A synergistic biosorption and biomineralization strategy for Kocuria sp. to immobilizing U(VI) from aqueous solution

Accepted Manuscript A synergistic biosorption and biomineralization strategy for Kocuria sp. to immobilizing U(VI) from aqueous solution

Yiqian Wang, Xiaoqin Nie, Wencai Cheng, Faqin Dong, Yuanyuan Zhang, Congcong Ding, Mingxue Liu, Abdullah M. Asiri, Hadi M. Marwani PII: DOI: Reference:

S0167-7322(18)33837-6 https://doi.org/10.1016/j.molliq.2018.11.079 MOLLIQ 9989

To appear in:

Journal of Molecular Liquids

Received date: Revised date: Accepted date:

25 July 2018 5 November 2018 16 November 2018

Please cite this article as: Yiqian Wang, Xiaoqin Nie, Wencai Cheng, Faqin Dong, Yuanyuan Zhang, Congcong Ding, Mingxue Liu, Abdullah M. Asiri, Hadi M. Marwani , A synergistic biosorption and biomineralization strategy for Kocuria sp. to immobilizing U(VI) from aqueous solution. Molliq (2018), https://doi.org/10.1016/j.molliq.2018.11.079

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT A synergistic biosorption and biomineralization strategy for Kocuria sp to immobilizing U(VI) from aqueous solution YiqianWanga, b, XiaoqinNiea, b*, Wencai Chenga, b*, Faqin Dong c, Yuanyuan Zhangb, Congcong Dinga, Mingxue Liud, Abdullah M. Asiri,e Hadi M. Marwanie a

Fundamental Science on Nuclear Wastes and Environmental Safety Laboratory,

b

PT

Southwest University of Science and Technology, Mianyang 621010, P. R. China School of National Defence Science & Technology, Southwest University of Science

Key Laboratory of Solid Waste Treatment and Resource Recycle, Ministry of

SC

c

RI

and Technology, Mianyang 621010, P. R. China

Education，Southwest University of Science and Technology, Mianyang 621010, P. R.

d

NU

China

School of Life Science and Engineering, Southwest University of Science and

e

MA

Technology,Mianyang Sichuan 621010, P. R. China

Chemistry Department, Faculty of Science, King Abdulaziz University, Jeddah

PT E

D

21589, Saudi Arabia

Abstract

CE

In order to investigate the immobilization ways of uranium (U(VI)) on Kocuria sp, we investigated the interaction behavior under different conditions by batch

AC

experiment. U(VI) products on Kocuria sp were characterized by SEM, XRD, FTIR, and XPS techniques. SEM-EDS results presented U(VI) mineral-like precipitation formed on the cell surface which contained high percentage of P and U elements. XPS results also confirmed the appearance of bond P-O-U. XRD results illustrated characteristic UO22+ peaks after U(VI) interaction with Kocuria sp. According to FTIR analysis, in addition to PO43- groups, C=O, -OH, -COOH groups might play

1

ACCEPTED MANUSCRIPT important roles in complexation with U(VI). The biomineralization process of U(VI) on Kocuria sp required longer time than sorption process, indicating that biomineralization was induced by the biosorption process. Our findings highlight the synergistic biosorption and biomineralization process of Kocuria sp for U(VI)

PT

immobilization, which concentrated U(VI) on the cell surface via fast biosorption

RI

by providing nucleation sites for the precipitation to insoluble minerals, while the

SC

formation of U(VI) biomineral led to the relatively permanent immobilization of U(VI), and then emphasize the important roles of phosphate which are of

NU

significance in predicting the U(VI) immobilization properties.

MA

Keywords U(VI), Kocuria sp, biosorption, biomineralization, phosphate 1. Introduction

D

With the rapid development of the nuclear industry, nuclear energy is becoming

PT E

more and more widely used in nuclear power, military, medical treatment, agriculture and so on [1]. But the risk of the nuclear leak into groundwater has plagued

CE

generations of scientists. Considering the complexity of components in soils, it is

AC

necessary to understand the possibility of radionuclides to flow into biosphere and their interaction with soil components [2]. Organic matter and inorganic matter are two major categories in soils. Microbes, especially the bacteria, are one of the most active organic matter in soils [3, 4]. Therefore, understanding the interaction mechanisms between radionuclides and bacteria is of significant for predicting the chemical behavior, toxicity, bioavailability, and migration of radionuclides in biosphere. 2

