Physicochemical characteristics of Monocrotophos and Endosulfan
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\r\n\tThis book intends to provide the reader with a comprehensive overview of the current epidemiology, valuable information in relation to the management of specific poisoning agents, and important evidence-based developments in the toxicology field, with special focus on children, who are a more vulnerable population for severe poisonings. Its aim is to be a practical handbook to aid health care professionals involved in individual care of patients poisoning.
It was 2.4 billion (Ga) years ago that oxygen accumulated atmosphere began in our planet and cyanobacteria (earlier known as Bluegreen algae) are inhabitant of almost 3.5 billions years ago. This oxygenic atmosphere lead to the evolution of life on the earth. The exponential growth rate and long life span of human beings now a days creating a population bomb which is going to affect the environmental stability. In present day scenario of population explosion, it is essential to increase food production to meet the food demands and to maintain the socioeconomic status of the people in all the developing countries including India. In the year 2050, India will reach to the highest population (1.22 billion in 2012), within this globe total population of world will be approx 9.1 billion in 2050 (Carvalho, 2006). The immediate response to increase food production in limited agricultural land areas is possible by intensive use of agrochemicals. Agrochemicals include two large groups of compounds: chemical fertilizers and pesticides. The use of chemical fertilizers tremendously increased worldwide since 1960s and was largely responsible for the ‘‘green revolution’’, i.e. the massive increase in production obtained from the same surface of land with the help of mineral fertilizers and intensive irrigation. The revolution was assisted also with the introduction of more productive varieties of crops.
The use of pesticides, including insecticides, fungicides, herbicides, rodenticides, etc., to protect crops from pests, allowed to significantly reduce the losses and to improve the yield of crops. The application of different agrochemicals is region specific. In the tropical regions, where insect pests and plant diseases are more frequent, pesticides are generally applied in massive amounts, both in small farms as well as in cash crop. It has been reported that especially the organochlorine and organophosphorus pesticide residues, are found in soils, atmosphere and in the aquatic environment in relatively high concentrations (Carvalho et al., 1997). Pesticides are poisons, intentionally dispersed in the environment to control pests but they also act upon other species causing serious side effects on non-target species and destabilise the ecosystem. Cyanobacteria the natural nitrogen engineer of the soil are also adversely affected by indiscriminate use of pesticides.
Increasing rate of population
World production of formulated pesticides. Data for year 2005 is estimated (sourse Agrochemical service,2000)
Physicochemical characteristics of Monocrotophos and Endosulfan
Cyanobacteria are the most diversified ecologically, most successful and evolutionarily most important group of photosynthetic prokaryotes (Peschek et al., 1994) and maintain the homeostasis of nitrogen budget of the rice agroecosystem by photobiological nitrogen fixation in a specialized cell called heterocyst (Fay et al., 1968) at almost zero cost (Mishra & Pabbi 2004). Diversity and evolutionary information of cyanobacteria are available in the internet and for images one can search for “cyanobacteria, images” using Google. Most paddy soils have a natural population of cyanobacteria as they grow and multiply at the simple expense of water, light and air (Fay 1983). Soil nitrogen is the main source of nitrogen for crop growth and rice plant consume 50% of soil nitrogen (Fernandez-Valiante et al., 2000). Several reports are available on the adverse effect of agrochemicals on cyanobacteria (Marsac& Houmard, 1993; Das & Adhikary, 1996; Kapoor & Arora, 2000a, 2000b;Shikha & Singh, 2004; Xia, 2005; Kim & Lee, 2006). Although a lot of work has been done on the effect of pesticide in general, no attempt has been made on the effect of pesticide in locally growing cyanobacteria of Western Odisha, India. Farmers of this region use Monocrotophos and Endosulfan on a large scale in rice fields as both the pesticide have broad spectrum activity and they control the attack of insects; the physicochemical properties of both pesticides are given in Table 1.
BGA biofertilizer are added to rice fields to increase the fertility of soil and to minimize dependence on chemical fertilizer. The aim of the present study was to investigate whether Anabaena sp. and Nostoc sp., the locally isolated rice field cyanobacteria can be recommended to use as biofertilizer by tolerating the deleterious effect of Monocrotophos and Endosulfan. The chapter presents experimental results to illustrate the effects of Monocrotophos and Endosulfan in time and concentration dependent manner on growth, pigments and photosynthesis of these two alga.
Two species of heterocystous cyanobacteria belonging to genera Anabaena and Nostoc isolated from rice field. Selection of these two genus was based on their relatively better growth rate and wider occurance. Two commercial grade pesticide i.e.Monocrotophos (organophosphate 36%SL) and Endosulfan (organochlorine 35%EC) were used in the investigation. Fresh stock solutions of these pesticides were prepared in double distilled water and added to the culture medium to obtain the desired concentration. pH of all the medium was adjusted to 7.4 prior to sterilisation. Experiments were conducted in 15×150mm Borosil test tube containing 10 ml of nitrogen free BG11 medium (Rippka et al.,1979) and by inoculating equal amount of homogenized culture suspension (absorbance of the inoculum of each organism from their exponential growth phase at 760nm was 0.4 always). The medium contained various concentration of Monocrotophos (20,50,100 &150ppm) and Endosulfan (1,3,5,10 and 15 ppm),
Growth was measured by light scattering technique by taking the absorbance at 760nm, Chl a pigment of the cyanobacterial cells were extracted with 80% chilled acetone. Absorbance of the acetone extract was recorded at 660 nm and the amount of Chl a was determined using extinction coefficient of Mackinney, 1941.
Algal suspension was homogenized in a glass hand-homogenizer for 5 minutes and then centrifuged at 3500 rpm for 10 minutes. After centriguation, the pellet containing algal cells was resuspended in 50 mM tris-HCl buffer, pH 7.8 containing 175 mM NaCl. Room temperature Chl a fluorescence emission of algal suspension was measured as per Panda (1999) in a spectrofluorimeter (Hitachi, model, 650-40, Japan). For all scanning, a slit width of 10 nm was used. The whole cell algal suspension equivalent to 10 g of Chl in a total volume of 3 ml containing 50 mM Tris-HCl buffer and 175 mM NaCl (pH 7.8) was excited at 450 nm and emission was recorded at 685 nm for PS II and 735 nm for PS I emission.
