Abstract
Trichoderma harzianum (T. harzianum) was isolated from uranium mill tailing soils, and a cold atmospheric plasma jet as a mutational method was applied for the treatment of T. harzianum to improve its performance of U(VI) biosorption. The effects of pH, adsorption time and biosorbent doses were performed on the biosorption of U(VI) by T. harzianum and mutated T. harzianum at different environmental conditions. The maximum adsorbability for U(VI) on mutated T. harzianum was 83.59 mg/g at 303 K and pH 6.0, which was observably better than the raw T. harzianum. FTIR analysis indicated that the functional groups on the surface of mutated T. harzianum interacting with U(VI) were primarily hydroxyl, amino and carboxyl groups. SEM coupled with EDX analysis demonstrated that U(VI) can be adsorbed to mutated T. harzianum, and the surface of mutated T. harzianum became rough and incompact after the biosorption. This study showed that the mutated T. harzianum could be considered as a highly effective biosorbent for removal of U(VI) from radioactive wastewater.
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Introduction
Uranium, a scarce strategic resource in large demand, is massively exploited and widely used for nuclear power production [1]. However, with the development of the nuclear energy industries, large amounts of uranium-containing radioactivity wastewater were generated and leaked into adjacent soils and groundwater [2]. Due to the radioactivity and chemical toxicity of uranium, the free uranium(VI) (U(VI)) ions leaking into the environment will cause severe damage to human health and ecological environment [3]. Consequently, it is urgent to develop environment-friendly and efficient technologies to eliminate U(VI) from aqueous solution.
There are numerous treatment techniques for removing radionuclides from environment, including chemical precipitation, ion exchange, adsorption, extraction and so on [4,5,6]. Compared with traditional chemical treatment techniques, microbial bioremediation is gaining more and more attention, considering its high removal efficiency, low operation cost and no secondary pollution. Recent researches have revealed that different kinds of living microorganisms, such as bacteria [7, 8], fungi [9,10,11] and algae [12,13,14] have been used as biosorbents for binding U(VI) from aqueous solutions. Among them, filamentous fungi, such as Rhizopus, Penicillium and Aspergillus, have been proved to be promising biosorbents with favorable advantages for effective removal of uranium from radioactive wastewater [15,16,17]. In order to enhance the biosorption performance of microorganisms, various kinds of mutation strategies have been extensively applied [18,19,20]. Sun et al. used Hydroxylamine hydrochloride and UV light to mutate Penicillium funiculosum, and biosorption capacity of U(VI) on mutated P. funiculosum increased obviously [21]. Moreover, Song et al. employed dielectric barrier discharge plasma to alter the DNA of Aspergillus oryzae for more effective mutants with improved bioremediation properties [22].
A cold atmospheric plasma jet (CAPJ) could produce reactive species, which is composed of an excited state of free radicals, ions, electrons, and reactive oxygen and nitrogen species [23]. In addition, CAPJ is a relatively soft ionization technology with higher ionization efficiency of low molecular weight compounds [24], and can induce DNA change in the cells, which indicates that CAPJ is an excellent technique to mutate microbes due to its high mutation rate, simple operation, low cost and shorter reaction time [25]. In fact, CAPJ has been successfully employed to mutate Haematococcus pluvialis [26], Cladosporium sphaerospermum [27], Rhodosporidium toruloides [20] and Ganoderma lingzhi [28].
In the present study, T. harzianum was isolated from the uranium mill tailing and its morphological characteristics were studied in details. In order to enhance U(VI) biosorption properties, CAPJ was conducted to mutate T. harzianum strain. Then, U(VI) biosorption characteristics of T. harzianum and mutated T. harzianum were invesigated in different environmental conditions, and possible biosorption mechanisms of mutated T. harzianum were explored by scanning electron microscopy (SEM) with Energy Dispersive X-Ray Spectroscopy (EDX), and Fourier Transform infrared spectroscopy (FTIR).
