Characterization of Selenite Reduction by Lysinibacillus sp. ZYM-1

Research Article pubs.acs.org/journal/ascecg

Characterization of Selenite Reduction by Lysinibacillus sp. ZYM‑1 and Photocatalytic Performance of Biogenic Selenium Nanospheres Lin Che, Yuxuan Dong, Minghuo Wu, Yonghe Zhao, Lifen Liu, and Hao Zhou* Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Food and Environment, Dalian University of Technology, 124221 Panjin, China S Supporting Information *

ABSTRACT: This study comprehensively investigated the feasibility of biogenic selenium nanomaterials (Se NMs) as a photocatalyst in dye degradation. The marine selenite-reducing bacterium Lysinibacillus sp. ZYM-1 was isolated. This strain can reduce selenite to Se NMs over a wide range of pH (5−9), selenite concentration (1−25 mM), and temperature (20−50 °C) within 48 h. Draft genome data suggested that sulfite reductase may be responsible for selenite reduction. Biogenic Se NMs generated under different conditions were subsequently characterized. The morphology and size of Se NMs were dependent on medium composition, pH, incubation time, selenite concentration, and temperature. Se nanospheres (Se NSs) exhibited significant visible light-driven photocatalytic activity on Rhodamine B (RhB) with H2O2. Three N-deethylation intermediates and phthalic acid were identified as degradation products of RhB by using liquid chromatography-high resolution mass spectrometry (LC-HRMS), indicating the coexistence of chromophore cleavage and the N-deethylation pathway. KEYWORDS: Selenium nanomaterials, Lysinibacillus sp., Biogenic, Controllable synthesis, Photocatalysis

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adsorbents for Hg(0), Zn2+, Cu2+, and Cd2+.10−13 In addition, Se NMs exhibit a band gap of 1.99 eV (amorphous Se) or 1.8 eV (crystalline Se), so they are potentially efficient photocatalysts.14 Chiou et al. used NaBH4-reduced Se NRs as photocatalysts to decompose methylblue under UV irradiation, and they found that Se NRs demonstrated high stability during long-term photocatalysis.15 However, only a few works focus on the possible application of biogenic Se NMs as photocatalysts, especially under visible light (λ > 420 nm). In this study, a marine selenite-reducing bacterium strain ZYM-1 was isolated. Selenite reduction capacity of ZYM-1 was characterized, and the genes linked to Se NMs generation were investigated through the genome data. The effects of initial selenite concentration, temperature, pH, and incubation time on the size and morphology of Se NMs were evaluated, and the visible light-driven photocatalytic capacity of Se NMs was determined. Overall, this study confirmed that bacteria can generate Se NMs with different morphology, and the Se NSs exhibited visible light photocatalytic activity for RhB degradation with H2O2.

INTRODUCTION Selenium (Se) is an essential nutrient in the human diet.1 However, a narrow gap exists between its essential and toxic effects on human health.2 The Se oxyanions, selenate and selenite, are more toxic than elemental Se because of their high solubility and bioavailability.3 Therefore, reduction of dissolved Se oxyanions to solid Se(0) will significantly decrease their toxicity. On the other hand, Se(0) has been widely used in optical devices, photovoltaic solar cells, catalysis, and chemical sensors because of its anisotropy of thermoconductivity, high photoconductivity, thermoelectric response, and nonlinear optical response.4 During the past decades, many approaches have been developed to obtain Se nanomaterials (Se NMs). Given that traditional synthetic methods of Se NMs (laser ablation, UV radiation, and hydrothermal techniques) usually require high temperature, high pressure, and toxic precursors, an alternative eco-friendly approach would be more attractive.1 Microbes develop aerobic detoxification or anaerobic respiration to resist Se oxyanions and reduce them to Se(0).5 This process can be catalyzed by various enzymes, such as selenate reductase, nitrite reductase, and sulfite reductase.6−8 Reduced thiols like glutathione can also reduce selenite to Se(0).9 Biogenic Se NMs usually exist as amorphous or monoclinic allotrope nanospheres (NSs) of different sizes, but sometimes trigonal Se nanorods (NRs) form through simple deposition because their free energy is lower than in Se NSs.4 Given the high affinity of Se to certain heavy metals, biogenic Se NMs have been used as © 2017 American Chemical Society

