rotary evaporator, and resuspended in eluent buffer (95% solution of 10 mL/L TEA and 150 mM sodium acetate (pH = 6.4), and 5% acetonitrile) and separated using a Hewlett Packard 1050 HPLC system (Minneapolis, Minnesota, USA) with post-column UV detection (254 nm). Final results were analysed using Clarity Lite software, and all samples and standards were conducted at least in triplicate (Poncet et al. 2014).
Preparation of copper carbonate minerals
In this study, copper carbonate minerals synthesized in the different reaction systems were compared in order to characterize the role of amino acids in biomineralization. Copper carbonate minerals were prepared (1) from biomass-free fungal growth supernatants, (2) by chemical synthesis without the addition of amino acids as a control and (3) copper precipitates obtained by chemical synthesis with the addition of glutamic acid, aspartic acid and cysteine separately at different concentrations.
Copper carbonate nanoparticles produced in fungal growth supernatants
After 12 days growth, N. crassa growth supernatant was collected by centrifugation (× 4000g, 30 min). CuCl2 solution at a 20mM final concentration was added dropwise to the growth supernatant of N. crassa, and samples were placed on a roller shaker (60 rpm) overnight. Precipitated products were collected and washed twice with MilliQ water after centrifugation (× 10,000g, 30 min).
Copper carbonate minerals produced by chemical synthesis
Chemical synthesized copper carbonate minerals were used as a control and obtained by mixing 20 mM ammonium carbonate and 20 mM copper chloride solutions. In order to identify the impact of amino acids on copper carbonate formation, amino acids that were detected in fungal growth supernatants (glutamic acid, aspartic acid and cysteine) were also added into the chemical reaction mixture as additives to final concentrations of 0.2, 1 and 10 mM. The samples were mixed overnight on a roller shaker (60 rpm), and after collection, the minerals precipitated were examined by SEM, XRPD, FTIR and TGA to investigate the influence of amino acids on their nucleation, morphology and growth.
Characterization of copper carbonate minerals
Scanning electron microscopy and energy-dispersive X-ray analysis
Scanning electron microscopy (SEM) images were obtained by using a field emission scanning electron microscope (FESEM) (Jeol JSM7400F). Dry samples were sputter coated with 5 nm gold and platinum using a Cressington 208HR sputter coater (Ted Pella, Inc., Redding, CA, USA). The chemical compositions were analysed by an energy-dispersive X-ray spectrometer (EDXA) (Oxford Instruments, Inca, Abingdon, Oxfordshire, UK). The particle size distribution histograms of nanoparticles were calculated by measuring 150 random particles using Nano Measurer 1.2.5. software.
X-ray powder diffraction analysis
X-ray powder diffraction (XRPD) patterns were obtained with Cu-Kα radiation using a Panalytical X-pert Pro diffractometer. The measurements were made using a step-scanning program with 0.02° per step in the range from 0 to 100°. XRPD data were analysed by reference to patterns in the International Centre for Diffraction Data Powder Diffraction File (PDF) for identification of the crystalline phases.
Attenuated total reflectance Fourier-transform infrared spectroscopy
The attenuated total reflectance Fourier-transform infrared (ATR-FTIR) spectra of samples in the form of powders were obtained using a Bruker Vertex 70 FTIR spectrometer. All spectra were measured in the wavelength range from 400 to 4000 cm−1, with a 4 cm−1 spectral resolution.
X-ray photoelectron spectroscopy
X-ray photoelectron spectroscopy (XPS) was performed using a Scienta ESCA-300 instrument (Scienta AB, Uppsala, Sweden) fitted with a non-monochromatic Al-Kα X-ray source. The survey (wide) spectra was collected from 1200 to 0 eV with a step size of 0.2 eV, and more detailed scans for elements C, O, N and Cu were performed over the regions of interest. CasaXPS software was used to analyse the XPS spectra core-level lines for curve fitting. All spectra were referenced to the O 1s peak of carbonate at 530.9 eV.
Thermodynamic modelling by Geochemist’s Workbench (GWB)
Log K is referred to stability constant of the complexes. All thermodynamic modelling was conducted at ambient temperature (25 °C).
Thermogravimetric analysis (TGA) was used to assess the thermal stabilities of the copper minerals produced in the presence of amino acids using a Shimadzu TGA 50. About 50 mg mineral samples were heated from 20 to 1000 °C at a uniform nitrogen flow rate of 100 ml min−1. The chemical components of the final products after thermal decomposition were analysed by XRPD.