The same algal suspension was also used to measure the excitation emission. During scanning, the emission was monitored at 685 nm and a slit width of 10 nm was maintained. Excitation emission was recorded at 439 nm, 471 nm and 485 nm. The excitation energy transfer from Car to Chl was measured by exciting the algal suspension at 475 nm and 600 nm. The emission was recorded at 685 nm for PS II and 735 nm for PS I. Efficiency of the energy transfer was assessed by calculating the ratio of excitation at 475 nm to 600 nm as described by Gruszescki et al., 1991.
Fluorescence polarization was measured by exciting the algal suspension at 620 nm and polarization was recorded at 685 nm. Polarization (P) was calculated as per the following formula of Swain et al., 1990.
where,I = intensity of fluorescence
v = vertical geometry of the polarizer
h = horizontal geometry of the analyzer
The 2,6-dichlorophenol indophenol (DCPIP) photoreduction was measured spectrophotometrically as described by Swain et al., 1990 with modification. 3 ml of reaction mixture contained whole cell algal suspension (equivalent to 10 g Chl), 50 mM Tris-HCl buffer (pH 7.8) and 175 mM NaCl. This reaction mixture was illuminated for 30 seconds with saturating white light (7x104 ergs cm-2 sec-1) coming from a projector lamp. The incident radiation beam was passed through a water filter to minimize infrared radiation. The photoreduction of the dye was measured at 600 nm. The reduction of the dye is expressed as moles DCPIP reduced/mg Chl/hr.
Photosynthetic efficiency of algal suspension in terms of chlorophyll fluorescence was measured at room temperature using a Plant Efficiency Analyzer (Handy PEA, Hansatech Instruments, Norfolk, UK). The Fv/Fm of algal suspension was measured by the Handy PEA after 20 minutes dark-adaption.
The nitrogen-fixing cyanobacteria represent as one of the prominent component of microbial population in wetland soils, especially in rice fields. They significantly contribute to soil fertility as a natural biofertilizer (Kumar & Kumar, 1998). Some cyanobacterial strains that thrive and grow in rice fields release small quantities of the major fertilizing product ammonia and small polypeptides during active growth whereas most of the other fixed products become available mainly through autolysis and decomposition (Hammouda, 1999). Therefore, cyanobacteria are considered as a vital component of the rice agroecosystem. However, excessive use of pesticides has a detrimental effect on the growth of these beneficial microorganisms, soil fertility and ultimately on the crop productivity. The effect of pesticides on the population of nitrogen fixing organisms varies with characteristics of the species and chemical nature of the pesticide.
Growth response of two different species of heterocystous cyanobacteria namely Anabaena sp. and Nostoc sp. to different concentrations of insecticide Monocrotophos is shown in Fig.3. Experiments showed that Anabaena sp. tolerated up to 100 ppm whereas Nostoc sp. tolerated upto 150 ppm of the insecticide where as for Endosulfan its limit was 5ppm & 15 ppm respectively. Growth curves indicate that both the algae showed lag phase up to 3rd day of incubation followed by rapid growth up to 12th day in case of control and treated (20 ppm for Anabaena sp. and 50 ppm for Nostoc sp.) samples. The present study of growth pattern of Anabaena sp. and Nostoc sp suggest that the tolerance capacity of Nostoc is more compared to Anabaena for both the pesticides. Both the alga also tolerate higher doses of pesticides Monocrotophos compared to Endosulfan. Endosulfan has more inhibitory effect on growth of both the BGA. These findings support the observation of Das and Adhikary, 1996 that organophosphate insecticide is less toxic than organocholorine. Several authors (Rath & Adhikary, 1994; Goyal et al., 1994; Das &Adhikary, 1996; Anand & Subramanian 1997; Kaur &Ahluwalia, 1997; Kapoor & Arora, 1998; 2000 a, 2000b; Xia, 2005; Chen et al.,2007; Kumar et al.,2008; Bhattacharyya et al., 2011) have reported inhibitory effect of various pesticides on the growth of cyanobacteria. The inhibition of growth in different concentrations of the pesticides is due to alteration in synthesis of nucleic acids, amino acids and proteins (Kumar et al., 2011) as well as due to impairment in photosynthetic activity (Lal &Saxena, 1980) of the BGA.
Almost all oxygenic photosynthesizer, with the exception of Acaryochloris a cyanobacterium, use chlorophyll a (BjÖrn et al., 2009). The amount of Chl content in the photosynthetic unit of cyanobacterial cell indicates its growth and physiological status. Fig.4 depicts the kinetics of Chl a accumulation and loss in Anabaena sp. and Nostoc sp. treated with different concentrations of Monocrotophos (Fig.4B) and Endosulfan (Fig.4A) in the BG11 medium over 15 days of incubation along with the control. The kinetics pattern was closely similar to that of growth kinetics with minor variations for both the treated and control samples. Except in Anabaena (control sample), the Chl a content reached its maximum level on the 10th day of incubation followed by decline both in control and treated samples. The rate of pigment loss in treated sample was more than that of control. As indicated from the levels, the pigment synthesis was very less in Anabaena with 100 ppm Monocrotophos, 5ppm Endosulfan and Nostoc with 150 ppm Monocrotophos, 15 ppm Endosulfan treatment. In these two concentration of pesticides the pigment levels were almost same with the initial level of the pigment in both the samples through out the experimental period of 15 days. The Chl a content was maximum on 10th day though growth rate was maximum at 12th day of incubation. The pigment content declined after 10th day of incubation in all treated samples and control of Nostoc sp. On the other hand, except in the control samples of Anabaena sp. pigment level was highest on 10th day then followed by a sharp decline.
Effect of different concentration of Endosulfan (A) &Monocrotophos (B) on growth of Anabaena and Nostoc cultured under laboratory condition.