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EXPERIMENTAL SECTION

Chemicals and Medium. Na2SeO4 and Na2SeO3 were purchased from Sigma-Aldrich. All the other chemicals were of analytical purity Received: November 29, 2016 Revised: January 16, 2017 Published: January 19, 2017 2535

DOI: 10.1021/acssuschemeng.6b02889 ACS Sustainable Chem. Eng. 2017, 5, 2535−2543

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ACS Sustainable Chemistry & Engineering and used without further purification. Luria−Bertani (LB) media was used to acclimate the initial microbial consortium. It contained peptone, 10 g L−1; yeast extract, 5 g L−1; and NaCl, 10 g L−1. Tryptic soy broth (TSB, Beijing Aoboxing Biotech Co. Ltd., China) media was used for Se NMs production. Isolation, Identification, and Genome Analysis of SeleniteReducing Bacterium. The sample of marine sediments was obtained as a previous work as mentioned.16 Here, 5 mL of slurry was added into 95 mL of sterilized LB media with 2 mM Na2SeO3 and incubated at 30 °C , 150 rpm for 7 days. Then, the microbial colony with a red color was selected and further purified for several runs. The obtained strain, designated as ZYM-1, was identified through 16S rRNA sequence alignments using BLASTn (http://blast.ncbi.nlm.nih.gov/ Blast.cgi). The draft genome of strain ZYM-1 has been sequenced using Illumina Hiseq-2500 by the PE125 strategy as reported.17 In this paper, the RAST server was used to annotate the genome and found the possible genes related to the selenite reduction and metal resistance.18 Effects of Various Environmental Factors on Se NMs Generation. For minimal inhibition concentration (MIC) determination, from 0.1 to 150 mM of substrate (Na2SeO4 or Na2SeO3) was added into 20 mL of LB or TSB media and incubated with 200 μL of preincubated bacteria suspension (without Na2SeO4 and Na2SeO3) for 48 h at 30 °C, 150 rpm. The highest substrate tolerance was ensured by the production of red Se NMs. Then, the effects of temperature (20−60 °C), pH (4−11), metal ions (1 mM Cu2+, Mn2+, Co2+, Cd2+, and Zn2+) on the selenite reduction were investigated under the same conditions of MIC determination. For anaerobic selenite reduction, the medium was first deoxygenated by boiling, then packed into bottles and sealed with rubber stoppers under the N2 atmosphere. This medium was then sent to be autoclaved. For all of the experiments except the effect of substrate concentration, the selenite concentration was fixed to 5 mM. Selenite concentration was determined using a spectrophotometric method described by Biswas et al.19 In brief, 1 M Na 2 S converted selenite to a red-brown solution, and the concentration of Se(0) could be determined by UV−vis spectrophotometer at 500 nm. Characterization of Biogenic Se NMs. The Se NMs production could be easily observed through the appearance of a red color in the medium. The broth of strain ZYM-1 containing Se NMs was subjected to sterilization at 121 °C and 17 psi for 20 min in order to release intracellular Se NMs.20 The released Se NMs were centrifuged at 12,000 rpm for 20 min and washed three times with distilled water. The samples were then dried in a vacuum at 60 °C for 12 h. The obtained Se NMs were characterized by X-ray power diffraction (XRD), X-ray photoelectron spectroscopy (XPS), transmission electron microscopy (TEM), UV−vis diffuse reflectance spectrometry (DRS), and Raman spectra. The XRD patterns of Se NMs were obtained using a Bruker AXS D8 advance powder diffractometer (Cu Kα, λ = 1.5418 Å). XPS measurement was performed on a Thermo Fisher Scientific Escalab 250 spectrometer with monochromatized Al Kα excitation, and C1s (284.6 eV) was used to calibrate the peak positions of the elements. XPSPEAK software was employed to fit the peaks. The morphology and size were observed by TEM (JEOL 2000), and the optical properties of the product were determined by DRS using a PerkinElmer Lambda 35 UV/vis spectrometer. Raman spectra was obtained using a confocal laser micro-Raman spectrometer inVia (Renishaw Co., U.K.), with laser excitation at 532 nm. Photocatalytic Performance of Se NMs. The photocatalytic performance of the Se NMs was characterized by decomposing Rhodamine B (RhB) under visible irradiation. A 300 W Xe arc lamp (PLS-SXE300, Beijing Perfectlight Co., Ltd.) with a 420 nm cutoff filter was used to simulate visible light. Before the experiment, the previously obtained Se NMs were suspended in ultrapure water, and the resultant dispersions were amended with n-hexane and placed in a separate funnel. The biomass was extracted into the n-hexane phase, and the Se NMs were kept in the aqueous phase.21 The Se NMs containing an aqueous fraction were centrifuged at 12,000 rpm for 20 min, washed using distilled water three times, and then dried in a vacuum at 60 °C for 12 h. Ten milligrams of Se NMs powder and 2

