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Environmental Science and Pollution Research

, Volume 26, Issue 3, pp 2873–2881 | Cite as

Effects of reaction conditions on light-dependent silver nanoparticle biosynthesis mediated by cell extract of green alga Neochloris oleoabundans

  • Zeqing Bao
  • Jiahui Cao
  • Guangbo Kang
  • Christopher Q. LanEmail author
Research Article
  • 141 Downloads

Abstract

Silver nanoparticles (AgNPs) were synthesized by incubating the mixture of AgNO3 solution and whole-cell aqueous extracts (WCAEs) of Neochloris oleoabundans under light conditions. By conducting single-factor and multi-factor optimization, the effects of parameters including AgNO3 concentration, pH, and extraction time were quantitatively evaluated. The optimal conditions in terms of AgNP yield were found to be 0.8 mM AgNO3, pH 5, and 9-h extraction. The AgNPs thus synthesized were quasi-spherical with a mean particle diameter of 16.63 nm and exhibited decent uniformity as well as antibacterial activities, which may facilitate AgNP biosynthesis’s application in the near future.

Keywords

Biosynthesis Silver nanoparticles Microalgae AgNO3 concentration pH Extraction time Light-dependent reaction 

Introduction

Particles smaller than 100 nm are regarded as nanoparticles (NPs), which are characterized by large surface to volume ratio (Mahdieh et al. 2012). The extraordinarily small size and large surface to volume ratio of NPs allow their unique and improved performance in numerous applications (Narayanan and Sakthivel 2011), making production of NPs a topic of extensive interests of both the academic and industrial communities (Sharma et al. 2016). Among various metallic nanoparticles, silver nanoparticles (AgNPs) are one of the most promising and versatile nanomaterial for which numerous applications such as antimicrobial (Sudha et al. 2013; Rajan et al. 2015) and catalytic (Bhatte et al. 2010) have been established.

NP production methods can be categorized into three groups: physical, chemical, and biological (Thuc et al. 2016). Physical and chemical approaches are in general costly, involving complex facilities and/or involving physical and chemical hazards (Ramya and Subapriya 2012). On the other hand, synthesis of NPs utilizing different forms of bio-derived materials including bacteria, fungi, microalgae, and plants have shown potentials to produce NPs in a cost-effective, environmental friendly, biologically compatible, and sustainable manner (Quester et al. 2013).

Microalgae of selected species may prove to be particularly advantageous because of their fast reproduction (Zhu et al. 2013), non-toxicity (Slade and Bauen 2013), and rich contents of various bioactive materials (Molina Grima et al. 2003). Furthermore, they are one of the primary producers that could be produced in a sustainable manner in combination with dynamic carbon dioxide recycling and are therefore excellent candidates for green NP synthesis (Shakibaie et al. 2010).

Although the number of research articles on algae-mediated synthesis of metallic NPs was rapidly increasing (Sharma et al. 2016), studies in this field are still relatively scarce. Extensive research efforts are therefore warranted to better our understanding to the mechanisms involved in alga-mediated (or in a more general sense biomass-mediated) nanoparticle synthesis and to eventually bring it to a commercially viable level. It is also worth noting that the mechanism underlying light dependency in alga-mediated AgNP biosynthesis has been recently reported (Bao and Lan 2018).

In this study, we investigated for the first time the synthesis as well as optimization of AgNPs using whole-cell aqueous extract (WCAE) of green algae Neochloris oleoabundans (N. oleoabundans) under different conditions including and light/dark conditions, AgNO3 concentration, pH, and extraction time. It was demonstrated that the synthesis was completely light-dependent and the WCAE of N. oleoabundans could effectively mediate the bio-reduction of Ag+ to Ag0 at room temperature. Use of WCAE offers the advantage over the use of disrupted cell aqueous extract (DCAE) in eliminating the cell disruption process. On the other hand, the fact that the dilute WCAE could mediate AgNP formation in a meaningful way also suggest there is a great potential of enhancing the efficiency of alga-mediated AgNP biosynthesis by increasing the concentration of bioreactive components in cell extracts one way or the other.