Effect of different concentration of Endosulfan(A) &Monocrotophos (B) on Chl a of Anabaena and Nostoc cultured under laboratory condition.
The data indicates that Chl a accumulation and loss in the present study is also time and concentration dependent manner (Fig 4). The pesticides are known to interfere with the synthesis of Chl a pigment by inhibiting the formation of porphyrin rings (Moreland, 1980; Lal and Saxena, 1980). In the present work, the low level of Chl in pesticide treated samples supports the observations of Das & Adhikary, 1996, Megharaj et al., 2011, Kumar et al., 2008, Battah et al., 2001; Sikha & Singh, 2004 and Xia, 2005.
The DCPIP photoreduction reflects the photochemical potential of PS II. The activities also reflect the coupling between light absorption and photochemical reaction of the thylakoid membrane. In the present study the rate of dye reduction in control and pesticides treated samples of both the alga resemble with the kinetics of Chl a accumulation and loss. The rate of dye reduction in treated samples is low compared to the control (Table 2 and 3). This could be due to loss of pigments and protein content of the organism under the pesticide treated conditions due to stress-induced formation of ROS (Behera & Choudhury, 2001; Hideg & Vass, 1996) and possible changes in the thylakoid microenvironment. The degradation of D1 protein under stress condition may be another reason (Long & Humphries, 1994). These observations are similar to the findings of Shikha and Singh,2004, Bhattacharyya et al., 2011.
µ mol of DCPIP Reduced (Anabaena sp) | |||||||||||
Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day | Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day |
Control | 20±1.2 | 101±3.6 | 175±3.5 | 241±5.5 | Control | 20±1.2 | 101±1.8 | 175±5.9 | 241±8.5 | ||
Monocrotophos | 20 | 20±1.2 | 94±2.7 | 180±6.2 | 152±2.9 | Endosulfan | 1 | 20±1.2 | 91±22 | 165±8 | 135±6 |
50 | 20±1.2 | 83±1.1 | 140±2.8 | 132±3.6 | 2 | 20±1.2 | 80±0.8 | 120±3 | 110±7 | ||
100 | 20±1.2 | 65±5.3 | 95±3.3 | 85±2.6 | 3 | 20±1.2 | 65±1.6 | 95±5 | 75±3 |
Electron transport efficiency of PS II in terms of DCPIP photoreduction of Anabaena sp grown under different concentrations of Monocrotophos and Endosulfan in laboratory condition. (±SD)
µ mol of DCPIP Reduced (Nostoc Sp) | |||||||||||
Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day | Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day |
Control | 29±2.6 | 145.8±4.2 | 190±8 | 142±6.5 | Control | 29±2.6 | 145.8±7 | 190±11 | 142±8.2 | ||
Monocrotophos | 50 | 29±2.6 | 94±6 | 126±6 | 84±3.2 | Endosulfan | 5 | 29±2.6 | 100.8±3.8 | 116±7 | 54.6±5 |
100 | 29±2.6 | 55.5±4 | 96±7 | 49.6±3.6 | 10 | 29±2.6 | 84±3.3 | 102±6 | 50±6 | ||
150 | 29±2.6 | 25.2±2.6 | 45.8±5.4 | 30±6 | 15 | 29±2.6 | 82±3.4 | 94±8 | 32.4±4 |
Electron transport efficiency of PS II in terms of DCPIP photoreduction of Nostoc Spgrown under different concentrations of Monocrotophos and Endosulfan in laboratory condition. (±SD)
Analyses of fluorescence emission, excitation emission, fluorescence polarization and excitation energy transfer of thylakoids provide information about the structural organization and the microenvironment of thylakoid membrane. The analyses also give information about the degree of coupling of different pigment complexes. Information about the coupling of light absorption and photochemical reactions could also be obtained by monitoring fluorescence characteristics of whole cells of the cyanobacteria. Therefore, to determine the structural and functional status of the thylakoid, fluorescence excitation, emission and polarization measurements are very much important. Campbell et al.,1998 have opined that fluorescence analysis is an integral part of the studies of photosynthesis in BGA. Shikha & Singh, 2004 have extensively used fluorescence studies to monitor photosynthetic status of A. doliolum treated with herbicide glyophosphate.
Cyanobacteria fluorescence characteristics are distinct from those of plants due to their specific structural and functional properties (Campbell et al., 1998). These include significant fluorescence emission from the light harvesting phycobiliproteins, large and rapid changes in fluorescence yield (state transitions) which depend on metabolic and environmental conditions as well as flexible and overlapping respiratory and photosynthetic electron transport chains. In cyanobacteria, the photosynthetic system is tightly linked to other principal metabolic pathways and is itself a major metabolic sink for iron, nitrogen and carbon skeletons. Therefore, Chl fluorescence signals can provide rapid, real-time information on both photosynthesis and overall acclimation status of cyanobacteria.
The fluorescence characteristics of test organismsboth in control and insecticides treated samples are shown in Table4 and 5. There is gradual increase in fluorescence intensity at F685 and F735 in all conditions over 15 days of incubation under laboratory condition except on 5th day of control. The ratios of F685 to F735 increased from 5th day till the end of experiment both in control and treated samples. The ratios were also more in treated samples than in the control. The ratios gradually increased as the concentration of the insecticide and treatment period increased in both the organisms.
