Potential application of Fusarium fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) for removal of Tl (I) ions from water

Water pollution caused by heavy metals poses a serious threat to the ecosystem and human health. Among the various treatment techniques for water remediation, adsorption is an efficient method due to its high capacity, low cost, and simplicity. Thallium (Tl) is highly toxic to mammals and its removal from water is gaining increasingly prominent attention. In this study, three fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) were tested for removal of Tl (I) from aqueous solutions and showed excellent removal performance. The prepared inactive fungal strains were characterized by XRD, FT-IR, SEM, and XPS analyses. The effects of pH, contact time, biomass dosage, and reaction temperature on the removal efficiency of Tl (I) were systematically investigated. The results indicated that the adsorption isotherm data fit well with the Langmuir model, and the pseudo-second-order model was more consistent with the kinetic data description. The maximum adsorption capacity of the fungal strain (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) for Tl (I) was found to be 94.69 mg/g, 66.97 mg/g, and 52.98 mg/g, respectively. The thermodynamic data showed that the sorption process was spontaneous and endothermic. The present study showed that the inactive fungal strains could be a promising adsorbent material for Tl (I) removal.


Introduction
Water is essential for all living organisms on earth. However, freshwater is no longer easily available due to unwanted toxic chemicals such as heavy metals (Chiban et al. 2011;Wang et al. 2019;Honarmand et al. 2021). Among the various heavy metals, thallium (Tl) is one of the most toxic ones to the ecosystem and human health Peter and Viraraghavan 2008) and causes significant adverse health effects even at a low level. Tl mainly exists in two oxidation states, Tl (I) and Tl (III), in the aqueous environment (Li et al. 2019b;Wick et al. 2017). Tl (I) ions are highly stable and mobile, thus the dominant species in natural water (Birungi and Chirwa 2015). In comparison, Tl (III) is highly reactive and can be easily hydrolyzed in alkaline or neutral solutions. Tl is widely used in the industries of optical lenses, alloys, dyes, rodenticides, semiconductors, and pigments ). Long-term Tl poisoning can cause anorexia, headache, abdomen pains, alopecia, blindness, and even death (Galván-Arzate and Santamarıá 1998). To minimize these health risks, a maximum contaminant level of 2 μg/L was set as drinking water standard by the US Environmental Protection Agency (Zou et al. 2020). A much more stringent standard for the source of drinking water was established in China, in which the upper limit of Tl is 0.1 μg/L (Deng et al. 2021). This indicates a great need to develop efficient methods for the Tl (I) treatment technology. To date, various techniques have been investigated for the removal of Tl (I) wastewaters, including adsorption (Li et al. 2020a, b, c), oxidation (Li et al. 2019a;Liu et al. 2017), ion exchange (Hanafi 2010), and solvent extraction (Rajesh and Subramanian 2006). Among these techniques, adsorption is extremely attractive due to its simple operability and high efficiency. A variety of adsorbents, such as carbon nanotubes (Pu et al. 2013), modified Aspergillus niger biomass (Peter and Viraraghavan 2008), modified sugar beet pulp (Zolgharnein et al. 2011), Macroalgae , activated carbon (Rivera-Utrilla et al. 1984), titanate nanotubes , MnO 2 @pyrite cinder (Li et al. 2018a,b), saw dust (Memon et al. 2008), microbial fuel cells (Wang et al. 2018), and amorphous hydrous manganese dioxide ) have been tested for the removal of Tl (I) ions from water. Notably, there are abundant functional groups on the surface of microbial cell walls, such as sulfhydryl, hydroxyl, carboxyl, and amide, whose complexation and coordination make both the active and inactive biomass of microorganisms exhibit a good ability to adsorb heavy metals. These groups can form covalent bonds with the adsorbed metal ions to achieve the purpose of adsorption removal. The usage of inactive biomass for heavy metal removal is more advantageous than active one owing to a variety of mechanisms such as complexation, electrostatic interactions, chelation ion exchange, and non-toxicity concerns . Other advantages of using inactive biomass as adsorbent are no requirement of growth media or nutrients. Therefore, the inactive biomass of microbes has become one of the prominent options among the adsorbents for the removal of Tl from wastewaters.
Fungal strains, which contain a large number of active groups, such as sulfhydryl groups, carboxyl groups, and hydroxyl groups, can have a strong affinity to Tl (I) and may lead to effective removal of Tl (I) by adsorption. Therefore, three different thallium-resistant fungal strains, Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR, were selected and compared for the adsorption of Tl (I), which were screened from thallium tailings. These three different fungal strains were cultivated, characterized with X-ray diffraction (XRD), scanning electron microscope (SEM), and applied in Tl (I) removal from water. The Tl (I) removal mechanism was also explored by FT-IR and XPS analyses. Various operating parameters, such as solution pH, adsorbent dosage, initial Tl (I) concentration, contact time, and reaction temperature, were evaluated systematically in batch experiments. In addition to kinetic and isotherm, thermodynamic parameters were also evaluated to provide insights into the removal of Tl (I) ions. The obtained results will be helpful for the development of low-cost and eco-friendly sorbents for the removal of Tl (I) ions.

