Fungus hyphae-supported alumina: An efficient and reclaimable adsorbent for fluoride removal from water

Accepted Manuscript Fungus hyphae-supported alumina: An efficient and reclaimable adsorbent for fluoride removal from water Weichun Yang, Shunqi Tian, Qiongzhi Tang, Liyuan Chai, Haiying Wang PII: DOI: Reference:

S0021-9797(17)30167-4 http://dx.doi.org/10.1016/j.jcis.2017.02.015 YJCIS 22042

To appear in:

Journal of Colloid and Interface Science

Received Date: Revised Date: Accepted Date:

29 November 2016 27 January 2017 8 February 2017

Please cite this article as: W. Yang, S. Tian, Q. Tang, L. Chai, H. Wang, Fungus hyphae-supported alumina: An efficient and reclaimable adsorbent for fluoride removal from water, Journal of Colloid and Interface Science (2017), doi: http://dx.doi.org/10.1016/j.jcis.2017.02.015

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Fungus hyphae-supported alumina: an efficient and reclaimable adsorbent for fluoride removal from water Weichun Yang

a,b

, Shunqi Tian a, Qiongzhi Tang a, Liyuan Chai

a,b

,

Haiying Wang

a,b*

a

Department of Environmental Engineering, School of Metallurgy and Environment,

Central South University, Lushan South Road 932, Changsha Hunan 410017, China b

Chinese National Engineering Research Center for Control & Treatment of Heavy

Metal Pollution, Lushan South Road 932, Changsha Hunan 410017, China *

Corresponding author.

Tel.: +86 731 88830875; fax: +86 731 88710171. E-mail address:[email protected] (Haiying Wang)

1

ABSTRACT A

reclaimable

adsorbent

of

fungus

hyphae-supported

alumina(FHSA)

bio-nanocomposites was developed, characterized and applied in fluoride removal from water. This adsorbent can be fast assembled and disassemble reversibly, promising efficient reclamation and high accessible surface area for fluoride adsorption. Adsorption experiments demonstrate that the FHSA performed well over a considerable wide pH range of 3-10 with high fluoride removal efficiencies (> 66.3%). The adsorption capacity was 105.60 mg g-1 for FHSA, much higher than that for the alumina nanoparticles (50.55 mg g-1) and pure fungus hyphae (22.47 mg g-1). The adsorption capacity calculated by the pure content of alumina in the FHSA is 340.27 mg g-1 of alumina. Kinetics data reveal that the fluoride adsorption process on the FHSA was fast, nearly 90% fluoride adsorption can be achieved within 40 min. The fluoride adsorption on the FHSA is mainly due to the surface complexes formation of fluoride with ≡AlOH and the attraction between protonated -NH2 and fluoride through hydrogen bonding. Findings demonstrate that the FHSA has potential applicability in fluoride removal due to its strong fluoride adsorbility and the easy reclamation by its fast reversible assembly and disassembly feature.

Keywords: fungus hyphae-supported alumina; fluoride adsorption; fast reversible assembly; easy reclamation

2

1. Introduction Fluoride is the 13 th most abundant element in the earth’s crust and exists in almost all groundwaters around the world[1]. High concentrations of fluoride in water has been a worldwide environmental concern for decades[2,3]. Exposure to high fluoride concentrations can result in fluorosis (dental and skeletal abnormalities) or neurological damage in severe cases[4–6]. It is estimated that more than 200 million people worldwide rely on drinking water with fluoride concentrations exceeding 1.5 mg L-1, maximum contaminant level (MCL) set by World Health Organization (WHO), and more than 70 million people in 25 countries suffered from fluorosis[7]. Various methods including ion exchange[8], precipitation[9,10], membrane filtration[11], electrodialysis[12] and adsorption[13] have been studied for fluoride removal. The main disadvantage for these methods are the generation of waste, high cost, membrane degradation and fouling. Adsorption is an economical and efficient method for removing low-concentration aqueous contaminants [14–17]. Among the available adsorbents for fluoride removal, activated alumina has been extensively studied and widely used because of the high binding affinity and selectivity for fluoride [18–22]. However, activated alumina for defluoridation has considerably limited application, since individual alumina nanoparticles tend to aggregate during the operation resulting in the low adsorption capacity. Typical adsorption capacities of nano-alumina for fluoride was below 20 mg g-1[23–25] accompanied by difficult reclamation of the nanoparticles due to the small size [26,27]. Also the dispersed nanoparticles in water can enter into the environment and lead to second pollution. To solve the problems, the assembly of nanomaterials with macroscale components has attracted intensive attention. However, the formation of macrostructures could lead to a great loss of specific surface area and mass transfer efficiency, which is not totally applicable to the adsorption [28]. Generally speaking, assembly and dispersion of nanoparticles respectively provide contradict advantages for adsorption, easy recovery and high mass transfer efficiency [29]. Filamentous fungus is abundant and characterized with fast growing, low cost, easy obtained and environment-friendly. Moreover its hyphae can grow into uniform 3

long fibers, which possess microscale and macroscale features[19–20]. Recently, it has been found that filamentous fungus (e.g Aspergillus niger ) can act as a feasible matrix to carry polyaniline nanoparticles and achieve a novel hybrid structure with fast reversible macroscopic assembly and disassembly features[30]. We thus conceived that constructing a bio-nanocomposites comprising filamentous fungus and nano alumina could benefit the practical adsorption by increasing surface active areas of nano alumina coated along fungus matrix, and the easy reclaim of the bio-nanocomposites from water based on filamentous fungus with microscale and macroscale features. Moreover, the surface of fungi usually present abundant function groups such as –OH, –C=O and –NH2 groups[31], which can promote the performance of fluoride adsorption[2,32,33]. Therefore, the objective of this study were to i) develop a novel adsorbent of fungus hyphae-supported alumina (FHSA) with characteristics of high fluoride adsorption performance and easy reclamation；ii) examine the adsorption behavior of fluoride on the FHSA; iii) illustrate the predominant nature of the interactions between the adsorbent and fluoride. 2. Materials and methods 2.1 Materials Aspergillus niger was purchased from China Center for Type Culture Collection (CCTCC). Alumina nanoparticles were purchased from Aladdin Industrial Corporation (Shanghai, China). All chemicals involved in this study were of analytical grade and used as-received. The stock solution containing 1000 mg/L fluoride was prepared by dissolving certain amount of NaF into deionized water. All solutions for adsorption and analysis were freshly prepared by diluting fluoride stock solution with deionized water. 2.2 Preparation of FHSA bio-nanocomposites The fungus pellets were inoculated into potato-dextrose medium (20 g L-1) and incubated at 37 °C with shaking rate of 150 rpm for 72h. Then the fungus pellets were captured by vacuum filtration and washed by distilled water for 3 times. Afterwards, 4