ACCEPTED MANUSCRIPT Bacteria have the characteristics of fast metabolism rate, strong environmental tolerance, larger surface area [5], which contribute to radionuclides immobilization. Bacteria affect the solubility of radionuclide mainly via direct (i.e., biosorption, reduction, or biomineralization of radionuclides) or indirect ways (alteration of

PT

microenvironment by the production of various metabolites) [6-8]. Most research

RI

mainly focused on the influence of the bacteria itself. The most common interaction

SC

way between bacteria and radionuclides is surface sorption [9-11]. It is easy to observe radionuclide ions sorption onto bacteria surface due to the presence of

NU

enriched functional groups like carboxyl, hydroxyl and amide groups etc. Bacteria

MA

species such as Bacillus sp, Pseudomonas sp, Streptomyces sp, Escherichia sp and Micrococcus sp, etc., have been tested for uptake of heavy metals or organics [12, 13].

D

By comparison, mineralization of radionuclides occurs only on a small number of

PT E

bacteria and is not so common like sorption process. However, radionuclide biominerals mediated by bacteria is more stable than the adsorbed radionuclides and vulnerable

to

environmental

factors.

Therefore,

understanding

CE

less

AC

radionuclide-bacteria biomineralization mechanism is critical for predicting biogeochemical behavior of radionuclides in environment [14]. Relevant knowledge can provide guide for the development of sustained and effective in-situ bioremediation method. U(VI) biominerals was observed in the surface of Shewanella putrefaciens, Bacillus Mucilaginosus, radiodurans (pK1) [15]. In this study, we chose rose-colored Kocuria I-7R (a gram-positive Kocuria sp bacteria) as a soil bacteria and U(VI) as study object of radionuclides. During the study, we observed the 3

ACCEPTED MANUSCRIPT phenomenon of surface mineralization of U(VI) on Kocuria sp. The goals of this study are: (1) to investigate the interaction behavior between uranium and Kocuria sp under different environmental conditions (i.e., pH, contact time, the concentration of icon); (2) to identify the uranium products after reaction

PT

with Kocuria sp using scanning electron microscopy (SEM), X-ray diffraction (XRD),

RI

infrared spectroscopy (IR) and X-ray photoelectron spectroscopy (XPS); (3) to study

SC

the interaction mechanism between U(VI) and Kocuria sp. This research contributes to understanding the tip of the iceberg in the complex geological body of the

NU

radionuclides, and screens potential bacteria strains for the biological treatment of

2. Materials and method

D

2.1 Materials

MA

radionuclide-contaminated sites.

PT E

Kocuria sp was provided by the laboratory center of the life science of Southwest University of Science and Technology. The bacteria were grown in liquid

CE

culture medium (10 g/L tryptone, 5 g/L yeast extract and 5 g/L sodium chloride at pH

AC

7). Next, the cells were harvested by centrifugation (6000 rpm, 10 min) and were washed three times using NaCl solutions (0.9%, mass percent). The U(VI) stock solution (1 g/L) was prepared from UO2(NO3)2·6H2O. All reagents were purchased as analytical grade chemicals and all experimental solutions were prepared by distilled water. 2.2 Experiments All experiments were conducted at bacterial concentration of 1.0 g/L and 20 4

ACCEPTED MANUSCRIPT mg/L U(VI) solutions at 25 °C. To evaluate the pH effect on the U(VI), considering the slightly acidic and alkaline environment in different uranium tailings, the pH scope of 3.0−10.0 was chosen. The targeted pH values of the solution were adjusted by 0.1 mol/L Na2CO3 or 0.1 mol/L HCl, and the ionic

PT

strength was adjusted by NaCl. After the equilibrium was established, the

RI

samples were centrifuged at 6,000 rpm for 10 min and the concentrations of

SC

U(VI) in the solutions were measured by spectrophotometrically Arsenazo III method at wavelength of 652 nm. Besides, the U(VI) adsorption capacity and

NU

kinetics process of Kocuria sp was investigated at different reaction time. The

MA

supernatant was collected to calculate the adsorption capacity, and the precipitate was collected to analyze the phase composition. The potential of

PT E

and (2), respectively.