mL of H2O2 were added into the RhB aqueous solution (50 mL, 10 mg L−1) with constant stirring. The final concentration of H2O2 was 0.424 M. The H2O2 could be decomposed to generate the active species •OH with the assistance of a specific catalyst to accelerate the photocatalytic degradation of RhB.22 Prior to the irradiation, the suspensions were magnetically stirred in the dark for 1 h to establish the adsorption/desorption equilibrium. At given time intervals, 1 mL of the suspension was taken to determine the residual concentration of RhB using an UV−vis spectrophotometer at 554 nm (wavelength scanning mode, 450 to 650 nm). Due to the self-degradation behavior of RhB, a control with 0.424 M H2O2 but without Se NMs was also performed. The photodegradation rate of RhB by Se NMs-H2O2 was calculated using a pseudo-first-order kinetic model (eq 1):

⎛C ⎞ ln⎜ 0 ⎟ = Kt ⎝C⎠

(1)

where C0 is the initial RhB concentration, and C is the corresponded concentration at time t. Here, K is the pseudo-first-order reaction rate constant (min−1). In order to compare the photocatalytic performance, chemogenic Se NMs were also synthesized. Briefly, 5 mL of 500 mM NaBH4 was added into 100 mL of 5 mM selenite and reacted for 12 h at 30 °C. The Se NMs were collected by centrifuging at 12,000 rpm for 10 min, washed with distilled water three times, and dried in a vacuum (80 °C, 6 h). Then, the photocatalytic performance of chemogenic Se NMs was determined. The degradation products of RhB were analyzed using liquid chromatography-high resolution mass spectrometry (LC-HRMS) equipped with an electrospray ionization (ESI) interface (Q-Exactive, Thermo Fisher Scientific). Separation was performed on a C18 column (Ultimate XB C-18, 3.0*150 mm, 3 μm Welch Material, Shanghai, China) and linear gradient elution (mobile phase A, water containing 0.1% FA; mobile phase B, acetonitrile containing 0.1% FA). Gradient: 0−2 min, 30−80% B; 2−4 min, 80% B; 4−4.1 min, 80− 95%; 4.1−9 min 95%, 9−9.1 min, 95−30% B; 9.1−10 min, 30% B; flow rate, 0.4 mL/min). The full scan mode with m/z of 200−500 was used to detect the possible degradation products.

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RESULTS AND DISCUSSION Isolation, Identification, and Genome Sequencing of Strain ZYM-1. When the marine sediments were incubated

Figure 1. Images of biogenic Se NMs generated by incubating strain ZYM-1 with 2 mM Na2SeO3 in both (a) aerobic and (b) anaerobic conditions.

with 2 mM Na2SeO3, the medium became red within 24 h. This color change indicated the presence of selenite-reducing microbes. After several runs of purification, a selenite-reducing bacterium was obtained. This strain, designated as ZYM-1, was identified based on morphological and molecular methods. 2536


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Figure 2. Selenite reduction percentages at different selenite concentrations (a) and pH values (b). The corresponding selenite concentration was 5 mM.