Characterization of copper carbonate minerals
Energy-dispersive X-ray analysis (EDXA) results showed that the main elements in the biomineral product were carbon, oxygen and copper. However, the XRPD pattern of the biominerals did not show any characteristic sharp peaks but only a broad peak which indicated the biominerals were amorphous without long-range atomic order (Fig. S1). Unlike the biominerals produced by reaction with the fungal growth supernatants, the chemical component of the inorganically synthesized copper mineral was determined as malachite (Cu2(OH)2CO3), as high-intensity peaks occurred at 15°, 18°, 24°, 31° and 36° corresponding respectively to the (020), (120), (220), (− 201) and (240) faces of the malachite crystals (Süsse 1967).
Determination of fungal extracellular amino acid secretion
Effect of amino acids on the formation of copper carbonate minerals
FTIR spectral analysis
FTIR data of copper complexes produced in the presence of 10 mM aspartic acid (Cu-asp) and 10 mM cysteine (Cu-cys), respectively
(Navarrete et al. 1994)
(Pawlukojć et al. 2005)
X-ray photoelectron spectroscopy
Speciation modelling using Geochemist’s Workbench
Thermal stability analysis
XRPD analysis of the final products after thermal decomposition (Fig. S5) showed that different copper-bearing minerals resulted. For the inorganic control, cuprite (Cu2O) was produced. The biominerals, the sample with 10 mM glutamic acid and 10 mM aspartic acid showed the production of metallic copper after TG analysis. It is therefore suggested that the copper carbonate minerals containing organic material were more easily reduced to metallic copper compared to the inorganic controls, and they may also possess less thermal stability. TGA of the samples produced with 10 mM cysteine gave pure phase chalcocite (Cu2S).
The copper carbonate nanoparticles formed by a fungal-mediated biomineralization reaction showed an amorphous powder form without any clear crystallinity, and this result was also consistent with XRPD data as no distinguishable peaks in XRPD patterns were observed for the amorphous minerals in the absence of any ordered atomic structure. Although the GWB modelling and FTIR results suggested that basic copper carbonate, malachite (Cu2(OH)2CO3), was formed under the experimental conditions, the presence of amino acids and other organic molecules secreted from fungi can affect the purity and valence state of the Cu mineral. The Cu2p3/2 XPS bands appeared at around 932 eV which was assigned to either Cu(I) or Cu(0) species, indicating the reductive Cu species formed via some complex-forming reactions inside the structure of the copper carbonate minerals. Our XPS results further suggested the Cu complexes were formed by bonding the N atoms of organic molecules with the Cu species (Cu-N) on the mineral surface. Liu et al. (2016) studied the reaction of a novel organic surfactant HATT (which has amino and thione functional groups) with malachite, and showed that HATT was associated with malachite by the formation of Cu-N and Cu-S surface complexes. It is not unusual that Cu(II) can be reduced to Cu(I) and form Cu(I) and/or Cu(II) complexes with amino acids, e.g. glycine (Cedzynska et al. 1981) and cysteine (Rigo et al. 2004). Redox reactions of Cu are also involved in many enzymatic processes, for example the functions of copper chaperone and copper transport proteins (Valentine and Gralla 2002). Some previous studies showed that cysteine and tyrosine residues played a key role in the reduction of Cu(II) to Cu(I) by some copper-binding proteins (Opazo et al. 2003).
The copper carbonate precipitated in the presence of various concentrations of different amino acids showed different morphologies compared with abiotically synthesized copper carbonate particles produced from mixture of 20 mM (NH4)2CO3 and 20 mM CuCl2. The mean size of the inorganic control copper carbonate particles in the absence of any additives was ~ 130 nm in diameter after 1 h reaction time, and these crystals aggregated together to form microscale particles after 12 h. Nanoparticles have a high surface area to volume ratio, and the total free energy of nanoparticles tends to decrease on reducing the interfacial area to maintain the stability of the system. This usually results in particle agglomeration or recrystallization. One of the most remarkable features of these minerals was the uniformity of the nanocrystals within the aggregates which all had the same morphology and size, and this suggested that the nanoparticles nucleated simultaneously and grew at the same rate before aggregation (Kwon and Hyeon 2008). When various amino acids were added into the chemical reaction of copper carbonate, the incorporation of amino acids within the mineral structure was confirmed by FTIR analysis. Among all the amino acids tested, the reaction with 10 mM glutamic acid produced the smallest sized particles, and these particles were stabilized in the early phase of crystal growth and prevented from aggregation with only 1 mM glutamic acid. It is reported that the point of zero charge (pzc) of malachite is around pH 7.6, and malachite also has a high positive charge, ~ 20 mV on the surface at a neutral pH (Saha and Das 2009). Therefore, it can be concluded that the negatively charged amine group side chain of glutamic acid showed a high affinity for binding to positive mineral surfaces (Wang et al. 2015; Wolthers et al. 2008; Zare et al. 2013). Whether particles stay dispersed or aggregated in a system is controlled by repulsive and attractive forces between particles, for example, gravity, electrical charge and van der Waals forces (Adamczyk and Weroński 1999). It is therefore suggested that the Glu-associated particles with a negatively charged surface would have a stronger repulsive force than an attractive force which would make the particles more dispersible and also inhibit their further growth. The mean size of particles synthesized in the presence of 10 mM Glu was ~ 130 nm in diameter, which was smaller than those produced in the presence of 1 mM Glu (mean diameter ~ 160 nm). It is suggested an increasing concentration of the added amino acid can decrease the activation energy for nucleation, increase the rate of nucleation and decrease the size of the crystals (Mann 2001).