D

removal percentage (R (%)) and capacity (Q (mg/g)) could be expressed as Eqs. (1)

(1)

Q = (C0-Ce)V/m

(2)

CE

R = (C0-Ce)×100%/C0

AC

where Q (mg/g) was the amount of U(VI) adsorbed onto the biomass, C0 (mg/L) and Ce (mg/L) were U(VI) concentration before and after adsorption. m (g) and V (mL) were the mass of Kocuria sp and the volume of the suspension, respectively. 2.3 Characterization In this study, we used an acoustic spectrometer SEM-EDS to observe Kocuria sp surface structure and measure the types and contents of the samples. FT-IR spectra were collected from a PerkinElmer Nicolet-5700 spectrophotometer in the 5

ACCEPTED MANUSCRIPT wavenumber range of 400-4000 cm−1. XRD patterns use a Bruker D8 Advance diffractometer equipped. XPS spectroscopy (Escalab 250Xi, Thermo Scientific) were recorded using normal Al Kαradiation (1486.8 eV) under a residual pressure of 2×10−9 Torr.

PT

3. Results and Discussion

RI

3.1 SEM-EDS analysis

SC

Fig.1. showed the SEM images of Kocuria sp after reaction with U(VI) for 0, 4, 12, and 24 h. Fig. 1a exhibited that the original Kocuria sp had smooth surface. After

NU

interaction with U(VI) for only 4h, granular deposits began to appear on the cell

MA

surface, and the EDS analysis detected the signal of uranium (Fig. 1b). By using EDS, it was found that the granular deposits also distribution of O, C, P, was

D

consistent with that of U. The abundant organic matter containing O, C, N, and

PT E

P in the cell further indicates that U(VI) was fixed by the organic functional groups of Kocuria sp as mentioned above. Compared between Fig.1b, c, d, with

CE

the increase in time, the lamellar precipitation on the surface increased. The

AC

presence of U element on corresponding EDS spectrum further indicated that the precipitation was U-related precipitates [40]. Based on these results, we assumed that the Kocuria sp immobilizes U(VI) from aqueous solution included two steps. First, U(VI) was adsorbed on the surface of Kocuria sp as amorphous U(VI) at initially reaction hours. Second, cell surface with concentrated U(VI) provided nucleation sites for the formation U-related lamellar precipitation. This hypothesis helps to explain why the lamellar precipitation become more and more obvious as time goes on [16]. 6

ACCEPTED MANUSCRIPT 3.2 XRD and FTIR analysis Fig. 2a exhibited the XRD results U(VI)-free and U(VI)-loaded Kocuria sp at 4, 12 and 24h. From the picture, we can see that the U(VI)-free bacteria have no obvious diffraction peaks. After reaction with U(VI), Kocuria sp presented diffraction peaks

PT

which were consistent with the PDF card of [CaU(PO4)2] (PDF01-086-0687). XRD

RI

results further demonstrated the lamellar precipitation as uranium phosphate

SC

compounds. Combined with SEM-EDS analysis, the results suggested that U(VI) was adsorbed on the cell surface and formed U-P precipitate extracellularly

NU

while the increase in time, these crystallization of precipitate increased. Which

MA

was determined that phosphoric acid or phosphate groups were the main biological groups that cause bio-mineralization [17]. The FTIR spectra of Kocuria sp after

D

reaction with U(VI) at 4, 12 and 24h were shown in Fig. 2b. We can easily find the

PT E

main functional groups of Kocuria sp, like -OH group (3200-3400 cm-1), C=O and N-H stretching vibrations (1529~1550 cm-1) and -COOH stretching vibration at

CE

1300~1470 cm-1 [18]. It should be pointed out that the intensity of P-O and UO22+

AC

bands (1250 cm-1 and 906~919cm-1) became stronger and stronger as the time goes on, which is consistent with the formation of the U-related biominerals. It means the mineralization of U(VI) on biomass increased with time going by. Overall, UO22+ might be firstly adsorbed by functional groups that were on Kocuria sp surface, which provided the favorable conditions for the subsequently participation between UO22+ and PO43- groups and the formation of [CaU(PO4)2]-like minerals. 3.3 Effect of time 7

ACCEPTED MANUSCRIPT Fig. 3a showed the reaction time curve for U(VI) immobilized by Kocuria sp. At initial one hour, the adsorption rates of U(VI) sharply increased, and then increased slowly to achieve the maximum immobilization amount of 104 mg/g at 4h. The fast sorption rates of U(VI) was mainly attributed to the large surface area of Kocuria sp