the fungus hyphae were dispersed in water as storage solution for further use. The mass concentration of the fungus hyphae suspension is ~10 mg mL-1. To prepare the FHSA bio-nanocomposites, 100 mL of 0.1 M aluminum sulfate solution (pH~ 6.0) was added dropwise into the 100 mL hyphae suspension under vigorous stirring for 2 h at 70 °C, and kept stirring for 24 h at room temperature.

Afterwards, the resulting

mixture was filtered, washed with deionized water for several times. 2.3. Characterization The prepared FHSA adsorbent was characterized after 8 h vacuum freeze-drying at 30 degrees below zero. The specific surface area, pore volume and pore size of the adsorbents were investigated by a Micromeritics ASAP 2050 instrument (Micromeritics, Norcross, GA, USA) based on Bruauer-Emmett-Teller (BET) and Barrett-Joyner-Halenda (BJH) models. X-ray photoelectron spectroscopy (XPS) measurements were carried out on a Thermo Fisher Scientific K-Alpha 1063 using Al Ka X-ray as the excitation source. The binding energies were referenced to the C 1s peak at 284.6 eV. The morphology and microstructure of the as-prepared adsorbents were examined by Scanning electron microscopy (SEM, JSM6360). The function group analysis of the adsorbents was carried out using a Nicolet iS10 Fourier Transformed Infrared Spectrometer (FT-IR, Thermo Fisher Scientific Instruments, PA, USA). Spectra were recorded in the wave number range of 4000-400 cm-1 at 4 cm-1 resolution.

Thermal gravimetric and differential thermal analysis (TG-DTA) was

carried out on a STA449F3A-0488M Rigaku Thermoflex thermal analyzer with 10 °C min-1 heating rate in Ar gas. The zeta potentials of the adsorbents were measured to obtain the point of zero charge of the adsorbents by a Zetasizer apparatus (Malvern Zetasizer Nano ZS90) supplied by Malvern Instruments, Worcestershire, UK. The Al content of 16.43% in the prepared FHSA was obtained by inductively coupled plasma atomic emission spectroscopy (ICP-AES, IRIS Intrepid II XSP, Thermo) after dissolution in 6 M HCl for 24 h. 2.4 Adsorption experiments

5

For each adsorption, 15 mL of the FHSA suspension containing 0.1 g dry weight was used. The FHSA was captured by vacuum filtration and dispersed in 100 mL fluoride solution with a certain concentration. The suspension was placed in thermostatic water bath and shaken for 24 h at 25 °C. Afterwards, the suspension was filtered and the fluoride concentration in solution was detected by fluoride-selective electrode as described previously[34]. Adsorption amount of fluoride adsorbed was calculated from the measured aqueous concentration according to mass balance. The effect of solution pH on fluoride adsorption was performed with the initial pH values from 2-12 and an initial fluoride concentrations of 50 mg/L. Adjustment of solution pH were made with either HCl or NaOH solution. The fluoride adsorption isotherms were studied with initial fluoride concentrations range of 5 -180 mg L-1 at pH 6.0. Adsorption kinetic experiments were carried out by batch experiment at pH 4.5 with various fluoride concentrations (5, 9, 28 and 98 mg L-1). The effect of ଶି ି co-existing anions including NOି , Brି and POଷି on fluoride ଷ , Cl , SOସ ସ

adsorption was examined by performing fluoride adsorption under a fixed initial co-anions concentration (2 mmol L-1), and an initial fluoride concentration of 20 mg L-1 at pH 7.0. All adsorption experiments were carried out in duplicate to obtain reproducible results with an error of less than 5%. For comparison, the pure fungus hyphae and alumina nanoparticles used for fluoride adsorption were investigated at selected experiments following the same procedures described above. To explore the regeneration and reuse, the FHSA was added into the 20 mg L-1 fluoride solution following the adsorption experiment. Afterwards the FHSA was assembled by vacuum filtration, and disassembled in 100 ml 0.005 M NaOH solution under stirring for 2 h for regeneration. The obtained FHSA was used for the next adsorption or reuse cycle. 3. Results and discussion 3.1. Characterization of the adsorbents Fig.1 shows the morphology and microstructure of the pure fungus hyphae and FHSA. The pure fungus hyphae are composed of column-like microfibers with the 6

size of around 3 µm and the length of more than 150 µm. The surface of the pure fungus hyphae is relatively smooth compared to the rough outside surface after their attachment of alumina. More interestingly, the FHSA can be assembled into a free-standing film by a simple vacuum filtration within 10 s, and the assembled film can be fast disassembled and dispersed in water just by shaking manually (Fig. 1c). That is to say, the well-dispersed FHSA in aqueous solution allows high accessible surface area, which will be beneficial to fluoride adsorption, meanwhile the FHSA can be easily reclaimed after fluoride adsorption. Thus, this interesting feature of fast macroscopic assembly and disassembly for the FHSA will be important to promote its practical applications in fluoride adsorption. a

b

4 µm

5 µm

c

Assembly (10s)

Disassembly(10s)

Fig.1. SEM images of (a) the pure fungus hyphae and (b) FHSA; (c) The performance of the fast reversible macroscopic assembly and disassembly of the FHSA 7