Fluorescence Intensity (Arbitrary unit) | |||||||||||||
Treatment | Dose (ppm) | F685 | F735 | F685/F735 | |||||||||
0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | ||
Control | 0 | 91.0 | 88.0 | 137.0 | 195.0 | 26.5 | 25.0 | 30.0 | 36.0 | 3.4 | 3.52 | 4.50 | 5.40 |
Monocroto phos | 20 | 91.0 | 100.0 | 167.0 | 202.0 | 26.5 | 28.0 | 34.0 | 40.0 | 3.4 | 3.57 | 4.90 | 5.05 |
50 | 91.0 | 122.0 | 178.0 | 240.0 | 26.5 | 32.0 | 36.0 | 42.0 | 3.4 | 3.81 | 4.94 | 5.71 | |
100 | 91.0 | 139.0 | 195.0 | 270.0 | 26.5 | 36.0 | 39.0 | 46.0 | 3.4 | 3.86 | 5.00 | 5.84 | |
Endosulfan | 1 | 91.0 | 110.0 | 183.0 | 299.0 | 26.5 | 27.0 | 37.0 | 54.0 | 3.4 | 4.07 | 4.90 | 5.53 |
3 | 91.0 | 122.0 | 193.0 | 314.0 | 26.5 | 29.0 | 38.0 | 55.0 | 3.4 | 4.20 | 5.07 | 5.70 | |
5 | 91.0 | 152.0 | 218.0 | 338.0 | 26.5 | 35.0 | 41.0 | 56.0 | 3.4 | 4.34 | 5.30 | 6.03 |
Chlorophyll a fluorescence emission of Anabaena grown in control and different concentrations of Monocrotophos and Endodahan in laboratory conditions.
Fluorescence Intensity (Arbitrary unit) | |||||||||||||
Treatment | Dose | F685 | F735 | F685/F735 | |||||||||
(ppm) | 0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | |
Control | 97.5 | 92.0 | 146.0 | 204.0 | 21.6 | 20.0 | 24.6 | 34.0 | 4.5 | 4.6 | 5.9 | 6.0 | |
50 | 97.5 | 108.0 | 177.0 | 220.0 | 21.6 | 22.1 | 29.0 | 36.0 | 4.5 | 4.9 | 6.1 | 6.1 | |
Monocrotophos | 100 | 97.5 | 134.0 | 188.0 | 257.0 | 21.6 | 25.2 | 30.3 | 39.1 | 4.5 | 5.3 | 6.2 | 6.6 |
150 | 97.5 | 147.0 | 203.0 | 284.0 | 21.6 | 26.3 | 31.7 | 42.3 | 4.5 | 5.6 | 6.4 | 6.7 | |
Endosulfan | 5 | 97.5 | 102.0 | 151.0 | 280.0 | 21.6 | 21.8 | 25.0 | 44.0 | 4.5 | 4.7 | 6.0 | 6.4 |
10 | 97.5 | 114.0 | 164.0 | 294.0 | 21.6 | 21.6 | 24.8 | 42.5 | 4.5 | 5.3 | 6.6 | 6.9 | |
15 | 97.5 | 148.0 | 198.0 | 328.0 | 21.6 | 26.6 | 28.4 | 45.8 | 4.5 | 5.6 | 6.6 | 7.1 |
Chlorophyll a fluorescence emission of Nostoc grown in control and different concentrations of Monocrotophos and Endodahan in laboratory conditions.
Chlorophyll a fluorescence emission spectra of whole algal cells measured at room temperature exhibit usually two emission maxima, the first at 685 (F685) nm and the second at 735 (F735) nm. F685 is considered as the emission from PS II and F735 from PS I (Papageorgiou, 1975). A gradual increase in fluorescence intensity (Table 4 and 5) at 685 nm (F685) and 735 nm (F735) is observed over 15 days of incubation of both the alga in control as well as insecticides treated samples. Increase in fluorescence intensity particularly during developmental stage has been ascribed due to improved organization of light harvesting (antenna) complexes of the thylakoid which results in trapping of more solar energy. However, if proportional increase in the photochemical activity will not take place, then the absorbed energy is emitted as fluorescence (Krause & Weis, 1991; Krieger et al., 1992). On the other hand, uncoupling of the photosynthetic pigments and RC during natural ageing or under stress conditions may also lead to increase in the fluorescence intensity. Continuous increase in the fluorescence intensity in the control sample could be due to higher trapping of solar energy as the algal cell improves their thylakoid organization during the culture. However, without proportional increase in photochemical activities, the excitation energy is emitted as fluorescence. On the other hand increase in the fluorescence intensity in the insecticides treated samples is much higher than the control. This suggests that the pesticides have induced uncoupling of light harvesting system and electron transport resulting emission of excitation energy as fluorescence. Higher susceptibility of PS II compared to PS I to different stress such as water stress (Deo and Biswal, 1998), light stress (Behera et al., 2002), oxidation stress (Behera and Choudhury, 2001) etc. have been reported in different plant systems. The gradual increase in the ratio of F685 and F735, when the concentration of pesticides increase suggests that PS II is more affected by the treatments.
Table-6 depicts the effect of different concentrations of pesticides on the ratio of peak heights of fluorescence excitation emission of Anabaena sp. The ratios of 471 nm to 439 nm and 485 nm to 439 nm increased throughout the 15 days of incubation in all concentrations of Monocrotophos and Endosulfan used along with the control sample. However, compared to the control, the ratio declined with insecticide treatment as well as with the increase in concentration of both pesticides.
Ratio of Peak Heights(a.u) | |||||||||
Dose | E471/E439 | E485/E439 | |||||||
Treatment | (ppm) | 0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day |
Control | 0.489 | 0.988 | 1.213 | 1.500 | 0.625 | 1.195 | 1.325 | 1.632 | |
Monocrotophos | 20 | 0.489 | 0.940 | 1.208 | 1.478 | 0.625 | 1.010 | 1.217 | 1.417 |
50 | 0.489 | 0.891 | 1.112 | 1.155 | 0.625 | 0.921 | 1.200 | 1.253 | |
100 | 0.489 | 0.695 | 0.789 | 0.918 | 0.625 | 0.900 | 1.182 | 1.208 | |
Endosulfan | 1 | 0.489 | 0.825 | 1.094 | 1.132 | 0.625 | 1.093 | 1.131 | 1.348 |
3 | 0.489 | 0.821 | 1.087 | 1.021 | 0.625 | 0.956 | 1.121 | 1.187 | |
5 | 0.489 | 0.624 | 0.721 | 0.802 | 0.625 | 0.795 | 0.860 | 0.934 |
Effect of different concentrations of Monocrotophos and Endosulfan on ratio of peak heights of fluorescence excitation of Anabaena grown in laboratory conditions.