PT

and plenty of active sites on its surface [19]. However, we are more interested in the

RI

second part of curve with slow sorption rate. The slower U(VI) immobilization

SC

feature in the second part might mean that U(VI) underwent the mineralization process. In order to further confirm our assumption, the release amount of phosphate

NU

in solution was determined in this study (Fig. 3b). Compared to the original Kocuria

MA

sp at 16h (0.76 mg/L), the phosphate content (0.36 mg/L) of U(VI)-interacted Kocuria sp sample was obviously lower. This is a strong proof that the released phosphate

D

group was precipitated with U(VI) as biominerals.

PT E

3.4 Impact of environmental factors Fig. 4a showed the effect of pH for the removal ability. It revealed the removal

CE

efficiency increased with the increase of pH from 3.0 to 6.5, and then decreased after

AC

pH > 6.5. The maxium removal ability for U(VI) at pH 6.5, and the removal ability could be up to 108 mg/g. It was deduced that H+ surrounded cell membrane which obstructed the active sites interact with UO22+ at acidic solution [20]. As Fig. 4b described, at basic solution, more negative charged species like (UO2)3(OH)7- and UO2(OH)3- gradually dominated [25, 26]. The distribution of U(VI) species (Fig. 4b) in 0.005 mol/L NaCl among the investigated pH range, calculated by Visual MINTEQ 3.0 which were bad for phosphate precipitation. According to the previous discuss 8

ACCEPTED MANUSCRIPT [21], the rising U(VI) removal ability at the start due to the sorption between the negative charge on the surface of Kocuria and the cation in the solution and later uranium combined with phosphate, forming biomineralization. As shown by Fig. 4a, U(VI) removal amount became less with the increased concentration of NaCl from

PT

0.001 to 0.01 mol/L. The result revealed that higher ionic strength affected cell

RI

osmotic pressure, resulted in the more severe the shrinkage of the cell, and then the

SC

surface area and the number of binding sites decrease [22]. Fig.4c showed the effect of Ca2+, Mg2+, Na+ for the removal ability. According to previous report [39], the

NU

aqueous complexes of U(VI)-CaCO3 do dominate the partitioning of U(VI) between

MA

aqueous and sorbed species so that more mobile U(VI) aqueous complexes form, leading to decreasing adsorption. From Fig.4c, it’s obviously that the removal ability

D

of Ca2+, Mg2+ are not as good as Na+. Fig.4d displayed that the removal capacity of

PT E

uranium adding F- decreased compared to Cl-, CO32-. Due to Cl- and CO32- ions can form soluble complexes with UO22+ (e.g., UO2Cl+, UO2CO3 species) [23] which

CE

demonstrated that the sorption of UO22+ on Kocuria composites was ionic

AC

exchange/outer-sphere surface complexation. Whereas F- inhibited the sorption between uranium and Kocuria because of the poisonousness would damage the cell. Besides, F- had a strong ability of complexation with metal ion and the complex ion morphology of uranium also affected adsorption. Under acidic conditions, the main complexes are UO2F2, UO2F3- and UO2F42- [24]. 3.5 Sorption Isotherm The adsorption isotherms of U(VI) on Kocuria sp at 298 K, 308 K, 318 K were 9

ACCEPTED MANUSCRIPT fitted by Langmuir (Fig. 5a) and Freundlich (Fig. 5b) model, respectively. Langmuir adsorption is assumed as monolayer sorption, while the Freundlich adsorption is presumed to apply to the cases where the layer adsorbed is more than one molecule in thickness or molecules binding on a surface site will affect the adjacent sites. The e

PT

Langmuir and Freundlich equations are expressed as in Eqs. (3) and (4), respectively.

RI

qe = bQmaxCe / 1+bCe

SC

qe = KCen

where Q max was the maximum adsorption capacity of adsorbent at complete

NU

monolayer coverage; b was a Langmuir constant; 1/n was the heterogeneity of the

MA

adsorptionsites; K represented equilibrium coefficient [27]. The calculated results of the Langmuir, Freundlich isotherm constants and the correlation coefficients were

D

given in Table 1. It can be noticed that Freundlich model performs better than

PT E

Langmuir model in fitting isotherm. Therefore, we can conclude that the adsorption between U(VI) and Kocuria sp are multilayer adsorption which was dominant for

CE

U(VI) interacted with Kocuria in this study [28].

