Abstract
To increase the bioaccumulation of Eu(III), low temperature plasma as a method of mutagenesis was introduced to mutate Cladosporium sphaerospermum (C. sphaerospermum). Mycelia doses, pH, and ionic strength obviously affected the Eu(III) immobilization on mycelia. The maximum immobilization capacities of Eu(III) on mutated C. sphaerospermum was 278.8 mg/g at pH 6.5, which was approximately three times than that of raw C. sphaerospermum. Before and after Eu(III) loaded mycelia were analyzed by XPS and FTIR, and intracellular structures of mycelia changed obviously under Eu(III) stress by TEM analysis. The results suggested that low temperature plasma could be utilized as a valuable treatment technology to improve fungi for the removal and immobilization of radionuclides in the environment.
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Introduction
Long-lived radionuclides posed serious threats to biological systems and human health due to its potential toxic and carcinogenic effects [1]. Europium (Eu(III)), one of the fission products of uranium, was often used as a chemical analogue for trivalent lanthanides/actinides in removal studies because of their comparable physicochemical properties and similar environmental behaviors [2,3,4]. Therefore, developing cost-effective and environment-friendly materials to remove Eu(III) from environments are of particular importance. There are lots of materials for Eu(III) removal, such as carbon materials [5,6,7,8,9], metal oxides [10,11,12] and clay minerals [13,14,15]. However, removal of radionuclides or heavy metal by microorganisms has been demonstrated to be more environmentally friendly and cheaper than chemical and physical materials, especially in the aspect of stimulating indigenous microbial communities [16]. Among microorganisms, fungi have advantages over bacteria for the bioremediation of contaminated sites owing to its mycelia network, biomass and longer life-cycle [17]. Moreover, radionuclides or metals tolerant fungi can compete with the native bacteria in hostile situations and have developed different strategies to protect themselves from oxidative stress caused by radionuclides or metals [18,19,20]. However, as far as we know studies about Eu(III) immobilization on fungi were still little [16].
Low temperature plasma (LTP) generated free electrons and ions, radicals and a variety of radiation ranging from UV via visible to infrared [21]. Research showed that LTP treatment could lead to intensively microbial DNA change, suggesting that LTP was expected to be used for microbial mutagenesis [22]. Therefore, LTP was successfully applied in many microbial mutagenesis [23,24,25,26].
LTP as a method of mutagenesis was introduced to mutate Cladosporium sphaerospermum (C. sphaerospermum) in order to improve 152+154Eu(III) immobilization. Eu(III) immobilization on mutated C. sphaerospermum was studied in different environmental conditions, and characterization of Eu(III) immobilization on mycelia was investigated by X-ray photoelectron spectroscopy (XPS), Fourier transform infrared spectroscopy (FTIR), and transmission electron microscopy (TEM). This study will better understand the Eu(III) immobilization mechanism on fungi and improve the bioremediation strategies of Eu(III) pollution.
Materials and methods
Cultivation of resistant fungus
Resistant fungus used in this study was isolated from radionuclide-contaminated soils, and the method of isolation and identification had been shown in previous study [16]. Cultivation of the fungus was carried out in 250 ml Erlenmeyer flasks with 100 ml potato dextrose agar (PDA) medium on a rotary shaker at 200 rpm and 28 °C. After 3 days’ cultivation, mycelia were harvested by centrifugation, washed three times in deionized water and stored at 4 °C for batch experiments. Besides, mycelia were trapped under glass using laetophcnol cotton lalue stain before being examined, and observed under an Olympus IX71 inverted fluorescence microscope (Olympus, Tokyo, Japan). All images were captured using a TH4-200 photo system (Olympus, Tokyo, Japan) at ×200 magnification.
Characterization of fungal mycelia
Fungus was incubated in PDA medium containing 0 or 200 mg/l Eu(III) at 28 °C and 200 rpm for 3 days. The samples for TEM were fixed in 5% glutaraldehyde for 3 h, then post-fixed in 1.0% osmium tetraoxide for 2 h and dehydrated in a graded ethanol series (50–100%) as previously described by El-Sayed [27]. The blocks were sectioned, stained and observed using a TEM with an energy dispersive X-ray analysis (EDS) (Hitachi HT-7700, Japan). The method of XPS (Thermo ESCALAB 250, USA), and FTIR (Perkin Elmer 100, USA) referred to related literature [16].
Eu(III) immobilization by mycelia
Immobilization of Eu(III) by mycelia was studied under ambient conditions. The different concentrations of mycelia suspensions, Eu(III) and NaCl solution were added into Erlenmeyer flasks, and pH of the solution was regulated to 6.5. After immobilization equilibrium, the solution was centrifuged at 8000 rpm for 10 min, and 152+154Eu(III) concentration was analyzed by Liquid Scintillation counting (Packard 3100 TR/AB Liquid Scintillation analyzer, Perkin-Elmer) with the scintillation cocktail (ULTIMA GOLD ABTM, Packard). The immobilization percentage and amounts of Eu(III) immobilization capacity (Q, mg/g) were described as Eqs. (1) and (2):
where C0 and Ce (mg/l) were initial and equilibrium concentrations, respectively. V and m were volume of suspension and the mass of mycelia, respectively. All tests were conducted in triplicate.