The ratio of peak heights of fluorescence excitation emission of Nostoc sp. is represented in Table-7 both in control and pesticides treated (50, 100 and 150 ppm of Monocrotophos and 5, 10 and 15 ppm of Endosulfan) samples over 15 days of incubation under laboratory condition. Similar trend of increase in the ratio of 471 nm to 439 nm was also noted in Monocrotophos and Endosulfan treated samples as well as in control over 15 days of incubation. However, the increase was less in insecticide treated samples and more so when the concentration of the insecticide was more. On the other hand, except in control, no definite increasing or decreasing trend in the ratio of 485 nm to 439 nm was noted in the treated samples.
Treatment | Dose (ppm) | Ratio of Peak Heights(a.u) | |||||||
E471/E439 | E485/E439 | ||||||||
0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | ||
Control | 0 | 0.627 | 1.055 | 1.368 | 1.600 | 1.304 | 1.505 | 1.602 | 1.678 |
Monocrotophos | 50 | 0.627 | 1.040 | 1.150 | 1.320 | 1.304 | 1.202 | 1.310 | 1.408 |
100 | 0.627 | 0.932 | 0.983 | 1.152 | 1.304 | 1.084 | 1.093 | 1.101 | |
150 | 0.627 | 0.729 | 0.765 | 0.997 | 1.304 | 0.935 | 1.012 | 1.087 | |
Endosulfan | 5 | 0.627 | 0.757 | 0.925 | 1.162 | 1.304 | 1.454 | 0.835 | 1.303 |
10 | 0.627 | 0.747 | 0.854 | 1.051 | 1.304 | 1.359 | 0.519 | 1.131 | |
15 | 0.627 | 0.629 | 0.765 | 0.908 | 1.304 | 0.909 | 0.429 | 0.933 |
Effect of different concentrations of Monocrotophos and Endosulfan on ratio of peak heights of fluorescence excitation of Nostoc grown in laboratory conditions.
The study of fluorescence excitation characteristics of chloroplast is used to explain the spatial arrangement and coupling of different pigment molecules in the thylakoid membrane (Behera & Choudhury, 1997). The changes in the relative peak values of fluorescence excitation at 471 (E471) nm and 485 (E485) nm with reference to peak at 439 (E439) nm reflects the alterations in pigment protein complexes in the thylakoid domain during development of the organism. Table 6 and 7 indicate the changes in the ratio of peak heights in control and with different concentration of Monocrotophos and Endosulfan. The decrease in the ratio of 471 nm to 439 nm is attributed to gradual decrease in coupling between Chl and Car with the increase of the duration of incubation period with the insecticides.
The simple and direct proof of excitation energy transfer from Car and phycobilisomes (PBS) to Chl comes from the contribution of the light absorbed by the Car and PBS in Chl a fluorescence. At shorter wavelength, only Chl, Car and PBS and at longer wavelength only Chl is responsible for the absorption. There is a significant decline in the capacity of energy transfer in PS II for all concentrations of Monocrotophos and Endosulfan in both the alga compared to the control (Table 8 and 9). The temporal kinetics of energy transfer follows similar pattern like the kinetics of DCPIP photoreduction (Table 2 and 3) and photosynthetic efficiency of PS II during the 15 days of incubation. The decrease in the Chl a contents in the insecticide treated samples (Fig. 4) may be correlated to certain conformational changes in the pigment protein complex in the photosystem in turns affecting the excitation energy transfer (Gruszescki et al., 1991). The energy transfer from Car to Chl is increasingly hampered (Table 8 and 9) as the concentration of the pesticides increased.
Though the values are different, the kinetics of energy transfer in PS I is similar to that of PS II for both Anabaena sp. and Nostoc sp. in control and treated samples. However, compared to PS II, PS I is less susceptible to the insecticide treatment in both the alga. Smaller changes in excitation energy transfer in PS I suggest that PS I is less effected even under stress condition. Relatively less susceptibility of PS I compared to PS II to various stress conditions has been shown earlier by various authors (Choudhury & Choe, 1996; Deo & Biswal, 1998; Campbell et al., 1998; Behera et al., 2002)
Treatment | Dose (ppm) | Efficiency of excitation energy transfer (a.u) | |||||||
PS II | PS I | ||||||||
0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | ||
Control | 0 | 1.48 (100) | 1.95 (131) | 2.15 (145) | 2.10 (142) | 1.22 (100) | 1.64 (134) | 1.83 (150) | 1.80 (147) |
Monocrotophos | 20 | 1.48 (100) | 1.87 (126) | 2.00 (135) | 1.92 (130) | 1.22 (100) | 1.59 (130) | 1.74 (143) | 1.69 (138) |
50 | 1.48 (100) | 1.75 (118) | 1.93 (130) | 1.80 (122) | 1.22 (100) | 1.52 (125) | 1.67 (137) | 1.58 (130) | |
100 | 1.48 (100) | 1.67 (112) | 1.70 (114) | 1.62 (109) | 1.22 (100) | 1.41 (116) | 1.52 (125) | 1.46 (120) | |
Endosulfan | 1 | 1.48 (100) | 1.82 (123) | 1.98 (134) | 1.88 (127) | 1.22 (100) | 1.58 (129) | 1.70 (149) | 1.67 (137) |
3 | 1.48 (100) | 1.70 (115) | 1.87 (126) | 1.82 (123) | 1.22 (100) | 1.54 (126) | 1.64 (134) | 1.56 (128) | |
5 | 1.48 (100) | 1.55 (105) | 1.64 (111) | 1.60 (108) | 1.22 (100) | 1.46 (120) | 1.54 (126) | 1.50 (122) |
Efficiency of excitation energy transfer from carotenoids to chlorophyll of PS II and PS I of Anabaena grown under control and different concentrations of Monocrotophos and Endosulfan in laboratory conditions.