Materials and methods

Culture and medium free culture

Neochloris oleoabundans (N. oleoabundans) was purchased from Culture Collection of Algae at the University of Texas in Austin (UTEX 1185).

The Modified Bristol Medium (MBM), which was adopted in our previous studies (Peng et al. 2015), was used in this study for the cultivation of N. oleoabundans. It was composed of (per liter) 0.35 g NaNO3, 0.138 g K2HPO4, 0.0823 g MgSO4, 0.025 g CaCl2, 0.322 g KH2PO4, 0.025 g NaCl, 0.0068 g FeCl3, and 1 mL A5 solution. The A5 solution was composed of the following components (per liter): 1.6423 g EDTA-Fe, 2.86 g H3BO3, 1.81 g MnCl2∙4H2O, 0.22 g ZnSO4∙7H2O, 0.079 g CuSO4∙5H2O, and 0.039 g (NH4)6Mo7O2∙4H2O. All chemicals used in the medium were of analytical grade. The media were sterilized using autoclave at 121 °C for 20 min.

The microalgae were cultivated in 500-mL Erlenmeyer flasks containing 400 mL sterile MBM for 8–10 days at 27 °C in an illuminated incubator (model LI15, manufactured in USA by Sheldon Manufacturing INC) until the microalgal cell density reached approximately 1.6 × 107 cells/mL. The culture was then centrifuged at 7750g and rinsed with deionized water three times to produce medium free cell aqueous suspensions, which were stored at − 80 °C in a ULT freezer (model 706, manufactured in USA by Thermo Electron Corporation) for future use.

AgNP synthesis

AgNO3 was used in this study as the silver source of AgNP production. AgNO3 powder (99.85%) was purchased from Acros Organics and a 10 mM AgNO3 stock solution was prepared with distilled water. The solution was kept in a brown bottle and stored at 4 °C.

Twenty microliters of microalgal culture thawed at room temperature before being incubated in boiling water bath for a certain period of time (0.5, 1, 2, 3, … 10 h) and then centrifuged at 7750g to remove cells and cell debris (Jena et al. 2013). The supernatant (WCAE) was used for AgNP synthesis.

Five milliliters of WCAE was added with different volumes (0.2, 0.4, 0.6, 0.8, 1.0, 2.0, 3.0, 4.0, 5.0 mL) of AgNO3 stock solution (10 mM), sterile deionized water was then added to make the total volume of the mixture to 10 mL. The mixture was mixed by hand shaking before being incubated at 27 °C for 12 h for synthesis of AgNPs with illumination at 5000 lx (Philips Fluorescent 800 series, 32 W). For AgNP synthesis in darkness, the test tubes were wrapped completely with aluminum foil.

Characterization of AgNPs

Spectrometric measurements were carried out by scanning the produced AgNPs suspensions from 350 to 800 nm using a GENESYS 10S UV-VIS Spectrophotometer.

The morphology of AgNPs was observed by subjecting the AgNP suspension samples to a TEM (FEI Tecnai G2 Spirit Twin TEM) at the Centre for Catalysis Research and Innovation (CCRI) in the University of Ottawa.

Cell number

Cell number was counted using a hemocytometer (improved Neubauer, Phase Counting Chamber w/2 cover glass, USA) under a phase-contrast microscope (Infinity II BX40, Olympus, Canada) at a magnification of 200 times.

Orthogonal tests

Orthogonal (factorial) tests were designed and analyzed by “IBM SPSS Statistics (Version 22).” As shown in Table 1, the tests were designed by the three-factor and three-level model.
Table 1

Orthogonal tests plan

Runs

Factors

A

B

C

1

A1

B1

C1

2

A1

B2

C2

3

A1

B3

C3

4

A2

B1

C2

5

A2

B2

C3

6

A2

B3

C1

7

A3

B1

C3

8

A3

B2

C1

9

A3

B3

C2

Where A represents AgNO3 concentration (A1 = 0.4 mM, A2 = 0.8 mM, A3 = 1.2 mM); B represents pH value (B1 = pH 3, B2 = pH 5, B3 = pH 7); C represents extraction time (C1 = 3-h extraction, C2 = 6-h extraction, C3 = 9-h extraction). Those values were chosen based on single-parameter optimization, which will be explained later.