Results and discussion
Isolate mutagenesis experiments
The LTP plasma was schematically illustrated in Fig. 1a, which was described in previous studies [28,29,30]. The reactor chamber has three poles, one air inlet and one air outlet. In the experiment, we used helium (99.99% pure) gas as work gas which flow rates was 80 l/h and injected 3 min before the experiment to expel air as much as possible from reactor chamber. Spores were collected, and diluted spore samples were mutated by LTP for 6 min. LTP was generated by voltage of 30 V and power of 42 W. Then, mutated spores were inoculated onto PDA petriplates containing Eu(III). Then, the best mutant isolate was selected from morphology and cultured for immobilization experiments.
Identification of the isolate
The length of ITS sequence of the isolate was approximately 526 bp. It showed 99% similarity with C. sphaerospermum in GenBank (KJ191437.1 and HG530663.1). Combining with external morphological features as shown in Fig. 1b, the isolate was identified as C. sphaerospermum.
Effect of time
The amount of Eu(III) immobilization on C. sphaerospermum increased linearly with time during the first 24 h, and then remained almost constant within 84 h (Fig. 2a). The initial observed immobilization rate of Eu(III) on mycelia was very fast, whereas it became slow in the second phase, which was in accordance with the previously Eu(III) immobilization study [12]. That was because at initial stages of the immobilization, the higher concentration of Eu(III) provided the driving force to facilitate Eu(III) diffusion from solution to the active sites of mycelia. As the process continued, the decrease of Eu(III) concentration and the active sites of mycelia resulted in the decrease in Eu(III) immobilization [31]. Data points were fitted better with the pseudo-second-order kinetic model as compared to pseudo-first-order kinetic model, and kinetic parameters and equations from both models were listed in Table 1. The results of kinetics indicated that C. sphaerospermum possessed high immobilization efficiency for Eu(III).
Effect of pH
Several factors caused changes in Eu(III) accumulation as pH levels were modified. For example, Eu(III) species changed with the increase of pH (Fig. 2b). Besides, changes in pH could produce modifications in the surface net charge of mycelia. The immobilization Eu(III) on C. sphaerospermum and mutated C. sphaerospermum increased obviously as pH increased between 2.0 and 7.0, and maintained high level at pH > 7.0 (Fig. 3a). About 80% Eu(III) accumulated on mutated C. sphaerospermum at pH 6.5, which was about 30% more than that of C. sphaerospermum. The electrostatic interaction between mutated C. sphaerospermum and Eu(III) resulted in lower immobilization at pH < 7.0. Higher immobilization of Eu(III) at pH > 7.0 could belong to electrostatic attraction between Eu(III) and mycelia as well as the precipitates of Eu(OH)3 [32].
Effect of mycelia doses
The influence of mycelia doses on capacity of mutated C. sphaerospermum immobilization Eu(III) from aqueous solution was studied by using different fungal doses in the range of 0.05–0.7 g/l (Fig. 3b). The immobilization of Eu(III) rapidly rised with the increase of mutated C. sphaerospermum doses. It’s because more available sites for immobilization as well as greater surface area for immobilization ascended with the increase of mutated C. sphaerospermum doses. Oppositely, Kd reduced with the increase of mutated C. sphaerospermum doses, because the aggregation of fungal mycelia and competition among fungal mycelia reduced effective enrichment sites on mutated C. sphaerospermum [33].
Effect of ionic strength
The immobilization of Eu(III) on mycelia as a function of NaCl strength was shown in Fig. 4a. Eu(III) immobilization onto C. sphaerospermum and mutated C. sphaerospermum percent decreased with the increase of NaCl strength. The immobilization percent of Eu(III) on C. sphaerospermum and mutated C. sphaerospermum decreased 20 and 11% from 0.01 to 0.05 mol/l NaCl, respectively. That might be ascribed to the decrease of competing NaCl strength led to the formation of electrical double layer complexes, which favored the accumulation of Eu(III) on mycelia. The phenomenon was indicative of an ion exchange mechanism. On the other hand, NaCl strength of solution influenced the activity coefficient of Eu(III), which limited their transfer to mycelia [34].