Materials and methods
Strain isolation and identification
The uranium contaminated soils were collected from a uranium mill tailing located in southern China, and the U(VI)-tolerance strains were isolated through standard dilution-plate method [29] in potato dextrose agar (PDA) plates which contained different concentrations of U(VI). The inoculated plates were incubated at 28 °C for 72 h. Then, the fungal isolates that could tolerate the highest U(VI) concentration were selected for purification and kept on fresh PDA plates. The pure fungal strain was identified by macroscopic characteristics using Olympus IX71 inverted fluorescence microscope (Olympus, Tokyo, Japan) and microscopic characteristics using molecular identification. Amplification of ITS region gene sequences was performed according to the previously method [30]. The purified product was followed by DNA sequencing (Sangon, Shanghai), and afterwards the sequence was analyzed with the BlastN search program in the NCBI GenBank database (http://blast.ncbi.nlm.nih.gov/). Then, the molecular phylogenetic analysis of the isolate was performed based on the ITS region gene sequence analysis.
Mutagenesis of the fungus
The CAPJ plasma for this work was schematically showed in Fig. 1a. The reactor chamber has 2 parallel copper electrodes with a distance of 60 mm. Helium (99.997% purity) gas was applied as the plasma working gas with its flow rate 900 mL/min, which was injected 2 min before the experiment to force air out from the reactor compartment. Spores of T. harzianum were collected from the mid-growth phase and diluted to 106–107/mL. Then the spore suspension was dripped onto sterilized plates and treated with CAPJ treatment for 3 min. After the CAPJ treatment, mutagenized spores were placed on the PDA solid medium and cultured for 3 days at 28 °C. Many survival single colonies with various morphologies were observed. Finaly, the high-growth-rate strain was selected and cultured for biosorption experiments.
Biomass preparation
Trichoderma harzianum and mutated T. Harzianum were used as adsorbents to remove U(VI) in this study. T. harzianum and mutated T. Harzianum were cultivated separately in the Erlenmeyer flasks (250 mL) containing 150 mL of PDA medium at 28 °C and agitated at 150 rpm. After 3 days of incubation, the fermentation broth was filtrated for the mycelia, and the mycelia was washed twice with distilled water and then freeze-dried for 24 h. Then, fungal biomass was stored separately in an amber bottle at a temperature of 4 °C until used for adsorption studies.
Characterization studies of biomass
The surface morphology and elemental composition of the mutated T. harzianum before and after loading of U(VI) were characterized by SEM coupled with EDX. For this purpose, The mycelia of mutated T. harzianum before and after loading of U(VI) were collected and washed three times with sterilized water. About 10 mg of the samples were solidified with 2.5% glutaraldehyde and then 1.0% osmic acid at room temperature for 1 h. After that, Samples were then dehydrated through a graded ethanol series, finally critical-point-dried, coated with gold and examined using a SEM (JEOL JSM-6330F, Japan) coupled with EDX (Oxford) system at 200 kV [31]. Infrared spectra of U(VI)-free and U(VI)-loaded mycelia prepared as KBr discs were recorded over the region 400–4000 cm−1 using a Perkin Elmer Spectrum 100 spectrophotometer (Waltham, MA, USA). Besides, The zeta potential of T. harzianum and mutated T. harzianum were investigated by an automatic titrator system (DL58, Mettler Toledo, Germany) at different pH values.