Treatment | Dose (ppm) | Efficiency of excitation energy transfer (a.u) | |||||||
PS II | PS I | ||||||||
0 day | 5 day | 10 day | 15 day | 0 day | 5 day | 10 day | 15 day | ||
Control | 0 | 0.558 (100) | 0.714 (128) | 0.822 (147) | 0.812 (145) | 0.469 (100) | 0.615 (131) | 0.724 (154) | 0.703 (150) |
Monocrotophos | 20 | 0.558 (100) | 0.708 (127) | 0.794 (142) | 0.760 (136) | 0.469 (100) | 0.600 (128) | 0.613 (146) | 0.656 (140) |
50 | 0.558 (100) | 0.675 (121) | 0.730 (131) | 0.712 (127) | 0.469 (100) | 0.572 (122) | 0.637 (136) | 0.609 (130) | |
100 | 0.558 (100) | 0.655 (113) | 0.647 (116) | 0.608 (109) | 0.469 (100) | 0.539 (115) | 0.562 (120) | 0.529 (113) | |
Endosulfan | 5 | 0.558 (100) | 0.704 (126) | 0.783 (140) | 0.753 (135) | 0.469 (100) | 0.605 (129) | 0.680 (145) | 0.656 (140) |
10 | 0.558 (100) | 0.671 (120) | 0.725 (130) | 0.704 (126) | 0.469 (100) | 0.586 (125) | 0.635 (136) | 0.609 (130) | |
15 | 0.558 (100) | 0.619 (111) | 0.636 (114) | 0.638 (110) | 0.469 (100) | 0.558 (119) | 0.572 (122) | 0.548 (117) |
Efficiency of excitation energy transfer from carotenoids to chlorophyll of PS II and PS I of Nostoc grown under control and different concentrations of Monocrotophos and Endosulfan in laboratory conditions.
Changes in fluorescence polarization of the two algal species under control and insecticides treated conditions give further information on the status of pigment-protein complexes with reference to their microenvironment in thylakoid membrane. The increase in polarization during the initial stage of incubation in all treated samples compared to the control (Fig.5 ) could be due to the poor coupling between the pigment protein complex and RC (Behera & Choudhury, 1997). On the other hand, increase in polarization in the later phase of growth (10-15 days of incubation) could be due to disorganization of pigment protein complexes and RC, leading to a decrease in quantum migration. Alternatively, peroxidation of lipid during later stage may induce gel phase of the thylakoid membranes restricting the mobility of Chl dipole (Panda & Biswal, 1989 and 1990). This may cause an increase in the polarization value at 100 and 150 ppm of Monocrotophos and 5 and 15 ppm of Endosulfan treatment to the Anabaena sp and Nostoc sp. respectively. Significant high levels of polarization suggests a greater disorganization of thylakoid membrane due to high lipid peroxidation (Kumar et al., 2008).
Effect of different concentration of Endosulfan(A) &Monocrotophos (B)on fluorescence polarization of Nostoc and Anabaena cultured under laboratory condition.
Photosynthetic efficiency of PS II can be measured by monitoring the ratio Fv/Fm. It is known that photoinhibition occurs when the rate of excitation energy captured exceeds the rate of consumption in photosynthetic reactions (Osmond, 1981; Powles, 1984). Photoinhibition in terms of Fv/Fm has been found both in higher plants (Panda et al., 2006; Rodrigues et al., 2007) as well as in algae (Ying and Hader, 2002; Xia, 2005; Chen et al., 2007). The primary site of photoinhibition is the reaction centre (D1 protein) of PS II (Demming and Bjorkman, 1987; Jordan, 1996). Photoinhibition is manifested as a decrease in oxygen evolution (Krause, 1988) and photochemical efficiency (Falk and Samuelsson, 1992). The data on the measurement of Fv/Fm during the laboratory incubation of the different samples (Table 10 and 11) show similar kinetics like that off the photosynthetic pigment and protein accumulation and loss and DCPIP photoreduction of both the BGA in control and treated (pesticide) samples. As the concentration of pesticides increased, photosynthetic efficiency decreased. This shows that both the species of cyanobacteria are sensitive to higher concentration of pesticides. Pesticides, particularly at higher concentration may (directly or indirectly) cause damage to D1 protein of PS II leading to photoinhibition. The decrease in Fv/Fm ratio in pesticide treated sample could also be due to decrease in Phycocyanin, Phycoerythrin and Allophycocyanin content, which results in a decrease of light energy absorption by phycobilisomes and reduction of photochemical efficiency (Fv/Fm) of PS II. Similar observations have been reported by Xia, 2005 in N. sphaeroids. The present finding is in confirmatory to the observation of Xia, 2005.
PS II efficiency | |||||||||||
Nostoc | |||||||||||
Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day | Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day |
Control | 0.370 (100) | 0.524 (142) | 0.562 (152) | 0.536 (145) | Control | 0.370 (100) | 0.524 (142) | 0.562 (152) | 0.536 (145) | ||
Monocrotophos | 50 | 0. 370 (100) | 0.500 (135) | 0.515 (139) | 0.473 (128) | Endosulfan | 5 | 0.370 (100) | 0.458 (124) | 0.520 (141) | 0.467 (126) |
100 | 0. 370 (100) | 0.431 (116) | 0.500 (135) | 0.429 (116) | 10 | 0.370 (100) | 0.387 (105) | 0.455 (123) | 0.375 (101) | ||
150 | 0. 370 (100) | 0.375 (101) | 0.404 (109) | 0.387 (105) | 15 | 0.370 (100) | 0.313 (85) | 0.333 (90) | 0.316 (85) |
Photosynthetic efficiency (in term of Fv/Fm) of PS II of Nostoc grown under different concentrations of Monocrotophos and Endosulfan in laboratory condition.