Immobilization isotherms
Eu(III) immobilization isotherms of C. sphaerospermum and mutated C. sphaerospermum were illustrated in Fig. 4b. At pH 6.5 and 295 K, the increase of Eu(III) immobilization on C. sphaerospermum and mutated C. sphaerospermum was observed distinctly with the increase of Eu(III) doses. Two isotherms models (Langmuir and Freundlich models) were used to simulate the experimental data. From Fig. 4b and Table 2, Langmuir model simulated the experimental data better than Freundlich, and the maximum immobilization capacities (Cs max) of Eu(III) on mutated C. sphaerospermum was 278.8 mg/g at pH 6.5, which was approximately three times than that of raw C. sphaerospermum. Besides, Cs max of mutated C. sphaerospermum was also higher than Eu(III) onto other biomaterials, such as Mycobacterium smegmatis (19.15 mg/g at pH 5.0), Pseudomonas aeruginosa (44.1 mg/g at pH 5.0 and 293 K), and Sargassum sp. [35,36,37]. These results indicated that mutated C. sphaerospermum was a feasible and efficacious material to control Eu(III) pollution in the environment.
XPS and FTIR analysis
XPS spectra demonstrated the sensitivity for identifying elements on mycelia. Therefore, the XPS technique was applied to investigate immobilization mechanism. The XPS spectra of Eu(III) immobilized on mutated C. sphaerospermum was shown in Fig. 5a. After immobilization, peaks at 1134.6 and 1164.4 eV were attributed to Eu 3d5/2 and Eu 3d3/2, respectively, which demonstrated the high absorbability of mutated C. sphaerospermum for Eu(III). Compared to mutated C. sphaerospermum, C, N, and O percentage of mutated C. sphaerospermum- Eu(III) correspondingly declined from XPS analysis (Table 3), which indicated Eu(III) immobilization on mutated C. sphaerospermum was partially related to groups contained O and N atoms on the surface of mycelia [38,39,40].
The FT-IR spectra of unloaded and Eu(III) loaded mutated C. sphaerospermum were presented in Fig. 5b. It showed some distinct peaks at 1034 cm−1 (> S=O), 1246 cm−1 (the amide III band, C–N stretch), 1332 cm−1 (C–O stretches), 1442 cm−1 (stretching of COO–), 1560 cm−1 (the amide II band, C–N stretching and N–H bending vibration), 1656 cm−1 (the amide I band, C=O stretching), 1748 cm−1 (> C=O stretching), 2926 cm−1 (–CH stretching vibrations), and band at 3200–3500 cm−1 (O–H and N–H stretching vibrations) [41, 42]. After Eu(III) immobilization, peaks of C–N stretching and carboxyl groups (C–O) shifted, which showed it contributed to the complexation between Eu(III) and mutated C. sphaerospermum [43]. XPS and FTIR analysis revealed amino, hydroxyl, and carboxyl groups were responsible for Eu(III) immobilization onto mutated C. sphaerospermum.
Changes of subcellular structure under Eu(III) stress
TEM was used to investigate the changes of subcellular structure of mutated C. sphaerospermum before and after Eu(III) exposure in the same nutritional state. No obvious change in extracellular structure of mutated C. sphaerospermum was observed before and after Eu(III) exposure (Fig. 6). There were some electron-dense bodies in the cells of mutated C. sphaerospermum after exposure Eu(III). The EDS spectra derived from electron-dense bodies indicated that they were consisted of carbon, oxygen, phosphorus, europium and copper. The copper band was from the grid used to support sections (Fig. 6b). The detoxification of Eu(III) by mutated C. sphaerospermum might be mediated through thiol compounds, which bound intracellular free Eu(III) in order to reduce damage to the metabolic process [44]. These changes might be part of the adaptation mechanism of fungi to metal toxicity according to previous results. The intracellular electron-dense area was revealed by TEM, indicating chromate penetration into the cell of Aspergillus niger [45]. TEM and EDS of Pseudomonad (CRB5) also demonstrated U(VI) appeared in the cell [46]. Besides, the analysis of TEM and EELS indicated that excessive amounts of Cu(II) induced subcellular changes of Allium sativum L. [47].
Conclusions
In this study, C. sphaerospermum was mutated by LTP to enhance Eu(III) immobilization. The mutated C. sphaerospermum presented higher adsorbability for Eu(III) immobilization investigated by batch experiments, and Langmuir model simulated the experimental data better than Freundlich model. The results of XPS and FTIR showed that carboxyl, hydroxyl and amino groups on mycelia favored Eu(III) immobilization on mutated C. sphaerospermum, and intracellular structures of mycelia changed obviously under Eu(III) stress by TEM analysis. These results were crucial for further understanding the transportation and accumulation of radionuclides on fungi in environmental cleanup.
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This research was supported by National Natural Science Foundation of China (21607156) and China Postdoctoral Science Foundation funded project (2015M581047).
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Liang, J., Li, L. & Song, W. Improved Eu(III) immobilization by Cladosporium sphaerospermum induced by low-temperature plasma. J Radioanal Nucl Chem 316, 963–970 (2018). https://doi.org/10.1007/s10967-018-5751-2
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DOI: https://doi.org/10.1007/s10967-018-5751-2