Table 1 presents the surface atomic ratio (at%) of elements for the pure fungus hyphae and FHSA. For the pure fungus hyphae, the content of C, O and N is 69.62%, 26.23% and 3.57%, respectively. After the decoration of nano alumina, the content of C reduced significantly, while the content of O increased to 55.77%, and Al atom was present on the surface with the content of 16.73%, demonstrating the coexistence of fungus hyphae and alumina on the surface of the as-prepared FHSA adsorbent. Table 1 Surface elemental composition, surface area and pore volume parameters for the pure fungus hyphae and FHSA Surface elemental composition a SBETb (m2g-1) Average pore Total pore volume c diameter (nm) (cm3g-1) C% O% N% Al% Pure fungus hyphae 69.62 26.23 3.57% 7.49 6.27 0.012 Nano alumina 16.76 26.99 0.083 FHSA 22.33 55.77 0.73 16.73 73.43 18.06 0.33 a Note: Determined by X-ray photoelectron spectroscopy (XPS) b Determined by N2 adsorption using the Brunauer-Emmett-Teller (BET) method c Total pore volume, determined at P/P0= 0.985 Adsorbents

The surface area and pore size distribution of the pure fungus hyphae and FHSA were determined by N2 adsorption-desorption measurements(Table 1). The BET surface area and total pore volume were 7.49 m2 g-1 and 0.012 cm3g-1 for the pure fungus hyphae, 16.76 m2g-1 and 0.083 cm3g-1 for nano alumina, and 73.43 m2g-1 and 0.33 cm3g-1 for the FHSA, respectively. The significant increase in BET surface area and total pore volume for the FHSA might be due to the reduced aggregation of alumina particles by virtue of the dispersive effect of the fungus hyphae. The N2 adsorption–desorption isotherms for pure fungus hyphae, nano alumina and FHSA are shown in Fig. 2. According to the IUPAC classification, all three adsorbents exhibit type IV isotherm plot with H1-type hysteresis loop. The pores of the FHSA are mainly distributed in the range of 10-40 nm, indicating the predominance of mesopores in the internal structures of the FHSA.

8

4

0.004

3

6

dV(d) (cm nm g

3 -1

Adorbed volume(cm g )

-1 -1

)

0.006

0.002 0.000

8 0

40

80

Pore diameter (nm)

2

120

a

60

-1

40

3

3 -1 Adsorbed volume (cm g )

-1

dV/d(cm nm g )

0.004

0.002

0.000 0

20

20

40

60

80

100

Pore diameter (nm)

b

0 0.0

0.2

0.4

0.6

0.8

1.0

Relative pressure (P/P0)

240

160

3

-1 -1

dV(d)(cm nm g )

3 -1

Adorbed volume(cm g )

0.010

0.005

0.000

80

0

20 40 Pore diameter (nm)

60

80

c

0 0.0

0.2

0.4

0.6

0.8

1.0

Relative pressure(P/P0)

Fig. 2. N2 adsorption-desorption isotherms and BJH pore size distribution (inset) of (a)the pure fungus hyphae, (b) alumina nanoparticles and (c) FHSA The FT-IR spectra of the pure fungus and FHSA are shown in Fig. S1 (Supplementary Material). For the pure fungus hyphae, the sharp peaks at 2925 and 2854 cm-1 are attributed to lipids[35]. The peaks between 1700-1300 cm-1 can be 9

assigned to the amide of proteins and chitin[36]. The peaks at 1150 and 1042 cm−1 are typical adsorption peaks of polysaccharides. The band at 3384 cm-1 can be assigned to -OH stretching bond of hydroxyl groups from physically adsorbed watermolecules[37]. After the decoration of nano alumina, the band at 3384 cm-1 broadened and its intensity significantly increased, demonstrating an increased amount of hydroxyl groups. This could be result from Al-OH on the FHSA adsorbent. The zeta potentials of the pure fungus hyphae and FHSA were measured at varied pH (Fig. S2, Supplementary Material). The point of zero charge (PZC) was 3.4 and 8.5 for the pure fungus hyphae and FHSA, respectively.

The pHPZC of the FHSA

is higher than most of adsorbents for fluoride removal reported in literature[38]. The high pHPZC indicates that FHSA can be positively charged at typical environmental pHs, which benefits the adsorption of negatively charged anions. The X-ray diffraction pattern of the FHSA (Fig.S3, Supplementary Material) implies its amorphous nature with the absence of peaks. In TG-DTA-DTG curves of the FHSA (Fig.S4, Supplementary Material), the weight loss in 50-200°C was mainly caused by the loss of water molecules in the sample[39]. When temperature increased further (up to 844°C), the weight loss could be due to the thermal decomposition of fungus hyphae. The overall mass losses amount was up to 65%, leaving alumina as residue of decomposition. 3.2 The pH effect on fluoride removal The effect of solution pH on fluoride removal was examined and the results are shown in Fig.3a. The FHSA exhibited a considerably high fluoride removal efficiencies(greater than 66.3%) over a relatively wide pH range of 3-10. However, the fluoride removal efficiencies of the pure fungus hyphae were very low (below 10%) over the investigated pH range. This demonstrated that the adsorption performance of the FHSA was significant prior to that of the pure fungus hyphae, indicating that the anchored alumina play a major role in fluoride adsorption by the FHSA. The relatively wide optimum adsorption pH for the FHSA can be explained by its 10

high pHPZC (8.5). It means that the surface of the FHSA is positive at pH below 8.5 and can attract the negatively charged fluoride ions[40]. On the contrary, when the pH values were above 8.5, electrostatic repulsion occurs between the negatively charged surface and fluoride ions, and also much more hydroxyl ions compete with fluoride ions for occupation of adsorption sites[25], leading to a decrease in fluoride removal. The equilibrium pH values decreased when initial pH was larger than 7.0 as shown in Fig.3b, and this can be attributed to the adsorption of hydroxyl ions by the adsorbent. Similar phenomenon has also been observed by Jia et al[41]. In addition, the deceased fluoride removal efficiency in pH range 2.0-4.0 might be due to the formation of weakly ionized hydrofluoric acid[23]. 3.3 Adsorption isotherm The fluoride adsorption isotherms of the FHSA, alumina nanoparticles and pure fungus hyphae are shown in Fig.3c. The Langmuir and Freundlich models were used to fit the adsorption isotherms and the parameters are summarized in Table 2. According to the correlation coefficients (R2), the Langmuir model is more fit to describe the adsorption isotherms than the Freundlich model. The adsorption capacity calculated based on Langmuir model for the FHSA, alumina nanoparticles and pure fungus hyphae was 105.60, 50.55 and 22.47 mg g-1, respectively. The FHSA exhibited much higher fluoride adsorption capacity, confirming that attached-alumina rather than fungus hyphae made the primary contributions in the fluoride adsorption. The superior fluoride adsorption performance of the FHSA was mainly due to the high assessable surface area of alumina , since the direct use of pure alumina nanoparticles is easily to agglomerate. It could be noted that the adsorption capacity calculated based on the content of alumina in the FHSA was estimated to be 340.27 mg F g-1 of alumina, which was much higher than the previously reported nano-alumina(the reported typical values <20 mg g-1)[22,23]. That is to say, the utilization efficiency for alumina was improved greatly by the incorporation of fungus hyphae compared with the unsupported alumina nanoparticles.