Antibacterial activity tests

Luria broth (LB), which was composed of (per liter) 10 g tryptone, 5 g yeast extract, and 10 g NaCl, was used to grow Escherichia coli (E. coli) inoculum. LB agar, which was composed of LB plus 15 g agar per liter, was used to make agar plates. Both LB and LB agar were autoclaved at 121 °C for 20 min. To make agar plates, the autoclaved LB agar was cooled to approximately 55 °C and then about 10 mL medium was transferred into each sterile petri dish under sterile conditions. Agar plates were then put on surface of lab bench further cooled down to room temperature to form solid agar plates.

The produced AgNP suspensions were centrifuged and rinsed with deionized water three times to produce pure AgNP suspensions, which were stored at 4 °C for future use.

To determine the growth curve in the presence of AgNPs, E. coli bacteria were grown in 100 mL liquid LB medium with 0 (control), 10, 50, and 100 μg/mL of AgNPs. Optical density (OD) values at 600 nm were measured for every 1 h until 6 h. Samples of 6-h cultures were then taken and diluted by appropriate ratios before being spread on nutrient agar plates. Agar plates were incubated further at 37 °C for 24 h, and the numbers of colonies were counted to determine number of surviving cells in the 6-h cultures.

Results and discussions

Single-factor optimization

Light-dependency

As shown in Fig. 1, AgNPs were synthesized by incubating WCAE with 1 mM AgNO3 under light conditions. Visual inspection of the mixtures indicated that they changed gradually from the original light greenish color to yellow. This color change was caused by surface plasmon resonance (SPR), which is an important indicator showing the presence of AgNPs (Mock et al. 2002). On the contrary, controls carried out under identical conditions except the absence of light showed no SPR peaks nor color change of the reaction solution. In other words, light is essential for the biosynthesis of AgNPs mediated by the WCAE of N. oleoabundans.
Fig. 1

UV-Vis spectra of WCAE obtained by 30-min extraction before and after incubation with 1 mM AgNO3 under light condition for 12 h

It should be noted that the majority of studies in the literature have reported biomass-mediated biosynthesis of NPs as light-independent (Barwal et al. 2011; Castro et al. 2013). Nevertheless, there are also reports demonstrating light-dependent AgNPs with extracts of microalgal biomass (Jena et al. 2015).

The WCAE was examined using bicinchoninic acid (BCA) method for total protein concentration (Smith et al. 1985) and FTIR for functional group analysis. However, no proteins or functional groups were detected, possibly due to the low concentration of cellular materials in the WCAE, which seemed to be beyond the threshold of detection of corresponding analytic methods. Nevertheless, chlorophyll was detected with UV-Vis spectrum according to the method described by Porra et al. (1989), as also shown in Fig. 1 (WCAE). The total chlorophyll (including both chlorophyll a and b) concentration was calculated to be 0.22 nmol/mL, which is extremely low. On a positive side, however, the fact that a WCAE with extremely low concentration of cellular materials could mediate meaningful biosynthesis of AgNPs implies that these components are extremely effective, pointing to a potentially high efficiency and low cost process when the extraction of these components is improved in the future. Secondly, the extremely low concentration of these components in the reaction mixture makes the separation of AgNPs from the mixture straightforward and cost-effective.

Reactive agents of low concentration initiating and mediating AgNP synthesis could be explained by the mechanism of light-dependent AgNP synthesis (Bao and Lan 2018). In that study, light was reported to be required for exciting chlorophylls to donate electrons, which would reduce Ag+ to Ag0. The oxidized chlorophylls are hypothetically replenished with electrons through reactions such as water splitting.