Anabaena | |||||||||||
Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day | Treatment | Dose (ppm) | 0 day | 5 day | 10 day | 15 day |
Control | 0.350 (100) | 0.520 (149) | 0.556 (159) | 0.515 (147) | Control | 0.350 (100) | 0.520 (149) | 0.556 (159) | 0.515 (147) | ||
Monocrotophos | 20 | 0. 350 (100) | 0.482 (138) | 0.500 (143) | 0.468 (142) | Endosulfan | 1 | 0.350 (100) | 0.404 (115) | 0.511 (146) | 0.455 (130) |
50 | 0. 350 (100) | 0.442 (126) | 0.482 (138) | 0.429 (123) | 3 | 0.350 (100) | 0.316 (90.3) | 0.419 (119.7) | 0.327 (93.42) | ||
100 | 0. 350 (100) | 0.375 (107) | 0.419 (120) | 0.351 (100.3) | 5 | 0.350 (100) | 0.313 (89.42) | 0.375 (107) | 0.308 (88) |
Photosynthetic efficiency (in term of Fv/Fm) of PS II of Anabaena grown under different concentrations of Monocrotophos and Endosulfan in laboratory condition.
The insecticide Monocrotophos and Endosulfan affected photosynthetic function which may have inhibited the growth of both the cyanobacteria by affecting the production of photosynthetic pigments in the antenna complex, electron transfer, and photosynthetic efficiency of PS-II. Both the cyanobacteria responded differently to both the pesticides with time and concentration dependent manner. Endosulfan has more inhibitory effect than Monocrotophos. Tolerance capacity of Nostoc sp. is more than Anabaena sp.. Our data indicate that use of Endosulfun may pose a risk to diazotropic cyanobacterium, and consequently to the nitrogen economy of the soil. It is currently understood from the extensive studies conducted so far on impacts of many pollutants on cyanobacteria and microalgae that evaluation with a wide taxonomic range in different ecosystem is necessary to arrive at a generalization on the nontarget effects of pollutant (Ramakrishnan et al., 2010) However, the effect of pesticides on the population of nitrogen-fixing cyanobacteria in rice fields also depends on pesticide concentrations, moreover, toxicity is affected not only by the types of pesticide, but also by the taxonomic groups and species. Since Endosulfan has more deleterious effect on natural engineer of the rice field (BGA) it’s use be limited to maintain the stability of paddy ecosystem.
Authors are thankful to HOD school of life Sciences, Sambalpur University for giving all types of facilities.
Carbon dots (CDs) are nanoparticles generated from organic/inorganic sources, was first discovered in 2004 when single-wall carbon nanotubes were electrophoretically purified [1]. CDs can be classified as carbon nanomaterials that are less than 10 nm in size, they are the latest class of fluorescent nanoparticles [2]. CDs have attracted the interest of researchers in diverse fields of science and technology such as; optoelectronics [3], environmental pollution and remediation [4], biosensor [5], bio-imaging and biomedical applications [6, 7].
CDs possess properties such as being dimensionless, durable, large surface area, enhanced porosity and stability, ease of being functionalized, fluorescence emission, biocompatibility and low toxicity [5, 8]. These properties of CDs can be applied to improve the environment and human health [4, 9, 10].
A toxic rival to the CDs is the popular semiconductor nanocrystals popularly known as quantum dots (QDs). The QDs are a type of semiconductor nanoparticles with diameter range from 1 to 10 nm [11]. More so, QDs normally are made from semiconducting materials, especially iron and cadmium, which are highly toxic and expensive to acquire [12]. Compared to QDs, CDs are considered best option with a high degree of biocompatibility, cost-effectiveness and non-toxic. It also serves as a suitable substitute to QDs in numerous areas of research such as bio-imaging, bio-sensing, pharmaceutical and fuel cells [13, 14].
Carbon dots (CDs) are suitable for the modification of electrode sensors. It combines fundamental aspects of biology, chemistry, and physical sciences, computer science and electrical engineering to meet various needs in a wide application field. Therefore, carbon as a sensor portrays several meanings, conditional upon what field the user subscribes [15, 16].
Over the years, various bulk materials and several processes and techniques have been developed and adopted by a wide range of researchers in the synthesis of CDs. These processes include the hydrothermal and microwave-assisted routes, heating, biogenic synthesis, thermal oxidation, ultra-sonification, subcritical water process (use of oil bath and salt bath), refluxing and chemical oxidation [17, 18, 19, 20, 21, 22, 23, 24, 25, 26].
Three important factors must be considered in synthesizing CDs which are control of size, uniformity of CDs in solvents, and mitigated aggregation [27]. Wang and Hu [28] confirmed that CDs carbonaceous aggregation tends to form during carbonization but this can be prevented when synthesized by methods such as electrochemical synthesis, hydrothermal, or by pyrolysis method.
The application of biological and agro-waste to synthesize CDs have been advocated in numerous research such as; cooking oil waste [29], egg-white and egg-yolk [30], orange juice [6] as well as eggshells [31]. Though it is advantageous to use waste biomaterials in the synthesis of CDs to avoid competition with essential food production [32], however, the downside of the application of biomass in the synthesis of CDs is lacking of essential purity and structural homogeneity to obtain homogenous fluorescent CDs for purposes of sensing minute concentrations of analytes [21, 33]. These had caused the application of clean materials to be used in the synthesis of homogeneous fluorescent CDs [2].
A competent carbon source for soluble CDs synthesis is needed to comply with the goals of green chemistry and not be in direct competition with essential food production and should be cheap to synthesize [34, 35, 36]. Research in the synthesis of CDs must consider low price of additives and less purification steps in case of using biomass as a precursor material.
Thus, the emphasis is necessary on the cost of producing typical CDs, not to be a replica of the currently observed situation with semiconductor QDs, with the high cost and potential environmental negative impact and yet to achieve its full potential in commercial applications [37, 38, 39].
Carbon dots (CDs) have emerged to be attractive materials due to their excellent photoluminescence (PL) properties and wide surface areas, which are needed for sensitive and selective sensing of analytes [40]. These qualities are owed to the characteristics of the carbon element at nano-dimension and five valence electrons to bind carbon atoms [31, 41]. The green and sustainable carbons dots refer to CDs that are synthesized from agro and biomaterials that can be readily available without depleting their sources [42].
CDs can be obtained from various source [3]. These sources include plants and animal origins such as bamboo leaves, woods, green algae, sugar cane, mangosteen, carica papaya, saffron, gringko, neem gum, prawn shells, orange, cucumber and pineapple [32, 43, 44, 45]. Further interesting applications of CDs have been reported in diverse sectors of the environment and health fields of science and technology [3, 32].