Biosorption experiments
In a general procedure, 0.05 g of uranium nitrate (UO2(NO3)2·6H2O) was dissolved in 0.1 L deionized water to obtain a stock solution (500 mg/L). The stock solution was diluted to an appropriate concentration for experiments. All the biosorption experiments on T. harzianum and mutated T. harzianum were operated under ambient conditions. To investigate the influence of pH and concentrations of biosorbent on biosorption of U(VI) by T. harzianum and mutated T. harzianum, different conditions of pH (2–11) and concentrations of biosorbent (0.05–0.7 g/L) were performed by batch experiments. Afterwards, the suspensions were shocked at 150 rpm for 24 h to achieve biosorption equilibrium, and the solution was centrifuged at 8000 rpm for 10 min. The concentration of residual U(VI) was determined by a Packard 3100 TR/AB Liquid Scintillation Analyzer (Perkin-Elmer). All the experiments were conducted in triplicate. The removal efficiency (Removal, %) and Adsorption capacity (Qe, mg/g) were determined by the following formulae:
where C0 (mg/L) is the initial U(VI) concentration; Ce (mg/L) represents equilibrium U(VI) concentration; V (mL) is the volume of the suspension and m (g) is the weight of fungal mycelia.
Results and discussion
Strain identification
The fungal isolate showed similar features to T. harzianum species, such as rapid growth of colony, with dense conidiation, turning dark green after 5 days as shown in Fig. 1b, and abundant sporulation with spherical smooth conidia was arranged in clusters (Fig. 1c). Besides, the length of detected ITS gene sequence from the fungal isolate was approximately 591 bp, and phylogenetic relationships on the basis of ITS gene sequences were created in Fig. 2. The fungal isolate showed 99% sequence similarity to sequences of T. harzianum strain JZY4 (MT786378.1) and T. harzianum strain NZD-mf15 (KM278121.1). Combining with external morphological features and DNA identification, the fungal isolate was identified as T. harzianum.
Effect of pH
The effect of the initial pH on the adsorption efficiency of U(VI) onto the T. harzianum and mutated T. harzianum biomass was presented in Fig. 3a. The adsorption rate increased obviously from pH 2.0 to 6.0, and achieved its maximum value at pH 6.0, above which it gradually reduced, which was consistent with the earlier study [32, 33]. From Fig. 3a, the highest removal efficiency of U(VI) onto mutated T. harzianum was about 90% at pH 6.0, which was approximately 10% more than that of T. harzianum. Earlier studies showed that modifications in pH could bring about changes in net charge of the mycelia surface but also changed the U(VI) species in the solution [34, 35]. The reason for this change trend of the adsorption rate may be due to a variation in the presence status of uranium. At low pH, uranium existed as the form of UO22+ in solution, and H+ occupied the active binding sites thus the uranium removal efficiency was very low [36]. As pH value increased, the UO22+ gradually hydrolyzed to (UO2)2(OH)22+, (UO2)3(OH)5+ and UO2OH+ [37], which bound more easily with active sites than H+, and the mycelia surface carried with negative charges; therefore, the mycelia could adsorb more uranium ions [38]. However, when pH is over 6.0, hydrolyzed species of uranium and the zero point of charge (Fig. 5b) may lead to the decline of sorption efficiency of uranium [39, 40].
Effect of biosorbent dosage
The effect of biosorbent dosage on adsorption of U(VI) onto the T. harzianum and mutated T. harzianum adsorption was evaluated by varying biosorbent dosage from 0.05 g/L to 0.7 g/L (Fig. 3b). It showed that the removal efficiency of U(VI) increased from 42 to 85% and 50 to 88% for T. harzianum and mutated T. harzianum, respectively, when biomass dosage was increased from 0.05 to 0.5 g/L, while the distribution coefficient (Kd) for T. harzianum and mutated T. harzianum was decreased, respectively. This indicated that the number of the binding sites for uranium (VI) increased with the increase of the biosorbent dosage in the range of 0.05–0.5 g/L [41]. However, when the biosorbent dosage was more than 0.5 g/L, the biosorption rate of uranium (VI) from the solution was almost constant, and Kd for T. harzianum and mutated T. harzianum almost did not change. It may be attributed to the fact that higher biosorbent dosage could produce aggregation and competition among biosorbent particles, which reduces the effective binding sites of functional groups at the surface of mycelia [42]. Therefore, 0.5 g/L of biosorbent was used in subsequent U(VI) biosorption experiments.