Chemicals and reagents
All chemicals and reagents used in the test were analytical grade and were used according to the provided specifications (Guangzhou Huaxin reagent Co. Ltd). The water for the whole experiments is obtained through the deionized water equipment (YL05-20L 75G, Shenzhen, China). A Tl (I) stock solution (1000 mg/L) was dissolved by TINO 3 (99.99%, Aldrich) in 2.0 mol/L HNO 3 solution. The working solution was serially diluted from standard solution when needed.

Preparation of adsorbents
The pure fungal colonies of different fungi were inoculated on sterilized Potato Dextrose Agar medium (PDA: peeled potato 200 g, glucose 20 g, deionized water 1000 ml, pH 6.8-7.0) and incubated at 25 °C in 250 mL conical flasks on a temperature-controlled shaker at 150 r/min for 72 h cultivation. After filtering and collecting the mycelium, the biomass was rinsed with deionized water several times to remove residual medium and impurities, and dried in an oven at 100 °C for 2 h, and then ground into fine powder for the subsequent adsorption studies.

Phylogenetic analysis of the Tl (I)-resistant fungi
The genomic DNA of the thallium-tolerant fungal was extracted and then was subject to polymerase chain reaction (PCR) amplified with the universal primers to amplify the ITS1-5.8S-ITS2 region sequence. The PCR products were analyzed by electrophoresis in 0.8% agarose gel and the objective gene fragment was collected and sent for gene sequencing at Shanghai Sangon Company. The obtained sequence was analyzed at Genebank database using BLAST program, and the aligned gene sequences of the related species were retrieved from the NCBI nucleotide database. The software Clustal X with default parameters was run for implementing the multiple sequence alignment. The phylogenetic tree was constructed using the neighborhood joining method through 1000 repeated samplings, and the phylogenetic tree and genetic distance were analyzed by MEGA6.0 program.

Characterization of the adsorbents
Fourier transform infrared (FT-IR) spectroscopy (ALPHA-T, Bruker German) was used to analyze surface functional groups. The samples were prepared by mixing dried biomass with KBr with the mass ratio of 1:100, and spectra were recorded in the wave number range of 400-4000 cm −1 . The surface morphology and elemental composition of the pure fungal strains and Tl (I) loaded ones were observed through SEM and EDX (PANalytical, Neitherland). XPS analysis (Kratos Axis Ultra, Japan) was carried out to elucidate the adsorption mechanism of fungal strains with Tl (I) ion. The concentration of Tl (I) in the samples was measured by ICP-MS (Agilent, 7700, USA).