100

12

80

60

um pH

l efficiency (%)

11

8

FHSA pure fungus hyphae

a

b

120

100

c qe (mg/g)

80 FHSA alumina nanoparticles pure fungus hyphae

60

40

20

0 0

50

100

150

200

Ce (mg/L)

Fig.3.

(a) Effect of pH on fluoride removal efficiency by the pure fungus hyphae

and FHSA; (b) The change of the pH values after fluoride adsorption; (c) The fluoride adsorption isotherms on FHSA, alumina nanoparticles and pure fungus hyphae fitted by Langmuir model.

Table 2 Langmuir and Freundlich parameters for fluoride adsorption on the FHSA, alumina nanoparticles and pure fungus hyphae Adsorbents

Langmuir

Freundlich q ୣ=KFCe1/n

q bCe qe = max 1 + bCe

qmax

b

R2 12

KF

n

R2

FHSA Alumina nanoparticles Pure fungus hyphae

105.60

0.089

0.981

17.00

2.65

0.923

50.55

0.009

0.985

1.543

1.69

0.984

22.47

0.014

0.995

1.12

1.91

0.978

Note: Ce (mg L-1) and qe (mg g-1) are the equilibrium fluoride concentrations in the aqueous and solid phase, respectively; q max is the maximum fluoride adsorption capacity (mg g-1); b is the affinity coefficients (L mg-1); KF and n are Freundlich constants related to relative adsorption capacity and adsorption intensity, respectively; R2 is correlation coefficient.

In addition, from the performance comparison between the FHSA and various adsorbents for fluoride adsorption (Table 3), the adsorption capacity of the FHSA is superior to most other adsorbents reported in the literature. Table 3 Comparison of fluoride adsorption capacity of the FHSA to other adsorbents Adsorbent

Adsorption capacity (mg g-1)

pH

Reference

Lanthanum-loaded magnetic cationic hydrogel Zirconium−carbon hybrid Sorbent iron-aluminium oxide-graphene oxide Fe3O4@n-HApCS Iron–aluminum oxide/graphene oxide nanoparticles bayerite/boehmite nanocomposites Al-doping chitosan–Fe(III) hydrogel Zr(IV) loaded cross-linked seaweed Al-O(OH) incorporated graphene oxide zirconium metal-organic frameworks Ag NP-coated chitosan−sodium alginate based bionanomaterial scaffolds FHSA

136.78

7.0

[2]

17.70 22.13–27.8 4.77 64.72

7.0 7.0 neutral pH 6.5

[4] [13] [43] [44]

56.80 31.2 16.15 51.41 102.40 60

7.0 5.0 5.0 6.5–7.5 7.0 7.0

[45] [33] [46] [47] [48] [49]

105.60 (340.27mg g-1 of alumina)

6.0

This study

3.4 Adsorption kinetics Fig.4 shows adsorption kinetics on the FHSA. Nearly 90% fluoride was removed in the initial 40 min. The fast adsorption at initial stage could be attributed to the specific adsorption of fluoride ions by the anchored alumina on the FHSA[50]. 13

Different kinetic models including pseudo-first-order, pseudo-second-order and Elovich models have been employed to describe the kinetic results of fluoride adsorption on the FHSA. The fit of the three models to the fluoride adsorption kinetic data are shown in Fig. 4b,c and d, and the model parameters obtained by curve-fitting kinetic data are listed in Table 4. Among these models, the pseudo-second-order model was more applicable in describing the adsorption kinetics of fluoride on the FHSA based on the highest correlation coefficient (R2) (R2> 0.996) (Table 4), indicating the chemical reaction was the rate-controlling step for fluoride adsorption on FHSA[34]. 80

2.0 b

a 60

1.0 5 mg/L 9 mg/L 28 mg/L 98 mg/L

40

log (qe-qt )

qt (mg/g)

5 mg/L 9 mg/L 28 mg/L 98 mg/L

1.5

.5 0.0 -.5

20

-1.0 0

-1.5 0

200

400

600

800

0

200

400

t (min)

250

800

80

c

d

200

5 mg/L 9 mg/L 28 mg/L 98 mg/L

150

60

qt (mg/g)

t/qt (min.g/mg)

600

t (min)

100

5 mg/L 9 mg/L 28 mg/L 98 mg/L

40

20

50

0

0 0

200

400

600

800

1

2

3

4

5

6

ln t Fig.4. (a) Effect t (min) of reaction time on fluoride adsorption on the FHSA; kinetics

modeling

of

fluoride

adsorption

(b)

pseudo-first-order

kinetic

plots;

(c)

pseudo-second-order kinetic plots; (d) Elovich model plots. t is the reaction time 14

7

(min), q e (mg g-1) and qt (mg g-1) are the amount of adsorbed fluoride at equilibrium and at any reaction time t.