AgNO3 concentration

Figure 2 shows the effects of AgNO3 concentration on the AgNP synthesis, in terms of AgNP concentration as well as yield. AgNP concentrations (μg/mL) were calculated using the optical density values (a.u.) and a conversion factor number, 8.2 (Bao and Lan 2018).
Fig. 2

AgNP concentration and yield rate of AgNP suspensions produced using cell extracted by 30-min extraction and different concentrations of AgNO3 incubated under light condition for 12 h

AgNP concentration increased significantly from 2.6 to 3.8 μg/mL, representing an increase of 46.2%, when AgNO3 increased from 0.2 to 0.4 mM, however, dropped to 1.5 μg/mL when AgNO3 concentration further increased to 0.6 mM. AgNP concentration decreased slowly but steadily with minor fluctuations when AgNO3 concentration further increased from 0.6 to 5.0 mM.

One possible explanation was that, from 0.2 to 0.4 mM, the bioreactive components in the extract was excessive and more Ag+ were available to be reduced to form more AgNPs when AgNO3 increased in this range. On the other hand, beyond 0.4 mM, excessive Ag+ became inhibitive to the reaction. It has been well established that, as a heavy metal ion, high concentration of Ag+ had inhibiting effects on bioactive agents (Choi et al. 2008), which are important carriers of reducing power in this reaction.

Meanwhile, yield kept decreasing from 12.1 to 0.10% when AgNO3 concentration increased from 0.2 to 5.0 mM. Under the investigated conditions, 0.2 mM AgNO3 gave the highest yield and 0.4 mM AgNO3 allowed the highest product concentration. It is reasonable to have lower yield when the portion of main reactant increased while the other components involved in the reaction were unchanged. These results indicate that the optimal AgNO3 concentration for AgNP synthesis is around 0.4 mM under the specific conditions.

Reaction pH

Since high pH leads to the formation of Ag2O, which may interfere the formation and detection of AgNPs, effects of pH 3–7 were tested. The pH values were adjusted using 1 mol/L HNO3 and 1 mol/L NaOH solutions. Figure 3 shows the UV-Visible spectra of AgNP suspensions produced at different pH in the range of pH 3–7 with 30 min WCAE and 0.4 mM AgNO3. It is clear that pH 5 gave the highest AgNP production. Under pH 6 and 7, the production of AgNPs was similar. However, the synthesis of AgNPs under pH 3 and 4 seemed to be significantly inhibited judging from the absence of distinguishable peaks. These results are compatible with that of Ibrahim (2015).
Fig. 3

UV-Vis spectra of AgNP suspensions produced using 30-min WCAE incubated under pH 3, pH 4, pH 5, pH 6, and pH 7 for 12 h with 0.4 mM AgNO3

The inhibitory effects of low pH on AgNP synthesis could be twofold: (1) reducing the activities of the bioactive components in the WCAE, and (2) the increased H+ concentration at low pH could lead to the formation of strong oxidant nitric acid (Tchoul et al. 2007), which could consume the reducing power (excited electrons) in the reaction mixture.

Extraction time

Figure 4 shows the change of AgNP concentration of the reaction with extraction time in the range of 0.5–10.0 h with 0.4 mM AgNO3 at pH 5. The yield of the AgNPs increased with extraction time continuously until 6 h, after which the increase leveled off gradually.
Fig. 4

Concentration of AgNPs produced using 0.5 to 10-h WCAE incubated under pH 5 for 12 h with 0.4 mM AgNO3

Many researchers reported the successful synthesis of AgNPs using boiled plants (Krishnaraj et al. 2010). Of particular relevance, it was reported that the successful synthesis of AgNPs using aqueous banana peel extract, which was obtained by stewing banana peel at 90 °C for 30 min (Ibrahim 2015). Those results indicated that the active agents were thermally stable and can be easily extracted from cells without cell disruption.