Figure 3. (a) XPS survey of the biogenic Se NMs. (b) Spectra of the Se 3d core level.

Figure 4. Fourier transform infrared spectrum of biogenic Se NMs.

Figure 5. Thermogravimetric curve obtained at 10 °C min−1 in air for biogenic Se NMs.

ZYM-1 is a Gram-positive, facultative anaerobic, rod-shaped bacterium. According to 16S rRNA analysis, the nearest neighbor of the strain ZYM-1 was Lysinibacillus fusiformis strain EC7 (Genbank accession number KP334988). Therefore, this bacterium belongs to the genus Lysinibacillus. Strain

ZYM-1 reduced selenite in both aerobic and anaerobic conditions, and produced red Se NMs (Figure 1). However, ZYM-1 could resist but not reduce up to 2 mM selenate. Many studies have reported that various microorganisms could produce inorganic materials either intra- or extracellu2537


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Figure 6. TEM images of Se NMs generated by strain ZYM-1 in TSB media at different conditions: (a) pH 9.0, (b) pH 7.0, (c) pH 5.0, (d) 48 h, (e) 96 h, (f) 240 h, (g) 1 mM selenite, (h) 5 mM selenite, (i) 25 mM selenite, (j) 30 °C, (k) 40 °C, and (l) 50 °C. The scale bar for each image was 200 nm (a), 200 nm (b), 200 nm (c), 500 nm (d), 500 nm (e), 500 nm (f), 200 nm (g), 200 nm (h), 200 nm (i), 500 nm (j), 200 nm (k), and 50 nm (l).

larly.23 However, the mechanism underlining the nanoparticles formation are various. Some thermodynamically favorable metal ions, such as Au3+, Ag+, and Pd2+, could easily be reduced by quinones, cyclopeptide, or some dehydrogenases with wide substrate spectrum.24 While for selenite reduction and resistance, specific genes may be requested. Therefore, the genome of ZYM-1 was sequenced to identify the genes involved in Se transport and metabolism. Basic information on the draft genome was previously reported.17 Two genes were found in the genome, i.e., dedA and cysA, which are possibly responsible for selenate and selenite transport. A gene-encoding sulfite reductase located at the downstream of cysA, is an important candidate for selenite reduction.25 Five thioredoxin reductase encoding genes, which are also possibly involved in selenite reduction, were found.26 There are a number of genes linked to metal resistance (As5+, Mn2+, Zn2+, and Cd2+) found in the genome. Details on Se metabolism and metal resistancerelated genes are listed in Table S1. Selenite Reduction Characterization of Strain ZYM-1. LB media and TSB media were used to incubate strain ZYM-1 and determine its selenite reduction capacity. The MIC of

selenite in TSB media was 120 mM, which was 2.4-fold of the corresponding MIC value in LB media (50 mM). This selenite resistance capacity was higher than most of the selenite reduction bacteria but lower than Pseudomonas migulae ES3-33 (150 mM) and Pseudomonas sp. CA5 (150 mM).26,27 As the higher MIC of selenite in TSB media, this media was chosen for the following experiments. According to the growth and selenite reduction experiments, strain ZYM-1 could reduce selenite over a range of concentrations. As shown in Figure 2a, up to 5 mM selenite could be reduced completely within 48 h, while when selenite concentration increased to 10 and 25 mM, the reduction ratio decreased to 53% and 31.7%, respectively. Strain ZYM-1 exhibited more than 88% of the selenite reduction ratio within 48 h between pH 5.0 to 9.0, and the optimal condition is pH 7.0 (Figure 2b). Meanwhile, high temperature significantly decreased the selenite reduction ratio within 48 h. When the temperature was higher than 60 °C, bacterium growth and selenite reduction was not observed (data not shown). The MIC of several common metal ions for strain ZYM-1 are listed in Table S2. Strain ZYM-1 could resist and grow with 0.5 mM 2538


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Figure 7. Morphology control of biogenic Se NMs by concentration of selenite in LB media: (a) 1 mM selenite, (b) 2.5 mM selenite, and (c) 5 mM selenite. (d) Energy dispersive X-ray (EDAX) analysis of Se NSs generated at 5 mM selenite.