Batch adsorption experiments
Batch adsorption experiments were conducted in a rotary shaker by using 100 mL Erlenmeyer flasks. All tests were repeated 3 times. The effect of solution pH on the removal of Tl (I) was studied at a certain concentration of Tl (I) with the pH range from 2.0 to 7.0. To adjust the solution pH, 0.2 mol/L HCl or NaOH was used. To study the effect of contact time on Tl (I) removal, adsorption experiments were carried out with the contact time ranging from 30 to 240 min. For kinetic and isotherm studies, the initial concentration of Tl (I) varied from 10 to 150 mg/L and the solution pH was adjusted to 5. After contact for 60 min, the solution was filtered thrice using Whatman filter paper and then sent for determination of the concentration of residual Tl (I) ion through inductively coupled plasma-mass spectrometry (ICP-MS). All experiments were performed in triplicate and the data were shown as the average values. The amount of Tl (I) adsorbed by the sorbent was determined from the difference of Tl (I) concentrations in the initial and final solutions, as shown in the following equations (Dai et al. 2021): where C 0 (mg/L) is the initial concentration of Tl (I), C e (mg/L) is the equilibrium Tl (I) concentrations of the solutions, V (L) is the solution volume, and M is the mass (g) of adsorbent.

Desorption and regeneration
Desorption is an important criterion to measure the reusability performance of materials. To further understand the recyclability of the adsorbent, desorption of Tl (I) onto the three strains was confuted. Adsorption-desorption cycles were repeated five times with 0.1 mol/L HCl at room temperature. Before sorption, 0.01 g of the adsorbent of Tl (I) was added to 10 mL of the eluate in 50 mL Erlenmeyer flasks and continuously stirred at 150 r/min for 60 min. The final concentration of Tl (I) in the supernatant was determined through ICP-MS, and the desorption efficiency was calculated as follows:

Point of zero charge
Potential is critical to the stability of colloidal dispersion in solution Zeta potentials of the three inactive strains were measured using Particle Metrix (Germany), weigh 0.1 g adsorbent, add it into 50 ml distilled water, adjust pH to 2-7, and shake it at 200 rpm for 30 min (Dittrich and Sibler 2005). The value obtained is the point of zero charge.

Adsorption kinetics
Kinetic study is important in batch experiments to optimize the contact time and to know the kinetic model that the adsorption is following. The pseudo-first-order kinetic (Lagergren 1898) and pseudo-second-order kinetic (Ho and McKay 1999) were used to evaluate the adsorption of Tl (I) ions.
The pseudo-first-order model describes the relationship between the adsorption rate on adsorbent and the equilibrium time. The linear form of the pseudo-first-order kinetic model can be expressed as follows (Huang 2019): where q e (mg/g) represents the adsorption capacity at equilibrium, q t (mg/g) represents the adsorption capacity at time (h) t, k 1 (h −1 ) represents the rate constant at equilibrium. The pseudo-second-order model was based on the assumption that the adsorption rate is controlled by the chemical adsorption mechanism. This chemical adsorption involves electron sharing or electron transfer between adsorbent and adsorbate (Wu et al. 2019;Boukarma et al. 2021). The linear form of the pseudo-second-order kinetic model can be expressed as follows (Sarı et al. 2011): where q e (mg/g) represents the adsorption capacity at equilibrium, q t (mg/g) represents the adsorption capacity at the time (h) t, and k 2 (g/mg/h) is the second-order rate constant of the adsorption process.

Adsorption isotherms
Adsorption isotherms describe the adsorption capacity of the adsorbent versus the concentration of the adsorbate at equilibrium. The Langmuir model assumes that the adsorption process occurs on a uniform surface through a single layer, and there is no interaction between the adsorbed ions. In this study, the experimental data were analyzed using the widely used Langmuir (Langmuir 1918) and Freundlich isotherm (Freundlich 1907) models. The linear form of the Langmuir equation can be expressed as follows: where q e (mg/g) is the adsorption capacity of Tl (I), C e (mg/L) is the equilibrium concentration of Tl (I), Q max (mg/g) is the saturated monolayer maximum adsorption capacity and b (L/mg) is the Langmuir isotherm constant that relates to the energy of adsorption. At the point of maximum adsorption, only a monolayer of adsorbate is formed and there is no interaction between sorbed molecules. The Freundlich model assumes that the adsorption of metal ions takes place on heterogeneous surfaces, and adsorption capacity is related to the concentration of the metal ions at equilibrium. The equation can be represented by the following formula (Li et al. 2020a, b, c, d): where q e (mg/g) is the adsorption capacity, C e (mg/L) is the equilibrium concentration of the study solutions, K f is the Freundlich constant related to the adsorption amount, n is the adsorption intensity of adsorption.