Multi-factor optimization

An orthogonal experiment (Table 1) was designed to analyze the significance of each factor and factors’ joint effects on the reaction (Du et al. 2002). The results are summarized in Table 2.
Table 2

Orthogonal tests results

AgNO3 concentration (mM)

pH

Extraction time (h)

AgNP concentration (μg/mL)

0.4

3

3

0.80

0.4

5

6

12.01

0.4

7

9

10.10

0.8

3

6

5.35

0.8

5

9

15.44

0.8

7

3

2.35

1.2

3

9

5.30

1.2

5

3

1.20

1.2

7

6

3.45

Significances of individual factors are shown in Table 3. The P values of both pH and extraction time were less than 0.05 while that of AgNO3 concentration (0.051) was merely greater than 0.05 but less than 0.10. These results indicate that all the three parameters could significantly affect the reaction in terms of product concentration although the effect of AgNO3 concentration was not as significant as that of the other two parameters.
Table 3

Significance analysis

Source

SSE

MSE

P

 

AgNO3 concentration

0.565

0.283

0.051

< 0.10

pH value

0.790

0.395

0.037

< 0.05

Extraction time

1.775

0.888

0.017

< 0.05

As shown in Fig. 5, the AgNO3 concentration showed no visible effect on AgNP production when it was increased from 0.4 to 0.8 mM (level 1 to level 2) but significant inhibitive effect was demonstrated when it further increased to 1.2 mM. When the extraction time increased from 3 to 9 h, the marginal mean value AgNP concentration increased continuously, and the rate of increase slowed down after 6 h. Similar to the previous results, the optimal pH for the AgNP synthesis was pH 5.
Fig. 5

Estimated marginal means of AgNP concentration versus AgNO3 concentration, pH, and extraction time

These results show the same trends as when the parameters were individually tested although at different scales. For instance, the optimal AgNO3 concentration was found to be 0.8 mM while it was determined to be 0.4 mM in the single-factor optimization. Likewise, the effect of boiling time was found to be minimal when increasing from 6 to 9 h in the single factor tests while significant improvement was predicted by the orthogonal optimization results in the same range of temperature change.

The estimated results of all the 27 combinations were further calculated based on 95% confidence interval and are summarized in Table 4, which show the optimal combination of conditions to be 0.8 mM AgNO3, pH 5, and 9-h extraction. Some negative values are shown in Table 4 as the predicted concentrations of AgNPs, which are not physically realistic and should be treated as zeros.
Table 4

Estimates of AgNP concentration using all the combinations of three parameters

Parameters

Mean of AgNP concentration (μg/mL)

Std. error

95% confidence interval

AgNO3 concentration (mM)

pH value

Extraction time (h)

Lower bound

Upper bound

0.4

3

3

0.45

0.89

− 3.36

4.27

6

5.95

0.89

2.13

9.77

9

9.29

0.89

5.47

13.11

5

3

6.19

0.89

2.37

10.01

6

11.68

0.89

7.87

15.50

9

15.02

0.89

11.21

18.84

7

3

1.94

0.89

− 1.88

5.76

6

7.43

0.89

3.62

11.25

9

10.77

0.89

6.96

14.59

0.8

3

3

0.53

0.89

− 3.29

4.35

6

6.03

0.89

2.21

9.84

9

9.37

0.89

5.55

13.18

5

3

6.27

0.89

2.45

10.08

6

11.76

0.89

7.94

15.58

9

15.10

0.89

11.28

18.92

7

3

2.02

0.89

− 1.80

5.83

6

7.51

0.89

3.69

11.33

9

10.85

0.89

7.03

14.67

1.2

3

3

− 3.87

0.89

− 7.68

− 0.05

6

1.63

0.89

− 2.19

5.44

9

4.97

0.89

1.15

8.78

5

3

1.87

0.89

− 1.95

5.68

6

7.36

0.89

3.54

11.18

9

10.70

0.89

6.88

14.52

7

3

− 2.38

0.89

− 6.20

1.43

6

3.11

0.89

− 0.71

6.93

9

6.45

0.89

2.63

10.27

Characterization

Synthesis of AgNPs under the optimal conditions as concluded from the afore discussed experiments, i.e., 0.8 mM AgNO3, pH 5, 9-h WCAE, and 12 h of incubation with illumination, were subjected to characterization. As shown in Fig. 6, the AgNPs synthesized in this process were nearly spherical with decent uniformity and the mean particle diameter was found to be 16.63 nm by counting 244 particles from six different TEM images.
Fig. 6

a Particle size distribution, which was obtained by counting 244 particles in six TEM images. b TEM image of AgNPs synthesized with 0.8 mM AgNO3 and 9-h WCAE at pH 5