Table 4 Kinetic and statistical parameters of the three kinetic models Data set

Pseudo-first-order model logሺqୣ − q୲ ሻ = logqୣ −

Pseudo-second-order model

Elovich model

t 1 1 = + t q୲ k ଶ qଶୣ qୣ

q୲ = βln ሺαβሻ+ βlnt

kଵ t 2.303

R2

qe,

k1

R2

5mg/L

0.86

1.9 × 10-3

0.894

3.20

3.04 × 10-2

0.997

8.97 × 108

0.12

0.785

9mg/L

1.12

3.3 × 10-3

0.956

6.36

1.57 × 10-1

1.000

9.48 × 107

0.27

0.964

28mg/L

4.96

3.4 × 10-3

0.860

24.24

6.5 × 10-3

1.000

1.87 × 104

1.47

0.962

98mg/L

20.73

2.9 × 10-3

0.903

68.45

1.4 × 10-3

0.999

4.14 × 102

4.79

0.946

qe

k2

-1

α

R2

β

-1

Note: t is the reaction time (min), qe (mg g ) and qt (mg g ) are the amount of adsorbed fluoride at equilibrium and at any reaction time t, k1(min-1) and k2 (g·mg-1 min-1) are the equilibrium rate constants for pseudo-first-order and pseudo-second-order models respectively, and the Elovich constant α is related to the sorption rate while β is related to the surface coverage, R2 is correlation coefficient.

3.5

Effect of coexisting anions ଶି ି ି The effect of coexisting anions including NOି and POଷି ଷ , Cl , SOସ , Br ସ , on

fluoride adsorption by the FHSA are examined. As shown in Fig.5,

it could be found

ଶି ି that the effect of NOି and Brି was not obvious, while POଷି ଷ , Cl , SOସ ସ

noticeably interferes with fluoride. In general, the fluoride removal efficiencies in the ଶି ଷି ି ି presence of anions decreased in the following order: NOି ଷ

Similar phenomenon has been observed in the literature for fluoride adsorption [53]. ଶି The Z/r (charge/radius) values of the anions varies in the order POଷି ସ (3/3.40)> SOସ

(2/2.40) >Clି (1/1.81)> Br ି (1/1.95)> NOି ଷ (1/2.81). The higher the Z/r is, the affinity between the adsorbent surface and the anion is greater, and consequently the influence of the anion on fluoride adsorption is more significant.

125

l efficiency(%)

15

100

75

Fig.5. Effect of co-existing anions on fluoride removal by the FHSA

3.6 The stability and Regeneration of FHSA The stability of the FHSA was tested by monitoring Al leaching concentration in the pH range 4-9, and the results are provided in Fig.S6. The leached Al concentrations were relatively high in both acid and base, while alumina from the FHSA was dissolved the least in the pH range of 5-7. This demonstrates that the FHSA is stable in this pH range. The uptake/release process for fluoride from the FHSA was also reversible. The relationship between adsorption-regeneration cycles and fluoride removal efficiency for the FHSA is presented in Fig.6. It was found that the FHSA still possessed strong adsorption ability after 4 adsorption-regeneration cycles, and the fluoride removal efficiency remained 89.5%. Such a highly efficient uptake and release of fluoride from the FHSA should be associated with its feature of the highly reversible assembly and disassembly. Clearly, the excellent regeneration and reusability capacity make the FHSA perform superiorly in the fluoride removal from water.

16

Fluoride removal efficiency (%)

100

80

60

40

20

0 1

2

3

4

Number of cycles

Fig.6. Recycling behavior of the FHSA in fluoride adsorption

3.7 Groundwater trial To assess the practicality, the FHSA was tested for fluoride removal in a fluoride-spiked (5 mgL-1) groundwater from Changsha, Hunan, China. Table 4 presents the water quality parameters before and after the FHSA-treatment. It was observed that the FHSA could reduce the fluoride concentration to 0.83 mg L-1, below WHO MCL of 1.5 mgL-1. Also there is a significant reduction in the levels of other water quality parameters, such as SO42- and Cl- concentrations. The groundwater trial demonstrates that the FHSA can be effectively employed for fluoride removal from water.

Table 5 Parameters of water before and after the FHSA-treatment (volume of water: 500 ml, FHSA dose: 1.0 g L-1, contact time: 24 h) Parameters

Untreated sample

Treated with FHSA

pH

7.89

7.54

Total organic carbon (mg L-1)

9.23

2.41

F- (mg L-1)

5.41

0.83 17

-1

SO42- (mg L ) -1

Cl- (mg L ) -1

Ca2+ (mg L )

32.76

10.34

100.62

24.67

60

56

3.8. XPS analyses To find out the main mechanism of fluoride adsorption by the FHSA, XPS was applied to study the surface chemical compositions of the adsorbent before and after adsorption, and the results are presented in Fig.7. Composition content relative to the total content of corresponding element was calculated from the peak area. The appearance of the F 1s peak in the XPS wide scan spectrum after adsorption (Fig.7a) indicated the fluoride has been successfully adsorbed. The XPS spectrum of the C 1s (Fig. 7b) comprised four peaks with differentiated binding energy values of 284.6, 286.0, 287.5 and 288.6 eV, which can be assigned to C-C,C-OH, O=C-N and O=C-O species, respectively. After adsorption, the content of O=C-N decreased from 11.17% to 4.43%, implying that the O=C-N function group is active site for fluoride adsorption. In Fig.7c , the O 1s spectrum can be well-resolved into two components, including C=O (531.83 eV), O-C-O or Al-OH (532.4 eV). After fluoride adsorption, the content of O-C-O or Al-OH (532.4 eV) decreased from 80.65% to 67.11%, and also the binding energy value of Al 2p was shifted from 74.64 to 74.47 eV (Fig.7d), confirming that the Al-OH groups might be involved in the adsorption process. The binding energy of F 1s in FHSA was 685.12 eV(Fig.7e), indicating that the fluoride phase on the adsorbent could be assigned to O-Al-F[52]. Based on above discussion, the possible mechanism of fluoride adsorption onto the FHSA is proposed and described as follow: (1) fluoride ions form surface complexes with ≡AlOH; (2) the protonated -NH2 groups on the surface attract fluoride ions through hydrogen bonding.