Thermodynamic studies
Various thermodynamic parameters like enthalpy change (∆H°), entropy change (∆S°), and Gibbs free energy (ΔG°) give insights into the sorption mechanism (Chiban et al. 2016). Enthalpy is the total heat of the system, whereas the entropy measures the degree of randomness of the system (Lu et al. 2013). Entropy is the driving force for adsorption when the system is isolated and no heat transfer occurs from the system to the environment and vice versa (Igberase et al. 2014). The thermodynamic parameters can be calculated from the following Van't Hoff's equations (Pongener et al. 2018): where K d represents the thermodynamic equilibrium constant without unit. R is the gas constant (8.314 J/moL/ K), T is the absolute temperature in Kelvin.

Phylogenetic tree analysis of Tl (I)-resistant fungus
According to the phylogenetic tree analysis of 16S rRNA, the gene sequences of the isolated strain JCCW-FP, JCCW-FB, and JCCW-FR have a 99% sequence identity to the members of the genus Fusarium sp., Arthrinium sp., and Phoma sp., respectively (Fig. 1), based on which the simplified names were denoted as Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR, respectively. To the knowledge of existing documentation, the three isolated strains have been demonstrated as high-efficiency adsorbents for the removal of heavy metals, Cd (II), Pb (II), and so on (Anagnostopoulos et al. 2012;Sanyal et al. 2005), and may also be applicable to the biosorption of other metals, such as Tl (I).

XRD analysis
The crystalline phase of inactive biomass of three strains before and after Tl (I) adsorption was determined by XRD analysis. The XRD analysis of pure Fusarium sp. FP, Arthrinium sp. FB, Phoma sp. FR, and their Tl (I) loaded ones are displayed in Fig. 2A-F. The XRD patterns of three strains had a weak and broad peak at 2θ = 22°, indicating that all the inactive biomasses of three strains were in low crystallinity. Compared with the adsorbent before adsorption, more intense peaks for the adsorbent after Tl (I) adsorption were observed, due to the presence of Tl (I) bonding with molecules that may lead to stronger crystallinity.

FT-IR analysis
The FT-IR spectra of pure fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) and Tl (I) loaded fungal strains are shown in Fig. 3. There was an obvious change in the intensity of the bands of the biomass after the adsorption of Tl (I) ions. The peak at 3392.10 cm −1 representing the stretching of -OH or -NH 2 groups shifted to 3404.89 cm −1 after adsorption for Fusarium sp. FP, from 3379.31 to 3398.87 cm −1 for Arthrinium sp. FB and from 3385.33 to 3425.20 cm −1 for Phoma sp. FR. This result could originate from the bonding of -OH or -NH 2 groups with Tl (I) ions. Before Tl (I) sorption, the band corresponding to C = O stretching of amide was observed at 1630.09  (Liao et al. 2020). The peaks at 1060.56 and 1034.23 cm −1 band were assigned to -H-C-H or C-O stretching vibrations (Huang et al. 2021). After Tl (I) adsorption, a change in peak positions as described above shifted from 1630.09 to 1650.41 cm −1 and from 1060.56 to 1074.11 cm −1 for Fusarium sp. FP, from 1636.87 to 1656.43 cm −1 and 1041 to 1053.79 cm −1 for Arthrinium sp. FB, and from 1643.64 to 1624.08 cm −1 and from 1034.23 to 1047.71 cm −1 for Phoma sp. FR, demonstrating that the involvement of C = O, -NH 2 and -OH groups in the Tl (I) adsorption process (Anton et al. 2013).