AC

3.6 Effect of concentration Fig. 5c appeared that initial uranium concentration affected the removal efficiency and the percentage of U(VI). From Fig. 5c, when the U(Ⅵ) concentration increased from 5 to 100 mg/L, the immobilization ability increased from 24.6 to 181 mg/g. This result further explained that higher probability of collision between the uranium and biomass, which was driven by the increase of the initial U(VI) concentration [29,30]. In a word, the rising tendency possibly was due to the higher 10

ACCEPTED MANUSCRIPT concentration promoted the formation of phosphate precipitation. It can be found that the U(VI) removal efficiency increased slightly at lower U(VI) concentrations, whereas decreased sharply at higher U(VI) levels greater than 25 mg/L. According to previous reports [31], the tendency possibly was due to the number of active sites

PT

were not sufficient to adsorb high concentration of uranium.

RI

XPS analysis

SC

XPS was employed to determine the valence states of uranium precipitation on the Kocuria.sp surface. Fig. 6a showed U4f XPS spectra of Kocuria.sp and

NU

U(VI)-interacted Kocuria sp samples at pH 5.5. The binding energies (BEs) of the

MA

spin-obrit split U4f lines closely correlate to the oxidation states of U. As shown in Fig. 6a, U peaks can be fitted by U(VI) at 382.1 and 392.9 eV and U(IV) at 380.8 and

D

391.8 eV [32]. The fitted U(IV) took a slight proportion of immobilized U, which

PT E

illustrated that the minority uranyl ion was reduced from U(VI) to U(IV) by Kocuria sp in aerobic condition [33]. Fig. 6b showed the high resolution of O2s peaks of

CE

Kocuria sp and U(VI)-interacted Kocuria sp. The U(VI)-interacted spectra can be

AC

divided into three components that were corresponded to ‐P=O peak at 531.3 eV, -OH peak at 532.5 eV, -C=O peak at 533.5 eV [34]. Before interaction the spectra can be fitted by -P=O 531.2ev, C=O 533.4ev, C-OH, C=O, O-C-O or COOR 532.4ev. Compared with Kocuria and uranium-interacted Kocuria, there were slight excursion of oxygen-containing group, suggesting the coordination of U(VI) with -P=O and C-OH. We thought that the different relative positions and areas of those peaks represented the influences of the adsorption of uranium [35-38]. Combined with the 11

ACCEPTED MANUSCRIPT previous finding, we suggested that P=O- might combine with uranium formed phosphate and C-OH possibly fractured -OH and produced ester group. In summary, after adsorption with uranium, UO22+ bonded with phosphate. XRD results further demonstrated the lamellar precipitation as uranium phosphate compounds which is

PT

consistent with the findings of SEM-EDS. The uranium precipitates occurred due to

RI

phosphate release from the cellular polyphosphate, which need to be further studied in

SC

our next research work.

4. Conclusions

NU

The U(VI) sorption behavior by Kocuria was studied through above researches.

MA

The biomass had a maximum U(VI) percentage of adsorption 98% at pH 5.0, t = 4h, CU = 20mg/L. The sorption data of Freundlich adsorption model and

D

pseudo-second-order model which revealed that the sorption of U(VI) on Kocuria

PT E

mainly was passive adsorption. The sorption mechanism of Kocuria toward U(VI) included adsorbing uranium by -P=O, -OH, -C=O, -COOH at the short time and then

CE

forming CaU(PO4)2 precipitation in surface. Thus, we guess the effect of sorption by

AC

Kocuria cells depends not only on the passive adsorption of active sites, but also the release of phosphate from the cell. Fast immobilization of U(VI) on the cell surface firstly and gradually the more phosphate was released by Kocuria and was immobilized with U(VI) as the species of uranium phosphate with very low solubility. This research also revealed that phosphatase plays an important role in the process of uranium immobilization.