4. Conclusions The FHSA bio-nanocomposites as an efficient adsorbent for fluoride removal was developed in the present study. This adsorbent can be effectively assembled into a 18

film by filtration and disassembled in water just by shaking manually within 10 s, therefore allowing easy reclamation of the adsorbent and high assessable surface area to the fluoride in adsorption application. The calculated adsorption capacity of the FHSA was much higher than that of the pure fungus hyphae and alumina nanoparticles. More importantly, the utilization efficiency of alumina for fluoride adsorption was improved greatly by the incorporation of fungus hyphae. The recycling results confirmed that the FHSA has the excellent regeneration and reusability capacity. The XPS spectra illustrated both ≡AlOH and protonated -NH2 groups on the FHSA contribute to the fluoride adsorption through surface complexation and hydrogen bonding, respectively. Results demonstrated the potential applicability of this FHSA in fluoride adsorption due to its high adsorption ability, efficient reclamation, simple synthesis procedure and excellent regeneration performance. The present study provided an environment-friendly, economical and simple strategy for synthesizing an efficient reclaimable bio-nanocomposite.

19

O1s

a

( C-C 54.35%)

67.11 % (C-OHor Al-OH)

b

( C-OH 33.70%)

(C=O 32.89 %)

(O =C-N 5.43%)

F1s C1s Al2p O1s

Before adsorption

(O =C-O 6.52%)

( C-OH30.32 %)

( C-C 53.19%)

(O =C-N 11.17%) (O =C-O 5.32%)

C1s

Before adsorption

Al2p

1200

1000

800

600

400

200

0

292

290

Binding Energy(eV)

288

286

284

282

280

Before adsorption

536

534

(C=O 19.35 %)

532

530

528

Intensity(a.u.)

0.17eV

80.65 % (C-OH or Al-OH )

e

F1s

Al 2p

After adsorption

Binding Energy(eV)

Binding Energy(eV) d

Intensity(a.u.)

Intensity(a.u.)

After adsorption Intensity(a.u.)

Intensity(a.u.)

After adsorption

c

After adsorption

Before adsorption

80

75 Binding Energy(ev)

70

700

695

690

685

680

675

Binding Energy(ev)

Fig.7. (a) XPS survey spectra, (b) C 1s , (c) O 1s and (d) Al 2p of the FHSA before and after fluoride adsorption and (e) F 1s for the FHSA bio-nanocomposites after adsorption. 20

Acknowledgement This research is financially supported by the Changjiang Scholars Program of Ministry of Education of China-Distinguished Professor (T2011116) and the National Natural Science Foundation of China (Grant 51304252, Grant 51374237) .

Appendix A. Supplementary data Fig.S1 shows FT-IR spectra of (a)the pure fungus hyphae and (b) FHSA . Fig.S2 shows the zeta potentials of the FHSA and pure fungus hyphae at varied pH. Fig.S3 shows XRD pattern of the FHSA. Fig.S4 shows TG-DTA-DTG curves of the FHSA. Fig.S5 shows Al concentrations in solution for the FHSA at various pH.

REFERENCES [1]

[2]

[3]

[4]

[5]

[6]

[7]

W. Tang, P. Kovalsky, D. He, T.D. Waite, Fluoride and nitrate removal from brackish groundwaters by batch-mode capacitive deionization, Water Res. 84 (2015) 342–349. doi:10.1016/j.watres.2015.08.012. S. Dong, Y. Wang, Characterization and adsorption properties of a lanthanum-loaded magnetic cationic hydrogel composite for fluoride removal, Water Res. 88 (2016) 852–860. doi:10.1016/j.watres.2015.11.013. J. Zhu, X. Lin, P. Wu, Q. Zhou, X. Luo, Fluoride removal from aqueous solution by Al ( III )– Zr ( IV ) binary oxide adsorbent, Appl. Surf. Sci. 357 (2015) 91–100. doi:10.1016/j.apsusc.2015.09.012. L.H. Velazquez-jimenez, R.H. Hurt, J. Matos, J.R. Rangel-mendez, Zirconium − Carbon Hybrid Sorbent for Removal of Fluoride from Water : Oxalic Acid Mediated Zr ( IV ) Assembly and Adsorption Mechanism, Environ. Sci. Technol. 48 (2014) 1166–1174. V.-J.L. Halla, V.-A. Esmeralda, F.-A.J. Luis, F.-Z. Horacio, R.-M.J. Rene, Water defluoridation with special emphasis on adsorbents-containing metal oxides and/or hydroxides: a review, Sep. Purif. Technol. 150 (2015) 292–307. doi:10.1016/j.seppur.2015.07.006. S. Jagtap, M.K. Yenkie, N. Labhsetwar, S. Rayalu, Fluoride in drinking water and defluoridation of water, Chem. Rev. 112 (2012) 2454–2466. doi:10.1021/cr2002855. A. Ghosh, K. Mukherjee, S.K. Ghosh, B. Saha, Sources and toxicity of fluoride in the environment, Res. Chem. Intermed. 39 (2013) 2881–2915. doi:10.1007/s11164-012-0841-1.

21

[8]

[9]

[10]

[11]

[12]

[13]

[14]

[15]

[16]

[17] [18]

[19]

[20]