SEM with EDS analysis
The scanning electron microscopy was used to understand the variation in morphological features and surface characteristics of the adsorbent. The elemental distribution over the surface is confirmed by EDS analysis. The SEM with EDS micrographs of the three inactive strains before and after Tl (I) adsorption were depicted in Fig. 4. Before adsorption, the surface of the adsorbent was relatively smooth. After adsorption, the surface became rough. Thus, distinctive changes in the inactive surface of the three strains were observed after Tl (I) adsorption. Through the EDS analysis of the adsorbent sample after Tl (I) adsorption, peaks of Tl (I) ion were observed along with all the other components identified in the adsorbent, which confirms the adsorption of Tl (I) ions onto the inactive biomasses (Bulut and Baysal 2006).

XPSanalysis
The chemical states of the surface elements of fungal strains of Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR were further determined with XPS measurements and are shown in Figs. 5, 6, and 7. As illustrated in Figs. 5A, 6A, and 7A, a wide scan spectrum comprised of carbon, nitrogen and oxygen. After the Tl (I) sorption, Figs. 5B, 6B, and 7B showed a pair of new weak peaks and it represents the Tl 4f spectra. This result confirms that the Tl (I) ions were successfully sorbed by the three bacterial strains. The deconvolution of C 1 s spectra produces three peaks with binding energy of 284.2, 285.6, and 287.8 eV. As shown in Figs. 5C, 6C, and 7C, these peaks can be allocated to the C atom in the form of C-C, C-OH, and O = C-O, respectively (Li et al. 2018a, b, c). After the Tl (I) sorption, the content of C increased from 75.82 to 80.32% for Fusarium sp. FP, 74.94 to 77.21% for Arthrinium sp. FB, and 70.82 to 73.21% for Phoma sp. FR. The peak at 398.4 eV mainly belongs to R-NH 2 /R 2 -NH group (Ho et al. 1999). It can be seen from Fig. 7C and D that the peak area percentage decreased from 8.1 to 6.8%. The R-NH 2 /R 2 -NH group may participate in the Tl (I) sorption, causing a significant reduction in its relative content. As to the peak at binding energy of 528.45 eV, the increment of peak area percentage indicated that the C = O groups contributed to the removal of Tl (I) ions from aqueous solution. The conclusions obtained were consistent with the FT-IR experimental results.

Influence of pH
The effect of pH on the adsorption of Tl (I) onto fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) was investigated by using 25 mL of Tl (I) (100 and 200 mg/L) for a pH range of 2.0 to 8.0 at room temperature, as shown in Fig. 8A. It is clear that the capture of Tl (I) tended to increase with increasing pH (2.0 to 5.0) and reached the maximum value at pH 5.0. When the pH values were below 3.0, there was a low Tl (I) removal efficiency because at these low pH values, H 3 O + ions compete with Tl (I) ions for the sorption sites. In acidic media, H 3 O + ions could not only protonate amine and hydroxyl groups generating strong electrostatic repulsion towards Tl (I) but also compete with Tl (I) for adsorption sites (Galván-Arzate and Santamarıá 1998). Hence, the removal efficiency of Tl (I) by fungal strains was poor at low pH values. The optimal removal efficiency of Tl (I) ions occurred at pH 5.0. Thus, all the subsequent sorption experiments of Tl (I) ions were operated under the optimal pH value of 5.0.

Influence of biomass dosage
The amount of adsorbent used in adsorption is important because it determines the sorbent-sorbate equilibrium and can also be used to predict the treatment cost of adsorbent per unit of Tl (I) ions. The effect of adsorbent dosage on Tl (I) ions removal was studied from 0.5 to 3 g/L and the results are represented in Fig. 8B. The results show that removal capacity of Tl (I) ions decreased with increasing adsorbent dosage. It indicates that Tl (I) sorption onto biomass is not strictly a surface phenomenon and that some sorption sites may remain unsaturated during the sorption process due to possible electrostatic interactions between binding sites, ineffective mixing of metal solutions, and high sorbent dosages (Bulut and Baysal 2006;Rao and Khan 2009;Sharma and Forster 1993). Maximum Tl (I) adsorption capacity of 63.75 mg/g for Fusarium sp. FP, 51.23 mg/g for Arthrinium sp. FB, and 49.80 mg/g for Phoma sp. FR was obtained when 0.5 g/L of biomass was used.