It was reported that the wavelengths of SPR peaks were related to the size of particles and decrease of particle size caused blueshift (Agnihotri et al. 2014). Also reported in the same study, the peak at 420 nm corresponded to the particle diameter of ~ 50 nm. However, this conclusion was not in agreement with our results and that of a study focusing on correlating SPR peaks to particle sizes (Baset et al. 2011). These results seem to suggest that SPR peaks might be affected not only by the mean particle size but also by other factors such as particle size distribution and shape as well. It seems also to be reasonable to suggest that the peak width reflects to certain extent the particle size distribution.

Antibacterial activity

As shown in Fig. 7, the AgNPs were able to inhibit the growth of E. coli, which is a Gram-negative bacterium that has been frequently used as the indictor strain for tests of antibacterial activities of different metal NPs (Sondi and Salopek-Sondi 2004; Zhang et al. 2007; Ruparelia et al. 2008). The inhibitory effects increased with AgNP concentration and reached near-complete inhibition at 100 μg/mL AgNPs. In fact, for the culture containing 100 μg/mL AgNPs, bacteria were not detectable in the first 4 h but a cell number density of 1.8 × 107/mL was observed in the 5-h samples, which represents a survival rate of 1.4% in comparison with the control (1.28 × 109/mL after 5 h of incubation). These results suggest that E. coli could adapt to AgNPs up to 100 μg/mL, although the survival rate is low. It was also reported that the particle morphology also affected AgNPs’ antibacterial activity, and AgNPs of smaller size usually perform better antibacterial activity (Yamamoto 2001).
Fig. 7

aE. coli growth curve in the presence of 0, 10, 50, and 100 μg/mL of AgNPs. b Cell number density of surviving bacterial cells after 6 h of cultivation with AgNPs

AgNPs possess better antibacterial activity than Ag+ ions mainly due to their large surface aera, which faciliates AgNPs’ attachment to cell membrane and penetration into cells (Rai et al. 2009). AgNPs interact with membrane proteins and DNA and can aslo be reoxidized to release Ag+ to further enchance their inhibiting effects (Rai et al. 2009). Siginicant morphology and cell membrane changes in E. coli cells were observed by SEM and TEM, and cell membrane was damaged after being exposed to 50 μg/mL of AgNPs (Li et al. 2010).

According to literature data, AgNPs seem to be a broad-spectrum antibacterial as they have been reported to show antibacterial effects on Gram-positive strains as well (Fayaz et al. 2010; Guzman et al. 2012). However, many studies reported that Gram-positive strain was more resistent to AgNPs (Kim et al. 2007). This is mainly because of the difference between the structures of Gram-positive and Gram-negative strains. Gram-positive bacteria are characterized by having a thick peptidoglycan layer (Kim et al. 2007), which could be resistant to the penetration of AgNPs. On the other hand, Gram-negative bacteria have a thin peptidoglycan layer and an outer membrane, which may facilitate attachment of AgNPs onto call surfurace and is poor in preventing them from pentrating the cell wall to reach cell membrane (Slavin et al. 2017).

Conclusions

WCAE of N. oleoabundans showed ability of mediating the reduction Ag+ to fabricate AgNPs at the presence of light. The AgNPs thus synthesized are quasi-spherical nanoparticles with antibacterial activity on E. coli. At light intensity of 5000 lx, the optimal condition for AgNP biosynthesis was determined to be 0.8 mM AgNO3, pH 5, and 9-h extraction.

Notes

Acknowledgments

This research was funded by a Discovery Grant (RGPIN – 1511) to Dr. Christopher Q. Lan by the Natural Sciences and Engineering Research Council of Canada (NSERC).

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zeqing Bao
    • 1
  • Jiahui Cao
    • 1
  • Guangbo Kang
    • 1
  • Christopher Q. Lan
    • 1
    Email author
  1. 1.Department of Chemical and Biological EngineeringUniversity of OttawaOttawaCanada

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