Effect of adsorption time
Figure 4a revealed the effect of adsorption time on the biosorption of U(VI) onto the T. harzianum and mutated T. harzianum biomass. The rate of U(VI) adsorption on the T. harzianum and mutated T. harzianum biomass increased rapidly within 4 h, and then achieved dynamic sorption equilibrium at approximately 10 h, whereas the biosorption rate slightly became slow with the increase of adsorption time. The data of biosorption kinetics was analyzed using pseudo-first-order and pseudo-second-order kinetic. The calculation equations of these two kinetic models are given by Eqs. (3)–(4):
where Qt (mg/g) and Qe represent the amounts of U(VI) adsorbed at time (t) and at equilibrium, respectively; k1 (h−1) and k2 (g/(mg h)) are the adsorption rate constants of the pseudo-first-order and pseudo-second-order models, respectively. The fitting results and relevant parameters were listed in Table 1, respectively. Evidently, the biosorption kinetics of U(VI) on the T. harzianum and mutated T. harzianum were successfully described by the pseudo-second-order model (R2 > 0.999), which indicated that the biosorption process was primarily controlled by chemical adsorption or ion exchange.
Adsorption isotherms
U(VI) adsorption isotherms of T. harzianum and mutated T. harzianum were shown in Fig. 4b. The amounts of U(VI) adsorption on T. harzianum and mutated T. harzianum enhanced dramatically with the increase of U(VI) concentration at pH 6.0 and 303 K. The experimental data of U(VI) adsorption were fitted with the Langmuir and Freundlich models to estimate the sorption capacity [43]. The calculation equations of these two isotherm models are as follows:
where Ce (mg/L), the equilibrium concentration; Qe (mg/g), the equilibrium biosorption capacity; Qm (mg/g), the maximum monolayer adsorption capacity; KL, KF and n are the model constants of Freundlich and Langmuir, respectively.
The linearized form of Freundlich and Langmuir fitting isotherms were listed in Fig. 4b, and the calculated parameters were presented in Table 2. The Langmuir isotherm models of T. harzianum and mutated T. harzianum fitted better to the experimental data since their R2 values were 0.989 and 0.993, respectively, which were higher than that of Freundlich model, suggesting that adsorption behavior of U(VI) onto T. harzianum and mutated T. harzianum cell surface may be a monolayer adsorption process. Similarly, uranium removal process by calcium alginate immobilized Yarrowia lipolytica powder beads was also shown to conform to Langmuir model [41]. As listed in Table 3, the maximum U(VI) sorption amount of mutated T. harzianum estimated from the Langmuir model was about 83.59 mg/g at 303 K and pH 6.0, which has higher Qmax for U(VI) sorption than other sorbents, such as Rhodotorula glutinis [34], Streptomyces sporoverrucosus [10], and immobilized Aspergillus fumigatus beads [14]. Therefore, mutated T. harzianum could be used as a promising biomaterial for removal of uranium from radioactive wastewater.
Biosorption mechanisms
In order to elucidate the active functional groups which participated in the mutated T. harzianum mycelia binding with uranium ions, FTIR spectra analyses were performed for control (U(VI)-free) and U(VI)-loaded mycelia between 4000 and 400 cm−1. FTIR spectra of mutated T. harzianum without U(VI) and with U(VI) were presented in Fig. 5a. The results indicated that a distinct absorption peak at 3410–3460 cm−1 (O–H stretching vibration) was strengthened after adsorption, which indicated that –OH or –NH emerged on the mycelia surface combine with U(VI) ions through hydrogen binding [45, 46]. In addition, the peak at 2927 cm−1, which may link with –CH asymmetric stretching vibrations, shifts to 2920 cm−1 after exposure to U(VI), indicating that the role of –CH groups in U(VI) binding. Moreover, The peaks at 1645 and 1432 cm−1 (C=O stretching vibration) also exhibit minor changes, which is possibly due to the complexing of the –C=O groups with U(VI) [47]. In summary, FTIR analysis revealed that the hydroxyl, amino and carboxyl groups of mutated T. harzianum cell wall played a significant role in the fungus U(VI) interaction.