Influence of initial Tl (I) concentration
Initial concentration provides an important driving force to overcome mass transfer resistances between the aqueous and solid phases (Dönmez and Aksu 2002). In the present study, initial Tl (I) concentration varied from 10 to 300 mg/L and the results are shown in Fig. 8C. The sorption capacity increased with increasing Tl (I) concentration and then reached an almost constant value. The initial increase in sorption capacity may be owing to the higher availability of Tl (I) ions. Moreover, a high concentration enables a driving force to overcome the mass transfer resistance between Tl (I) ions and adsorbents. No considerable increase in the sorption capacity with further increase in Tl (I) concentration suggests the saturation of binding sites (Huangfu et al. 2017).

Influence of contact time
In adsorption process, contact time is one of the most important factors that influence Tl (I) removal. All of the parameters except contact time, including temperature, adsorbent dose (10 g/L), pH (5), initial Tl (I) concentration (100 mg/L), and agitation speed (160 rpm), are kept constant, and the results are depicted in Fig. 8D. The adsorption capacity for the three biomasses reached equilibrium at 60 min, and the maximum adsorption capacity was found to be 63.86 mg/g for Fusarium sp. FP, 53.21 mg/g for Arthrinium sp. FB, and 49.50 mg/g for Phoma sp. FR. In initial stage, the metal removal efficiencies of adsorbents increased rapidly due to abundant availability of active binding sites on the biomass, and gradually these sites would be occupied by Tl (I) ions. Afterward, it continued at a slower rate and finally reached equilibrium when the adsorption sites on the adsorbent surface reached saturation.
The adsorption became less efficient in the later stages and finally reached equilibrium ). The contact time of 60 min was found to be sufficient to reach equilibrium, so it was selected as the optimum time for the further experiments.

Desorption and regeneration
As shown in Fig. 8E, the desorption efficiencies of Tl onto strain FP, FB, and FR only decreased by 10.9%, 9.9% and 11.60%, respectively, after five cycles. High removal efficiency of the strains remained, suggesting it can be employed as a potential economic, efficient, and environmental-friendly functional material for the effective removal of Tl (I) from the aqueous solutions.

Point of zero charge
The zero point of three strains in the pH range of 2-7 is shown in Fig. 8F. It is found that the pH increased to 7, which might be attributed to the largely increased amount of amine and hydroxyl groups on the surface of three strains. The result is consistent with that of infrared spectrum (Fig. 3). Undoubtedly, more negative zeta potential of absorbents is favor for the biosorption toward positively charged metal ions through electrostatic force. Similar results had  been reported by studies on the biosorption of other pollutants (Luo et al. 2014;Huang et al. 2020).

Adsorption kinetics
The pseudo-first-order and pseudo-second-order kinetic rate constants K 1 , K 2 , and q e values are determined from the slope and intercept of Fig. 8G, and the related calculated parameters are summarized in Table 1. The correlation coefficients of the pseudo-first-order kinetic constants were much lower than those of the pseudo-second-order kinetic model. As seen from the Table 1, the calculated q e values of the pseudo-first-order were too low compared with experimental q e values in all experiments, whereas the calculated q e values of pseudo-second-order model fitted well with the experimental data and were better than the pseudo-first-order kinetic model (Li et al. 2018a, b, c). This suggests that the pseudo-second-order adsorption was more appropriate to describe the overall rate of Tl (I) adsorption, which appeared to be controlled by the chemical sorption process (Li et al. 2019b).

Adsorption isotherms
It was found that the maximum sorption capacities of the synthesized fungal strains of Fusarium  Table 2 indicated that the Langmuir adsorption model fitted the equilibrium data very well. The R 2 values obtained by Freundlich isotherm fitting were low (0.9133, 0.9274, and 0.9195), which indicated that they were in poor agreement with Freundlich isotherm. The good fit of experimental data by the Langmuir equation confirms that the Tl (I) capture by the sorbent material in this study could be considered as homogeneous adsorption, which the target sorbate was adsorbed through the homogenous distribution of active site onto the surface (Padmavathy et al. 2003). Based on the above findings, it may be concluded the Langmuir isotherm is the most appropriate model that well fits with experimental data.