Q. Li, B. Wang, W. Li, C. Wang, Q. Zhou, C. Shuang, et al., Performance evaluation of magnetic anion exchange resin removing fluoride, 91 (2016) 1747–1754. doi:10.1002/jctb.4764. K. Jiang, K. Zhou, Y. Yang, H. Du, A pilot-scale study of cryolite precipitation from high fluoride-containing wastewater in a reaction-separation integrated reactor, J. Environ. Sci. (China). 25 (2013) 1331–1337. doi:10.1016/S1001-0742(12)60204-6. K. Jiang, K.G. Zhou, Y.C. Yang, H. Du, Growth kinetics of calcium fluoride at high supersaturation in a fluidized bed reactor., Environ. Technol. 35 (2014) 82–88. doi:10.1080/09593330.2013.811542. A. Boubakri, R. Bouchrit, A. Hafiane, S. Al-Tahar Bouguecha, Fluoride removal from aqueous solution by direct contact membrane distillation: Theoretical and experimental studies, Environ. Sci. Pollut. Res. 21 (2014) 10493–10501. doi:10.1007/s11356-014-2858-z. N. Arahmana, S. Mulyatia, M.R. Lubisa, R. Takagib, H. Matsuyamab, The removal of fluoride from water based on applied current and membrane types in electrodialyis, J. Fluor. Chem. 191 (2016) 97–102. S. Kanrar, S. Debnath, P. De, K. Parashar, K. Pillay, P. Sasikumar, et al., Preparation, characterization and evaluation of fluoride adsorption efficiency from water of iron-aluminium oxide-graphene oxide composite material, Chem. Eng. J. 306 (2016) 269–279. doi:10.1016/j.cej.2016.07.037. C.M. Kanno, R.L. Sanders, S.M. Flynn, G. Lessard, S.C.B. Myneni, Novel apatite-based sorbent for defluoridation: Synthesis and sorption characteristics of nano-micro-crystalline hydroxyapatite-coated-limestone, Environ. Sci. Technol. 48 (2014) 5798–5807. doi:10.1021/es405135r. B. Pan, J. Xu, B. Wu, Z. Li, X. Liu, Enhanced removal of fluoride by polystyrene anion exchanger supported hydrous zirconium oxide nanoparticles, Environ. Sci. Technol. 47 (2013) 9347–9354. doi:10.1021/es401710q. S. Wu, K. Zhang, J. He, X. Cai, K. Chen, Y. Li, et al., High efficient removal of fluoride from aqueous solution by a novel hydroxyl aluminum oxalate adsorbent., J. Colloid Interface Sci. 464 (2016) 238–45. doi:10.1016/j.jcis.2015.10.045. A. Flanagan, S.Q. Road, A Review on Adsorption of Fluoride from Aqueous Solution, Materials (Basel). 7 (2014) 6317–6366. doi:10.3390/ma7096317. N.A. Oladoja, B. Helmreich, Batch defluoridation appraisal of aluminium oxide infused diatomaceous earth, Chem. Eng. J. 258 (2014) 51–61. doi:10.1016/j.cej.2014.07.070. D. Dayananda, V.R. Sarva, S. V. Prasad, J. Arunachalam, N.N. Ghosh, Preparation of CaO loaded mesoporous Al2O3: Efficient adsorbent for fluoride removal from water, Chem. Eng. J. 248 (2014) 430–439. doi:10.1016/j.cej.2014.03.064. C. Yang, L. Gao, Y. Wang, X. Tian, S. Komarneni, Fluoride removal by ordered and disordered mesoporous aluminas, Microporous Mesoporous Mater. 197 (2014) 156–163. doi:10.1016/j.micromeso.2014.06.010. 22

[21] M. Li, Z. Si, X. Wu, D. Weng, F. Kang, Facile synthesis of hierarchical porous γ-Al2O3 hollow microspheres for water treatment, J. Colloid Interface Sci. 417 (2014) 369–378. doi:10.1016/j.jcis.2013.11.071. [22] L.A. Avinash Chunduri, T.M. Rattan, M. Molli, V. Kamisetti, Single step preparation of nano size gamma alumina exhibiting enhanced fluoride adsorption, Mater. Express. 4 (2014) 235–241. [23] E. Kumar, A. Bhatnagar, U. Kumar, M. Sillanpää, Defluoridation from aqueous solutions by nano-alumina: Characterization and sorption studies, J. Hazard. Mater. 186 (2011) 1042–1049. doi:10.1016/j.jhazmat.2010.11.102. [24] L.A.A. Chunduri, T.M. Rattan, M. Molli, V. Kamisetti, Single step preparation of nano size gamma alumina exhibiting enhanced fluoride adsorption, Mater. Express. 4 (2014) 235–241. [25] S. Tangsir, L. Divband, A. Lähde, M. Maljanen, A. Hooshmand, A. Ali, et al., Water defluoridation using Al 2 O 3 nanoparticles synthesized by flame spray pyrolysis ( FSP ) method, Chem. Eng. J. 288 (2016) 198–206. doi:10.1016/j.cej.2015.11.097. [26] Z. Liu, L. Chen, L. Zhang, S. Poyraz, Z. Guo, X. Zhang, et al., Ultrafast Cr ( VI ) removal from polluted water by microwave synthesized iron oxide submicron, Chem. Commun. (2014) 8036–8039. doi:10.1039/c4cc02517b. [27] H. Liang, X. Cao, W. Zhang, H. Lin, F. Zhou, L. Chen, et al., Robust and Highly Efficient Free-Standing Carbonaceous Nanofiber Membranes for Water Purification, Adv. Funct. Mater. 21 (2011) 3851–3858. [28] M.-R. Huang, H.-J. Lu, W.-D. Song, X.-G. Li, Dynamic Reversible Adsorption and Desorption of Lead Ions Through a Packed Column of Poly( m -phenylenediamine) Spheroids, Soft Mater. 8 (2010) 149–163. doi:10.1080/15394451003756316. [29] Y. Zhang, Z. Zhou, Y. Shen, Q. Zhou, J. Wang, A. Liu, et al., Reversible Assembly of Graphitic Carbon Nitride 3D Network for Highly Selective Dyes Absorption and Regeneration, ACS Nano. (2016) acsnano.6b05488. doi:10.1021/acsnano.6b05488. [30] H. Wang, X. Li, L. Chai, L. Zhang, Nano-functionalized filamentous fungus hyphae with fast reversible macroscopic assembly & disassembly features. TL - 51, Chem. Commun. (Camb). 51 (2015) 8524–8527. doi:10.1039/C5CC00871A. [31] W. Cheng, C. Ding, Y. Sun, X. Wang, Fabrication of fungus / attapulgite composites and their removal of U ( VI ) from aqueous solution, Chem. Eng. J. 269 (2015) 1–8. doi:10.1016/j.cej.2015.01.096. [32] L. Chen, S. He, B. He, T. Wang, C. Su, C. Zhang, et al., Synthesis of Iron-Doped Titanium Oxide Nanoadsorbent and Its Adsorption Characteristics for Fluoride in Drinking Water, Ind. Eng. Chem. Res. (2012). [33] J. Ma, Y. Shen, C. Shen, Y. Wen, W. Liu, Al-doping chitosan – Fe ( III ) hydrogel for the removal of fluoride from aqueous solutions, Chem. Eng. J. 248 (2014) 98–106. doi:10.1016/j.cej.2014.02.098.