For acidic amino acids like aspartic acid, it was found that these amino acids resulted in the formation of rod-like crystals. Long fibrous crystals were also observed in the samples with 10 mM cysteine. Peptides and amino acids can interact with divalent transition metals, and form ‘complexes’ that have received significant attention, especially the copper complexes of amino acids (Kryukova et al. 2005). The synthesis of such complexes via complexation and chelation also highlights the possibility of artificial mimics of metal-containing enzymes for use as catalysts. Previous work reported using the copper-cysteine complexes to enhance photocatalytic H2 production by 150 times compared with CdSe catalyst (Peng et al. 2015). In our reaction system, as shown by the GWB modelling results, the amino and carboxylate groups of aspartic acid and cysteine can chelate copper ions preferentially compared with carbonate ions, which will further prevent the formation of copper carbonate minerals (Sóvágó et al. 2012). The oriented nucleation and growth of minerals, which enhanced growth in specific directions but limited growth rates in other directions, resulted in formation of minerals with rod-like or fibrous structure. The formation of Cu2S from thermolysis of Cu-cysteine complexes confirmed the breakup of thiol group and formation of Cu-S bonding, which can shed some light on the production of copper sulphide with impressive electrocatalytic properties (Choi et al. 2009).
Biominerals that exist in natural and synthetic environments show a variety of morphologies and structures, but the effect of small biomolecules, such as amino acids, on the biomineralization process remains poorly understood. This work demonstrates the extracellular production of well-dispersed copper nanoparticles by using biomass-free urea-grown Neurospora crassa growth supernatants. The nanoparticles exhibited a spherical morphology with a mean diameter around 25 nm, which was much lower than inorganically synthesized particles or particles produced solely in the presence of amino acids. Eleven different amino acids were secreted by Neurospora crassa, and among these, glutamic acid was found to stabilize the particles in the early phase of growth and prevented them from aggregating, even at a low concentration (1 mM). FTIR revealed the molecular interaction of amino acids and copper minerals, confirming the association of organic substances secreted by the fungus into the mineral structure. Thermal treatment of copper carbonate biominerals also suggested a facile method for producing Cu, Cu2O and Cu2S mineral products. Overall, this work provides further understanding of the potential application of fungal system for nanoparticle synthesis, the significance of amino acids in microbially induced carbonate biomineralization and possible means of controlling particle size and aggregation, and the further production of useful metal and biomineral products.
Financial support in the author’s laboratory is received from the Natural Environment Research Council (NE/M010910/1 (TeaSe); NE/M011275/1 (COG3)) which is gratefully acknowledged. We also acknowledge financial support from the China Scholarship Council through a PhD scholarship to F.L. (No. 201609110150). The authors gratefully appreciate the help of Dr. Yongchang Fan (Materials and Photonics Systems Group, University of Dundee, Dundee, UK) for assistance with scanning electron microscopy, Dr. Paul F. Schofield (Department of Mineralogy, Natural History Museum, London, UK) for assistance with X-ray powder diffraction, Dr. Peter Taylor (School of Life Sciences, University of Dundee, Dundee, UK) for assistance with high-performance liquid chromatography, and Dr. Steve M. Francis (School of Chemistry, University of St Andrews, St Andrews, UK) for assistance with X-ray photoelectron spectroscopy as well as Dr. Jean Robertson (The James Hutton Institute, Aberdeen, UK) for assistance with Fourier-transform infrared spectroscopy.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
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