Thermodynamic studies
The values of ΔG 0 , ΔH 0 , and ΔS 0 are listed in Table 3. It can be seen from Table 3 that the positive value of ΔH 0 showed that the adsorption process was endothermic in nature (Pang et al. 2010). The negative value of ΔG 0 confirmed that the adsorption process was feasible and spontaneous (Saravanan et al. 2021). The negative values of ΔG 0 decreased with increasing temperature indicating that the adsorption became less favorable at higher temperatures. The positive value of ΔS 0 shows the increasing randomness between the sorbents and sorbate of the solution (Pan et al. 2009).

Removal mechanisms
To obtain insights into the Tl (I) adsorption by the three strains, FR-IR and XPS spectra before and after adsorption were analyzed. After adsorption, there was a significant shift of the broad characteristic peak at 3380 cm −1 which assigned to the functional groups with hydroxyl and amine (Chen et al. 2022); the adsorption peak at 1630 cm −1 attributed to C = O group was weakened after adsorption. These results revealed that C = O, -NH 2 , -OH functional groups participated in the complex reactions with Tl (I) after Tl (I) adsorption. The area of O 1 s peak with binding energy 528.45 eV, the relative content had changed remarkably, which was attributed to the functional groups such as C = O and Tl (I) and the formation of bonds between Tl (I) and oxygen atoms; these results indicated that C = O groups contributed to Tl(I) adsorption during the process. For N 1 s, the binding energies at 398.4 eV corresponding to -NH 2 groups shifted as well, suggesting that nitrogen atoms with a pair of lone electrons were involved in Tl (I) adsorption (López et al.2021). On this basis, a novel hybrid process, including surface complexation, electrostatic interaction, and adsorption, was proposed. The proposed mechanisms for Tl (I) removal by the strains are shown in Fig. 9. Firstly, Tl (I) diffused from the solution to the solid/water interface. Tl (I) ions then passed through the liquid film to the strain cell surface. The -OH, -NH 2 , and C = O groups on the surface of the strains were partially bound with Tl (I). Meanwhile, partial Tl (I) was adsorbed by surface electrostatic adsorption and surface complexation.

Comparison study of inactive fungal strains with other sorbents
The maximum monolayer adsorption capacity (q max ) of fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) for the removal of Tl (I) ions was compared with that of other adsorbents reported in the literature (Memon et al. 2008;Sangvanich et al. 2010; Şenol and Ulusoy 2010;  Table 4. From the above results, it may conclude that fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) can act as a promising adsorbent for removal of Tl (I) ions from aqueous environment.

Conclusions
The efficiency of the synthesized fungal strains (Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR) was studied for the removal of Tl (I) ions from aqueous solutions. Batch experiments at different conditions, such as various solution pH, Tl (I) initial concentration, biomass dosage, temperature, and contact time, were conducted. The adsorption equilibrium data can be well described by the Langmuir isotherm, with a maximum adsorption capacity of fungal strains of Fusarium sp. FP, Arthrinium sp. FB, and Phoma sp. FR being 94.69 mg/g, 66.97 mg/g, and 52.98 mg/g at equilibrium time of 60 min and 323 K, respectively. Thermodynamic analyses indicated that the adsorption nature of Tl (I) sorption onto the fungal strains were feasible, spontaneous, and endothermic. Furthermore, mechanistic characterization by FT-IR, SEM-EDS, XRD, and XPS demonstrated that hydroxyl, carboxyl, and amino functional groups on the surface of strains were involved in the adsorption process of Tl (I). Based on the above research findings, the three strains can be employed as a potential economic, efficient, and environmentalfriendly material for removal of Tl (I) from aqueous solutions, and it is of great practical significance to the sustainable development of ecological environment.
Author contribution All authors contributed to the study's conception and design. Material preparation, data collection, and analysis were performed by JM, YL, XG, SZ, YD, YK, LP, HL, SC, and JL. The first draft of the manuscript was written by JM and JL, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Availability of data and materials The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

Declarations
Ethical approval and consent to participate Not applicable.

Consent to publish Not applicable.
Competing interests The authors declare no competing interests.