Cu2+, 1 mM Zn2+, 5 mM Mn2+, 0.1 mM Cd2+, or 1 mM Co2+. However, even 0.1 mM of each metal ion could inhibit the selenite reduction in different levels. Cu2+ and Cd2+ nearly completely inhibit the reduction process, presumably by coordination to the selenite reductase. Characterization of Biogenic Se NMs. The surface element composition and valence state of Se NMs were first determined by XPS. C, N, O, S, and Se were the main elements existing (Figure 3a). C, N, O, S should be contributed by the biological molecules, such as DNA, polysaccharide, and proteins. Compared with other biogenic Se NMs, a relatively high amount of the S element was observed in our case, which may due to the protein sulfhydryl group or glutathione. Figure 3b shows that the Se 3d5/2 binding energy for the nanomaterials was 55.6 eV, which was in good agreement with element Se.8 Therefore, the result of XPS confirmed the generation of Se NMs. According to the Fourier transform infrared (FTIR) spectrum (Figure 4), the Se NMs had a wide peak centered at 3288 cm−1, corresponding to tthe −OH and −NH stretching vibrations of the amine and carboxylic groups. Peaks at 2965 and 2926 cm−1 corresponded to the aliphatic saturated C−H stretching modes. The band centered at 1646, 1545, and 1244 cm−1 corresponded to amide I, amide II, and amide III of the proteins, respectively. The presence of carboxylic groups was confirmed by the peaks at 1447 and 1397 cm−1. The peak at 1046 cm−1 corresponded to the C−H stretching mode of the carbohydrate groups. Therefore, not all of the biomolecules were removed from the surface of Se NMs after hexane treatment. The residual biomolecules, however, are important for the good water dispersity of biogenic Se NMs.

This result further confirmed the existence of biomolecules on the Se NMs.28 TGA analysis of biogenic Se NMs showed that two decomposition processes occurred during heating (Figure 5). The former one started from 230 °C and continued to 300 °C, which was due to the decomposition of selenium.29 The later decomposition process continuing up to 530 °C was due to the presence of biomolecules (especially proteins). According to the TGA curves, the mass percentage of Se was about 20%. As a few reports involved the controllable production of biogenic Se NMs, it is interesting to investigate the effects of various factors on morphology and size. The TEM images of Se NMs generated with different selenite concentrations are shown in Figure 6. When the selenite concentration was 1 mM, most of the Se NMs was cubic (termed Se nanocubes, Se NCs). Then, as the initial selenite concentration increased, the morphology of the Se NMs became spherical (i.e., Se NSs). The size distribution of Se NSs in different selenite concentrations was similar, generally in the range of 100−200 nm. Using 5 mM selenite as the initial concentration, the effects of pH, temperature, and reaction time were further determined. Compared with the Se NSs synthesized at pH 7.0, those Se NMs generated at pH 5.0 seemed more irregular, and some of the Se NMs became bowl-like at pH 9.0. The morphology and size of Se NMs were similar in despite of the incubation time being 48 or 96 h. Interestingly, when strain ZYM-1 was incubated at 50 °C, much smaller Se NSs were obtained. These Se NSs were spherical, monodisperse, and with a size distribution of 3.8 ± 1.8 nm according to the TEM analysis. It has been known that bacteria employ an export system for 2539


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Figure 8. Characterization of biogenic Se NMs. (a) Power XRD pattern of Se NRs and Se NSs. (b) Raman scattering spectra of Se NSs. (c) UV− visible diffuse reflectance spectra of biogenic Se NSs. The inset is the digital image of dried Se NSs powder. (d) Band gap calculation using plot of the (αhυ)2 vs hυ.