23

[34] L. Chai, Y. Wang, N. Zhao, W. Yang, X. You, Sulfate-doped Fe3O4/Al2O3 nanoparticles as a novel adsorbent for fluoride removal from drinking water, Water Res. 47 (2013) 4040–4049. doi:10.1016/j.watres.2013.02.057. [35] L. Zhang, Y. Wang, B. Peng, W. Yu, H. Wang, Preparation of a macroscopic, robust carbon-fiber monolith from filamentous fungi and its application in Li–S batteries, Green Chem. 16 (2014) 3926–3934. doi:10.1039/c4gc00761a. [36] G. Fischer, S. Braun, R. Thissen, W. Dott, FT-IR spectroscopy as a tool for rapid identification and intra-species characterization of airborne filamentous fungi, J. Microbiol. Methods. 64 (2006) 63–77. doi:10.1016/j.mimet.2005.04.005. [37] W. Yang, Q. Tang, J. Wei, Y. Ran, L. Chai, H. Wang, Enhanced removal of Cd(II) and Pb(II) by composites of mesoporous carbon stabilized alumina, Appl. Surf. Sci. 369 (2016) 215–223. doi:10.1016/j.apsusc.2016.01.151. [38] A. Bhatnagar, E. Kumar, M. Sillanpää, Fluoride removal from water by adsorption — A review, Chem. Eng. J. 171 (2011) 811–840. doi:10.1016/j.cej.2011.05.028. [39] H.T. Fan, J.B. Wu, X.L. Fan, D.S. Zhang, Z.J. Su, F. Yan, et al., Removal of cadmium(II) and lead(II) from aqueous solution using sulfur-functionalized silica prepared by hydrothermal-assisted grafting method, Chem. Eng. J. 198–199 (2012) 355–363. doi:10.1016/j.cej.2012.05.109. [40] C. Ding, W. Cheng, Y. Sun, X. Wang, Novel fungus-Fe3O4 bio-nanocomposites as high performance adsorbents for the removal of radionuclides, J. Hazard. Mater. 295 (2015) 127–137. doi:10.1016/j.jhazmat.2015.04.032. [41] Y. Jia, B.-S. Zhu, K.-S. Zhang, Z. Jin, B. Sun, T. Luo, et al., Porous 2-line ferrihydrite/bayerite composites (LFBC): Fluoride removal performance and mechanism, Chem. Eng. J. 268 (2015) 325–336. doi:10.1016/j.cej.2015.01.080. [42] E. Kumar, A. Bhatnagar, W. Hogland, M. Marques, M. Sillanpää, Interaction of anionic pollutants with Al-based adsorbents in aqueous media – A review, Chem. Eng. J. 241 (2014) 443–456. doi:10.1016/j.cej.2013.10.065. [43] K. Pandi, N. Viswanathan, Synthesis and applications of eco-magnetic nano-hydroxyapatite chitosan composite for enhanced fluoride sorption, Carbohydr. Polym. 134 (2015) 732–739. doi:10.1016/j.carbpol.2015.08.003. [44] L. Liu, Z. Cui, Q. Ma, W. Cui, X. Zhang, One-step synthesis of magnetic iron-aluminum oxide / graphene oxide nanoparticles as a selective adsorbent for fl uoride removal from aqueous solution, RSC Adv. 6 (2016) 10783–10791. doi:10.1039/C5RA23676B. [45] Y. Jia, B. Zhu, Z. Jin, B. Sun, T. Luo, X. Yu, et al., Fluoride removal mechanism of bayerite / boehmite nanocomposites : Roles of the surface hydroxyl groups and the nitrate anions, J. Colloid Interface Sci. 440 (2015) 60–67. doi:10.1016/j.jcis.2014.10.069. [46] H. Paudyal, B. Pangeni, K. Inoue, H. Kawakita, K. Ohto, K. Nath, et al., Preparation of novel alginate based anion exchanger from Ulva japonica and its

24

[47]

[48]

[49]

[50]

[51]

[52]

application for the removal of trace concentrations of fluoride from water, Bioresour. Technol. 148 (2013) 221–227. doi:10.1016/j.biortech.2013.08.116. M. Barathi, a. S. Krishna Kumar, C.U. Kumar, N. Rajesh, Graphene oxide–aluminium oxyhydroxide interaction and its application for the effective adsorption of fluoride, RSC Adv. 4 (2014) 53711–53721. doi:10.1039/C4RA10006A. J. He, X. Cai, K. Chen, Y. Li, K. Zhang, Z. Jin, et al., Performance of a novelly-defined zirconium metal-organic frameworks adsorption membrane in fluoride removal, J. Colloid Interface Sci. 484 (2016) 162–172. doi:10.1016/j.jcis.2016.08.074. A. Kumar, P. Paul, S.K. Nataraj, Bionanomaterial Scaffolds for Effective Removal of Fluoride, Chromium, and Dye, ACS Sustain. Chem. Eng. 5 (2017) 895–903. doi:10.1021/acssuschemeng.6b02227. J. Cheng, X. Meng, C. Jing, J. Hao, La 3 + -modified activated alumina for fluoride removal from water, J. Hazard. Mater. 278 (2014) 343–349. doi:10.1016/j.jhazmat.2014.06.008. L. Lv, J. He, M. Wei, D.G. Evans, X. Duan, Factors influencing the removal of fluoride from aqueous solution by calcined Mg – Al – CO 3 layered double hydroxides, J. Hazard. Mater. 133 (2006) 119–128. doi:10.1016/j.jhazmat.2005.10.012. X. Wu, P. Cong, H. Nanao, K. Kobayashi, S. Mori, Chemisorption and Tribochemical Reaction Mechanisms of HFC-134a on Nascent Ceramic Surfaces, Langmuir. 247 (2002) 10122–10127.

25

FHSA

●

Alumina

Filtration ● ● ● ● ● ● ● ● ● ● ● ● ●● ● ●● ● ●●

Film ●

Shaking manually

120

100

qe (mg/g)

80 FHSA alumina nanoparticles pure fungus hyphae

60

40

20

0 0

50

100 Ce (mg/L)

150

200