SEM combined with EDX analyses was also used in order to understand mechanism of U(VI)-fungus interactions. The morphological change of mutated T. harzianum before (a), and after loading of U(VI) (b) were shown in Fig. 6. It can be seen that granular protrusions can be obviously observed on the SEM micrographs of the U(VI)-loaded mycelia as compared with the sample without loaded U(VI). The SEM images also demonstrated that U(VI)-loaded mutated T. harzianum changed their extracellular structure. On the basis of SEM observation, the place where there were attachments on the surface of the mycelium was selected for EDX analysis (the point indicated by the red arrow in Fig. 6c, d). The EDX chart originated from electron-dense bodies appeared the characteristic peak of uranium which ascertained the presence of U(VI) on the external surface of mutated T. harzianum, and carbon, phosphorus, oxygen and sodium were also found in the EDX chart. Therefore, it could be inferred that the surface of the mutated T. harzianum mycelium had a strong capacity to adsorb U(VI). Some literature reports also had shown similar mechanisms which the adsorbed U(VI) mainly occurred on the hyphal cell surfaces [17, 48]. Especially, the characteristic peak of phosphorus was found in EDX images, and it could be inferred that the precipitates of mycelium surface maybe a form of uranyl phosphates [49].
Based on the above analyses, the possible biosorption mechanism of U(VI) by mutated T. harzianum have been proposed. Firstly, U(VI) was attached on the hyphal cell surfaces. This behavior primarily due to the electrostatic interactions between U(VI) and high affinity sites of the fungal cell envelope. Meanwhile, The hyphal cell surfaces was covered with a lot of active functional groups, including hydroxyl, amino and carboxyl, which were also played a significant role in the fungus U(VI) interaction. Then under the stimulation of U(VI), the mutated T. harzianum released phosphate from cells by metabolism-dependent process. Therefore, U(VI) gradually form uranyl phosphates precipitates with released phosphate on the hyphal cell surfaces. However, the biosorption of U(VI) by T. harzianum is a complicated interaction process, and biosorption mechanism of U(VI) using T. harzianum and mutated T. harzianum still need to be further studied.
Conclusions
In this study, a resistant fungal strain for uranium adsorption was isolated from the uranium mill tailing soils. According to the morphology and the phylogenetic analysis based on ITS gene sequencing fragment (99% similarity to T. harzianum), it was identified synthetically as T. harzianum. T. harzianum was mutated by CAPJ to enhance U(VI) adsorption capacity. The mutated T. harzianum presented higher potential for U(VI) adsorption investigated by batch adsoption experiments. The experimental data better conformed to Langmuir model, and its maximum adsorbability for U(VI) was estimated to be 83.59 mg/g at pH 6.0 and 303 K. FTIR analysis indicated that U(VI) adhered to hydroxyl, amino and carboxyl groups in the mycelia cell wall of mutated T. harzianum. SEM coupled with EDX analysis demonstrated that U(VI) attached onto the surface of the mycelia. Therefore, the mutated T. harzianum could be considered as a highly effective sorbent for removal of uranium from radioactive wastewater.
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Acknowledgements
This research was supported by National Natural Science Foundation of China (22006001 and 21876179), the Key Project of Natural Scientific Research of Universities in Anhui Province (KJ2019A0914) and University Outstanding Young Scientific Research Talent Cultivation Program Project in Anhui Province (gxyq2020091).
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Liang, J., Liu, L. & Song, W. Enhancement of U(VI) biosorption by Trichoderma harzianum mutant obtained by a cold atmospheric plasma jet. J Radioanal Nucl Chem 327, 1325–1333 (2021). https://doi.org/10.1007/s10967-021-07615-0
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DOI: https://doi.org/10.1007/s10967-021-07615-0