to the decrease in protein activity which involved selenium nanoparticles assembling. In addition, the size and morphology of the Se NMs generated to LB were also compared. It seemed the initial concentration of selenite could affect the morphology significantly. Se NRs, Se NCs, and Se NSs could be obtained at room temperature with different initial concentrations of selenite, and the energy dispersive X-ray (EDAX) analysis also confirmed the biomolecules coated at the surface of Se NSs (Figure 7). It is well known that trigonal Se (most exhibited as Se NRs) is the most stable phase of all Se allotropes, and the phase transformation from amorphous Se to trigonal Se usually involved both the linear aggregation of Se nanospheres and crystallization from the amorphous phase.31 In this case, the selenium nanoparticles synthesized at lower selenite concentration seems more unstable and transferred to Se NRs. While at higher selenite concentrations, the longer reaction time made more biomolecules coated at the surfaces of initial selenium nanoparticles, which limited their further growth and aggregation. Interestingly, the Se NCs were rarely reported regardless of chemical, physical, or biological methods. The crystallinity of two commonly reported morphologies, i.e., Se NSs and Se NRs, were further characterized using XRD (Figure 8a). It is shown that all the observed peaks of Se NRs could be indexed to the trigonal phase of selenium (JCPDS card code 06-0632). On the other hand, the Se NSs only showed a weakly crystalline trigonal phase. However, the Raman scattering spectrum showed a signature located at 254

Figure 9. Photocatalytic degradation of RhB using biogenic Se NSs (white squares) and chemogenic Se NMs (black squares) with 0.424 M H2O2. The control was RhB with 0.424 M H2O2 (red circles). Inset is the UV−vis spectral changes in RhB in the biogenic Se NSs−H2O2 system as a function of reaction time.

the secretion of Se atoms in the form of Se(0) nanoparticles, and a protein named Se factor A (SefA) was found involved with Se NMs assemble.30 As proteins usually become partly denatured at higher temperature, the smaller Se NSs may due 2540


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Figure 10. Proposed degradation pathway of RhB using biogenic Se NSs under visible light (λ > 420 nm).

cm−1, confirming the existence of monoclinic Se (Figure 8b). The difference in crystallinity of Se NSs should be due to the low stability of monoclinic Se under the vacuum heating conditions. Furthermore, as the photocatalytic performance of a material usually depends on the intrinsic electronic properties such as the band-edge potential, the band gap, and the chargecarrier mobility. The visible light adsorption of biogenic Se NSs was determined by DRS. It is shown in Figure 8c that the biogenic Se NSs exhibit a strong adsorption band in the longwavelength region, which may indicate the potential photocatalytic activity under visible light. The band gap energies (hυ) were calculated as 1.74 eV from the plot of (αhυ)2 versus hυ (α and hυ stand for absorption coefficient and photon energy, respectively), which were similar to the chemogenic Se NMs (Figure 8d).22 Photocatalytic Performance of Biogenic Se NMs. To establish the potentiality of the biogenic Se NMs as photocatalysts, Se NSs and Se NRs were subject to visible light irradiation in order to evaluate their photocatalytic performance. Se NRs did not show remarkable photocatalytic activity (data not shown). Meanwhile, no significant degradation of RhB was observed when the Se NMs were absent. In the case of Se NSs, the color of RhB changed from light pink to colorless within 300 min, and the maximum adsorption wavelength shifted from 554 to 532 nm, indicating the production of reaction intermediates. The corresponding reaction rate constant of the Se NSs−H2O2 system on RhB degradation was 0.0048 min−1, which is comparable with previously reported fluorinated Bi2WO6.32 In comparison, the RhB concentration exhibited a similar but slower decreasing trend in the chemogenic Se NMs−H2O2 system; the reaction rate constant was 0.0011 min−1 (Figure 9). According to the results of the SEM images and XRD pattern, the chemogenic Se NMs were regular trigonal phase microsheets (Figure S1). Zhang et al. reported that trigonal Se NRs could degrade methyl orange under visible light.22 In this study, the visible light-responsible capacity of monoclinic Se NSs was found, and it was higher than that of trigonal Se NRs when using RhB as the target pollutant. Interestingly, the photomemory effect of Se NSs, i.e., the decolorization process could continue in the dark after preirradiation, was also observed in this case.15 The underlying mechanism for the photomemory effect needs further investigation.