Acknowledgements 12

ACCEPTED MANUSCRIPT This work was supported by the China National Natural Science Foundation (grant number: 41877323, 41502316, 2170110, 41703118), the China Postdoctoral Science Foundation (grant number: 2017M612991, 2018T110994), the Scientific Research Fund of Si Chuan Provincial Education Department (grant number: 17ZB0445), the

PT

open Foundation of Fundamental Science on Nuclear Waste and Environmental

RI

Security Laboratory (grant number: 17kfhk01), the Funded by Longshan academic

SC

talent research supporting program of SWUST (17lzx528, 18lzx205, 18lzx206,

AC

CE

PT E

D

MA

NU

17lzx524, 18lzx521).

13

ACCEPTED MANUSCRIPT References [1] Mkandawire M. Biogeochemical. Behaviour and bioremediation of uranium in waters of abandoned mines. Environ. Sci. Pollut R. 20(11):7740-7767. [2] Ding C, Cheng W, Jin Z, et al. Plasma synthesis of beta-cyclodextrin/Al(OH)3 composites as adsorbents for removal of UO22+ from aqueous solutions J. Mol. Liq.

PT

207(2015):224-230. [3] Nie X, Dong F, Liu N, et al. An investigation on the subcellular distribution and

RI

compartmentalization of uranium in Phaseolus vulgaris L. J. Radioanal. Nucl. Chem.

SC

299(2014):1351-1357.

[4] Ding D X, T an X, H u N, et a1．Removal and recovery of uranium (VI)

Biosyst. Eng. 35(2012):1567-1576．

NU

fromaqueous solutions by immobilized Aspergillusniger powder beads. Biopro.

MA

[5] Cheng W, Wang M, Yang Z, et al. The efficient enrichment of U(VI) by graphene oxide-supported chitosan. RSC Adv. 4(2014):61919-61926. [6] Nie X, Dong F, Bian L, et al. Uranium Binding on Landoltia punctata as a Result

D

of Formation of Insoluble Nano-U (VI) and U (IV) Phosphate Minerals. ACS Sustain.

PT E

Chem. Eng. 5(2017): 1494-1502.

[7] Cecal A, Humelnicu D, Rudic V, et al. Removal of uranyl ions from UO2(NO3)2,

CE

solution by means of Chlorella vulgaris, and Dunaliella salina algae. Cent. Eur. Biol. 10(2012):1669-1675.

AC

[8] Huang W, Nie X, Dong F, et al. Microscopic and Spectroscopic Insights into Uranium Phosphate Mineral Precipitated by Bacillus Mucilaginosus. ACS Earth Space Chem. 1(2017):483-492. [9] Nie X Q, Dong F Q, Liu M X, et al. Characteristics of U (VI) biosorption by biological

adsorbent

of

platanus

leaves.

J.

Spectrosc.

Spect.

Anal.

33(2013):1290-1294. [10]Sun Y, Wu Z, Wang X, et al. Macroscopic and Microscopic Investigation of U(VI) and Eu(III) Adsorption on Carbonaceous Nanofibers. Environ. Sci. Technol. 50(2016):4459-4467. 14

ACCEPTED MANUSCRIPT [11] Sun Y, Yang S, Chen Y, et al. Adsorption and Desorption of U(VI) on Functionalized Graphene Oxides: A Combined Experimental and Theoretical Study. Environ. Sci. Technol. 49(2015):4255-4262. [12] Wang T, Zheng X, Wang X, et al. Different biosorption mechanisms of Uranium(VI) by live and heat-killed Saccharomyces cerevisiae under environmentally

PT

relevant conditions. J. Environ. Radioactiv. 167(2017):92-99. [13] Wang X, Wang T, Zheng X, et al. Isotherms, thermodynamic and mechanism

RI

studies of removal of low concentration uranium (VI) by Aspergillus niger. Water Sci. and Technol. 75(2017):2727-2736.

SC

[14] Cheng W, Ding C, Wu, QY et al. Effects of Bacillus subtilis on the reduction of U(VI) by nano-Fe-0. Geochim. Cosmochim. Ac. 165(2015):86-107.

NU

[15] Huang W, Nie X, Dong F, et al. Kinetics and pH-dependent uranium

Nucl. Chem. 312(2017):531-541.

MA

bioprecipitation by Shewanella putrefaciens under aerobic conditions. J. Radioanal.

[16] Nie X, Dong F, Liu N, et al. Subcellular distribution of uranium in the roots of

D

Spirodelapunctata, and surface interactions. J. Appl. Surf. Sci. 347(2015):122-130.

PT E

[17] Krawczyk-Bärsch E, Lütke L, Moll H, et al. A spectroscopic study on U(VI) biomineralization in cultivated Pseudomonas fluorescens biofilms isolated from granitic aquifers. Environ. Sci. Pollut. R. 2(2015):4555-4565.

CE

[18] Hu B, Mei X, Li X, et al. Decontamination of U(VI) from nZVI/CNF composites investigated by batch, spectroscopic and modeling techniques. J. Mol. Liq.

AC

237(2017):1-9.

[19] Liu X, Eusterhues K, Thieme J, et al. STXM and NanoSIMS Investigations on EPS Fractions before and after Adsorption to Goethite. J. Environ. Sci. Technol. 47(2013):3158-3166. [20] Hu W, Li M, Chen T, et al. Enrichment of U(VI) on Bacillus subtilis /Fe3O4 nanocomposite. J. Mol. Liq. 258(2018):244-252. [21] Ding C, Cheng W, Nie X, et al. Reactivity of carbonized fungi supported nanoscale zero-valent iron toward U(VI) influenced by naturally occurring ions. J. Ind. 15

ACCEPTED MANUSCRIPT Eng. Chem. 61(2018):236-243. [22] Xiang S, Cheng W, Nie X, et al. Zero-valent iron-aluminum for the fast and effective U(VI) removal. J. Taiwan Inst. Chem. E. 85(2018):186-192. [23] Cheng W, Ding C, Nie X, et al. Fabrication of 3D Macroscopic Graphene Oxide Composites Supported by Montmorillonite for Efficient U(VI) Wastewater

PT

Purification. ACS Sustainable Chem. Eng. 5(2017):5503-5511. [24] Wang D, Xu Y, Yang L, et al. Synthesis of aluminum pyrophosphate for efficient

RI

sorption of U(VI). J. Mol. Liq. 258(2018):327-334.

[25] Ding C, Cheng W, Sun Y, et al. Determination of chemical affinity of graphene

SC

oxide nanosheets with radionuclides investigated by macroscopic, spectroscopic and modeling techniques. Dalton Trans. 43(2014):3888-3896.

NU

[26] Sun Y, Yang S, Sheng G, et al. The removal of U(VI) from aqueous solution by oxidized multiwalled carbon nanotubes. J. Environ. Radioactiv. 105(2012):40-47.

MA

[27] Sun Y, Li J, Wang X. The retention of uranium and europium onto sepiolite investigated by macroscopic, spectroscopic and modeling techniques. Geochim.

D

Cosmochim. Ac. 140(2014):621-643.

PT E

[28] Beltrami D, Mercierbion F, Cote G, et al. Investigation of the speciation of uranium(VI) in concentrated phosphoric acid and in synergistic extraction systems by time-resolved laser-induced fluorescence spectroscopy (TRLFS). J. Mol. Liq.

CE

190(2014):42-49.

[29] Tang P, Shen J, Hu Z, et al. High-efficient scavenging of U(VI) by magnetic

AC

Fe3O4@gelatin composite. J. Mol. Liq. 221(2016):497-506. [30] Cheng W, Jin Z, Ding C, et al. Simultaneous sorption and reduction of U(VI) on magnetite-reduced graphene oxide composites investigated by macroscopic, spectroscopic and modeling techniques. Rsc Adv. 5(2015):59677-59685. [31] Yang S, Zong P, Ren X, et al. Rapid and highly efficient preconcentration of Eu(III) by core-shell structured Fe3O4@humic acid magnetic nanoparticles. ACS Appl. Mater. Inter. 4(2012):6890-6899. [32] Wang J S, Hu X J, Liu Y G, et al. Biosorption of uranium (VI) by immobilized 16

ACCEPTED MANUSCRIPT Aspergillus fumigatus beads. J. Environ. Radioactiv. 101(2010):504-508. [33] Wei Y, Zhang L, Shen L, et al. Positively charged phosphonate-functionalized mesoporous silica for efficient uranium sorption from aqueous solution. J. Mol. Liq. 221(2016):1231-1236. [34] Nie X, Dong F, Liu M, et al. Microbially Mediated Stable Uranium Phosphate

PT

Nano-Biominerals. J. Nanosci. Nanotechno. 17(2017):6771-6780. [35] Zhao C, Liu J, Li X, et al. Biosorption and bioaccumulation behavior of uranium

RI

on Bacillus sp. dwc-2: Investigation by Box-Behenken design method. J. Mol. Liq. 221(2016):156-165.