LC-HRMS was used to identify the possible reaction intermediates in the RhB biogenic Se NSs−H2O2 system. It was well studied that RhB could be photodegraded via two competitive processes: N-deethylation and the conjugated chromophore structure cleavage.32 In this case, three Ndeethylated intermediates were observed: N,N-diethyl-N-ethylrhodamine (DER, m/z 415), N,N-diethyl-rhodamine (DR, m/z 387), and N-ethylrhodamine (ER, m/z 359). Meanwhile, phthalic acid was also identified as an intermediate of the conjugated structure cleavage (Figure S2). The elution time and corresponded products were also listed in Table S3. This result suggested that RhB not only deethylated but also suffered an advanced ring cleavage process. On the basis of the result of LC-HRMS, the supposed degradation pathway of RhB is shown in Figure 10.

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CONCLUSIONS This study reported on the controllable synthesis of Se NMs using the marine bacterium Lysinibacillus sp. ZYM-1. Medium composition, pH, temperature, and initial selenite concentration could affect the size and morphology of Se NMs. Se NCs, Se NRs, and Se NSs could be obtained under different conditions. Se NSs demonstrated visible light-driven photocatalytic activity with H2O2, and this feature could be useful in dye wastewater treatment. Therefore, this study confirmed the novel application of biogenic Se NSs as a visible light-driven photocatalyst.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssuschemeng.6b02889. Figure S1: SEM image (a) and XRD pattern (b) of chemogenic Se NMs. Figure S2: LC and HRMS spectra of RhB degradation intermediates. (a) Liquid chromatogram of RhB and its degradation intermediates. (b) HRMS spectrum of RhB. (c) HRMS spectrum of N,Ndiethyl-N′-ethylrhodamine (DER). (d) HRMS spectrum of N,N-diethyl-rhodamine (DR). (e) HRMS spectrum of N-ethylrhodamine (ER). (f) HRMS spectrum of phthalic acid. Table S1: Selenium metabolism and metal resistance-related genes identified from the draft genome of strain ZYM-1. Table S2: MIC of different metal ions 2541