SC

[36] Cheng W, Ding C, Sun Y, et al. The sequestration of U(VI) on functional β-cyclodextrin-attapulgite nanorods. J. Radioanal. Nucl. Chem. 302(2014):385-391.

NU

[37] Li X, Li F, Jin Y, et al. The uptake of uranium by tea wastes investigated by batch, spectroscopic and modeling techniques. J. Mol. Liq. 209(2015):413-418.

MA

[38] Sun Y, Ding C, Cheng W, et al. Simultaneous adsorption and reduction of U(VI) on reduced graphene oxide-supported nanoscale zerovalent iron. J. Hazard. Mater.

D

280(2014):399-408.

PT E

[39] Wen H, Pan Z, Giammar D E, et al. Enhanced Uranium Immobilization by Phosphate Amendment Under Variable Geochemical and Flow Conditions: Insights from Reactive Transport Modeling. J. Environ. Sci. Technol. 52(2018):5841-5850.

CE

[40] Wang J, Chen Z, Shao D, et al. Adsorption of U(VI) on bentonite in simulation

AC

environmental conditions. J. Mol. Liq. 242(2017):678-684.

17

ACCEPTED MANUSCRIPT

NU

SC

RI

PT

Figures

AC

CE

PT E

D

MA

Graphic Abstract

18

NU

SC

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

MA

Fig.1. SEM images and EDS spectra of Kocuria before (a) and after reaction with U(VI) at 4h (b), 12h (c) and 24h (d).

19

NU

SC

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

MA

Fig.2. (a) XRD spectra of Kocuria before and after reaction with U(VI) at 4h, 12h and 24h; (b) FT-IR spectra of Kocuria before and after reaction with U(VI) at 4h, 12h and 24h.

20

SC

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

MA

NU

Fig.3. Effect of contact time on U(VI) immobilization by Kocuria (a); the release of phosphate for original and uranium-interacted Kocuria (b); pH = 5.0, CU(VI) = 20 mg/L, T = 25℃.

21

MA

NU

SC

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

Fig.4. (a) shows effect of pH and ionic strength (0.001mol/L, 0.005 mol/L, 0.01 mol/L) on U(VI) removal capacity; (b) shows different species in different pH. (c) shows effect of different cations (NaCl, MgCl2,CaCl2) on U(VI) removal; (d) shows effect of different anions (NaCl, Na2CO3, NaF) on U(VI) removal, Cionic = 0.005 mol/L, CU(VI) = 20 mg/ L, t = 4h, T = 25℃.

22

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

MA

NU

SC

Fig.5. Langmuir (a) and Freundlich (b) adsorption isotherm of U(VI) on Kocuria at different temperatures (298K, 308K, 318K). pH = 5.5, CU(VI) = 20 mg/L, T = 25 ℃, t = 4h. ( ) represent the fitting curves of the Langmuir model, and (●) represent the fitting curves of the Freundlich model. Effect of U(VI) concentration (c) on the immobilization of U(VI) and adsorption capacity in different temperature (298K, 308K, 318K) of Kocuria (b). pH = 5.5, CU(VI) = 20 mg/L, T = 25℃,t = 4h.

23

NU

SC

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

PT E

D

MA

Fig.6 XPS analysis of U4f spectra (a) and O2s spectra (b) of Kocuria before and after reaction with U(VI)

24

ACCEPTED MANUSCRIPT

Table Kinetics Models

Parameters

Pseudo-order-first model k1(min-1) qe-exp(mol/g) qe-cal(mol/g) R2 pseudo-order-second model k2(g/(mol·min) qe-cal(mol/g) R2

RI SC

0.081 111.11 0.999

PT

0.001 105 101.39 0.797

AC

CE

PT E

D

MA

NU

Table.1 The adsorption rate of pseudo-first-order and pseudo-second-order for uranium interacted by Kocuria.

25

ACCEPTED MANUSCRIPT

Highlights 1. Effective U(VI) removal by Kocuria sp. 2. Fast biosorption provide nucleation sites for the precipitation to uranium biominerals.

AC

CE

PT E

D

MA

NU

SC

RI

PT

3. PO43- groups play an important role in biomineralization of U(VI).

26