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of Cu in a multi-metal mixture onto biogenic elemental selenium nanoparticles. Chem. Eng. J. 2016, 284, 917−925. (13) Yuan, F.; Song, C.; Sun, X.; Tan, L.; Wang, Y.; Wang, S. Adsorption of Cd(II) from aqueous solution by biogenic selenium nanoparticles. RSC Adv. 2016, 6 (18), 15201−15209. (14) Liu, G.; Niu, P.; Cheng, H. M. Visible-light-active elemental photocatalysts. ChemPhysChem 2013, 14 (5), 885−892. (15) Chiou, Y. D.; Hsu, Y. J. Room-temperature synthesis of singlecrystalline se nanorods with remarkable photocatalytic properties. Appl. Catal., B 2011, 105 (1−2), 211−219. (16) Zhou, H.; Pan, H.; Xu, J.; Xu, W.; Liu, L. Acclimation of a marine microbial consortium for efficient Mn(II) oxidation and manganese containing particle production. J. Hazard. Mater. 2016, 304, 434−440. (17) Zhao, Y.; Dong, Y.; Zhang, Y.; Che, L.; Pan, H.; Zhou, H. Draft genome sequence of a selenite- and tellurite-reducing marine bacterium, Lysinibacillus sp. strain ZYM-1. Genome Announc. 2016, 4 (1), e01552-15. (18) Aziz, R. K.; Bartels, D.; Best, A. A.; DeJongh, M.; Disz, T.; Edwards, R. A.; Formsma, K.; Gerdes, S.; Glass, E. M.; Kubal, M.; Meyer, F.; Olsen, G. J.; Olson, R.; Osterman, A. L.; Overbeek, R. A.; Mcneil, L. K.; Paarmann, D.; Paczian, T.; Parrello, B.; Pusch, G. D.; Reich, C.; Stevens, R.; Vassieva, O.; Vonstein, V.; Wilke, A.; Zagnitko, O. The RAST server: Rapid annotations using subsystems technology. BMC Genomics 2008, 9 (1), 75. (19) Biswas, K. C.; Barton, L. L.; Tsui, W. L.; Shuman, K.; Gillespie, J.; Eze, C. S. A novel method for the measurement of elemental selenium produced by bacterial reduction of selenite. J. Microbiol. Methods 2011, 86 (2), 140−144. (20) Fesharaki, P. J.; Nazari, P.; Shakibaie, M.; Rezaie, S.; Banoee, M.; Abdollahi, M.; Shahverdi, A. R. Biosynthesis of selenium nanoparticles using Klebsiella pneumoniae and their recovery by a simple sterilization process. Braz. J. Microbiol. 2010, 41 (2), 461−466. (21) Dobias, J.; Suvorova, E. I.; Bernier-Latmani, R. Role of proteins in controlling selenium nanoparticle size. Nanotechnology 2011, 22 (19), 195605. (22) Zhang, R.; Tian, X.; Ma, L.; Yang, C.; Zhou, Z.; Wang, Y.; Wang, S. Visible-light-responsive t-Se nanorod photocatalysts: Synthesis, properties, and mechanism. RSC Adv. 2015, 5 (56), 45165− 45171. (23) Durán, N.; Marcato, P. D.; Durán, M.; Yadav, A.; Gade, A.; Rai, M. Mechanistic aspects in the biogenic synthesis of extracellular metal nanoparticles by peptides, bacteria, fungi, and plants. Appl. Microbiol. Biotechnol. 2011, 90 (5), 1609−1624. (24) Hennebel, T.; De Corte, S.; Verstraete, W.; Boon, N. Microbial production and environmental applications of Pd nanoparticles for treatment of halogenated compounds. Curr. Opin. Biotechnol. 2012, 23 (4), 555−561. (25) Harrison, G.; Curle, C.; Laishley, E. J. Purification and characterization of an inducible dissimilatory type sulfite reductase from Clostridium pasteurianum. Arch. Microbiol. 1984, 138 (1), 72−78. (26) Li, X.; Kot, W.; Wang, D.; Zheng, S.; Wang, G.; Hansen, L. H.; Rensing, C. Draft genome sequence of Se(IV)-reducing bacterium Pseudomonas migulae ES3−33. Genome Announc. 2015, 3 (3), e00406− e00415. (27) Hunter, W. J.; Manter, D. K. Reduction of selenite to elemental red selenium by Pseudomonas sp. Strain CA5. Curr. Microbiol. 2009, 58 (5), 493−498. (28) Jain, R.; Jordan, N.; Weiss, S.; Foerstendorf, H.; Heim, K.; Kacker, R.; Hübner, R.; Kramer, H.; van Hullebusch, E. D.; Farges, F.; Lens, P. N. Extracellular polymeric substances govern the surface charge of biogenic elemental selenium nanoparticles. Environ. Sci. Technol. 2015, 49 (3), 1713−1720. (29) Chen, Z.; Shen, Y.; Xie, A.; Zhu, J.; Wu, Z.; Huang, F. Lcysteine-assisted controlled synthesis of selenium nanospheres and nanorods. Cryst. Growth Des. 2009, 9 (3), 1327−1333. (30) Debieux, C. M.; Dridge, E. J.; Mueller, C. M.; Splatt, P.; Paszkiewicz, K.; Knight, I.; Florance, H.; Love, J.; Titball, R. W.; Lewis, R. J.; Richardson, D. J.; Butler, C. S. A bacterial process for selenium

to strain ZYM-1 and selenite reduction ratio. Table S3: Identification of RhB and the degradation intermediates of RhB during the photocatalytic process by LC-HRMS. (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel: +86-427-2631786. ORCID

Lifen Liu: 0000-0002-1087-9739 Hao Zhou: 0000-0002-3901-6582 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The project was supported by the National Natural Science Foundation of China (No. 31500080) and “the Fundamental Research Funds for the Central Universities” (DUT15RC(3) 050). We also are thankful for the help of Dr. Feng Liu, Dr. Lijuan Wei, Dr. Shaojie Li, and Fumei Deng for samples characterization.

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Characterization of Selenite Reduction by Lysinibacillus sp. ZYM-1

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