For instance, Pattanayak and Nayak, in 2013 [43] presented an eco-friendly synthesis of iron nanoparticles from various plants and spices extract. The synthesis of nanoparticles from plant parts (leaf) is essential since this will not require expensive processes that are involved mostly in biomaterial processing. Iravani et al., [46] demonstrated a green synthesis of metal nanoparticle using plants (emblica officinalis fruit extract) as a mean of mitigating the synthesis process of metal nanoparticles that are efficient and able to enhance green chemistry procedure for nanoparticles synthesis.
Liu [44], reported a research work on one-step green synthesized fluorescent carbon nano-dots from bamboo leaves for copper (ll) ion detection and demonstrated the exploration of bamboo leaves as a carbon source. Carbon nano-dots were synthesized hydrothermally and a resultant high quantum yield quantum dots, with sensitive Cu2+ detection at a limit of detection as low as 115 nM on a dynamic range from 0.333 to 66.6 μM. The zeta potential of the pristine carbon quantum dots was measured at −4.78 mV which changes to +13.8 mV after treatment with positively charged polyethyleneimine (a water-soluble cationic polymer).
Wembo et al., [47], researched on the economical and green synthesis of fluorescent carbon nanoparticles and their use as probes for sensitive and selective detection of mercury (II) ions. The adopted process by Wembo and colleagues was based upon the economy and green preparative strategy toward water-soluble fluorescent carbon nanoparticles with a quantum yield of 6.9% by a hydrothermal process using a low-cost waste from pomelo peel as a carbon source.
Piyushi, et al., [45] cultivated chlorella (a genus of single-cell green algae belonging to the phylum Chlorophyta) on brewery wastewater for nanoparticle biosynthesis. The method of bio-nanoparticle synthesis using chlorella algal biomass grown in single water sample were harvested from the culture medium by centrifugation at 4000 rpm for 5 min followed by washing with ultrapure water to eliminate impurities. Iron nanoparticles were synthesized by mixing 0.5 g (dry weight) Chlorella sp. MM3 with 5 mL of 0.1 M FeCl3 solution followed by incubation at 37 C for 48 h which entails long and tedious process.
Till et al., [48] synthesized CDs by microwave-assisted hydrothermal treatment of starch and Tris-acetate-EDTA. The process confirmed that nitrogen-doped CDs have emerged to be complementary to starch-derived CDs. Addition of nitrogen to CDs improved the yield of photoluminescence from 19% to 28%, making them promising luminescent materials for improving fluorescence of CDs. However, there is no added value in incurring additional chemicals during synthesis process of CDs. Starch is a better alternative to the use of nitrogen for synthesizing CDs. Till and colleagues observed the effect of nitrogen (N) additives, through the use of ethylenediaminetetraacetic acid (EDTA); tris (hydroxymethyl) aminomethane (Tris) and a combination of both (TAE-buffer) on the photophysical properties of CDs. Temperature (45 min at 230°C) plays an important role in the improved nitrogen-doped carbon structures [48].
Some researchers have adopted nitrogen for fluorescence and photoluminescence enhancement, but this approach has shown indistinct composition which required extensive purification steps. This, however, is environmentally not suitable and contravenes the concept of green chemistry since it involves many chemicals in the synthesis process [49].
Synthesis methods of CDs can be divided into two major parts; top-down and bottom-up as in Figure 1. Top-down starts from cutting the carbon materials into carbon particles or cleavage of larger carbonaceous materials such as carbon nanotube by laser ablation, arc discharge, electrochemical and candle/natural gas burner soot, and recently the hydrothermal route.
Synthesis methods of carbon dots (CDs).
The bottom-up route involves the use of molecules as support for localizing the growth of CDs by blocking aggregation during high-temperature treatment. However, this study explores the top-down process of CDs synthesis. As earlier stated the top-down approach concentrates on precursor carbonization that include microwave-assisted method, chemical oxidation, heating, and hydrothermal process [50].
It is a process removal of material from solid or liquid by irradiating it with a laser beam [51, 52, 53, 54]. Material evaporates or sublimates when the laser flux is low and converted to plasma at high laser flux. Goncalves and colleagues [51] reported the synthesis of CDs from carbon targets immersed in deionized water by direct laser ablation (UV pulsed laser irradiation). CDs were optimized and synthesized after being functionalized with NH2– polyethylene-glycol (PEG200) and N-acetyl-l-cysteine (NAC). To produce particles in tens of nanometer range by laser ablation, the energy is controlled within the incidence area of the precursor [54, 55].
Yu et al., [53] demonstrated the possibilities of relying on irradiating a toluene sample with a non-focused pulsed laser that is very different from the high powered laser irradiation employed in conventional ablation. This process by Yu and colleagues revealed an induced transformation of toluene into graphene sheaths, which subsequently produced fluorescent CDs. These nanoparticles can simply be functionalized using more than one molecule and stayed stable in an aqueous solution. It can also be applied to optical fiber devices through immobilization due to its stability in a specific optical nano-analytical sensor [56]. However, the equipment to conduct laser ablation is quite expensive and it needs technically skilled personnel to operate.
CDs were first discovered through this method accidentally when the separation of single-walled carbon nanotubes (SWNTs) were made using gel electrophoresis from carbon soot by arc discharge method. Carbon is formed when direct current arc voltage is applied in an inert gas across two graphite electrodes. The biggest challenge of this method is that it generates impurities that are difficult to purify [1].
Electrochemistry is another top-down approach used in synthesizing CDs, this process is facile and the product yield is normally high [57]. CDs with a size of 6 to 8 nm and 2.8% to 52% can be obtained through exfoliation that utilizes graphite rods and Pt wire in ionic liquid or water solution.
The mechanism of the exfoliation was due to complex interplay of anodic oxidative cleavage of water and anionic intercalation from the ionic liquid using titanium cathode and spectrum pure graphite in the center of electrolyzer to yield pure blue fluorescent CDs without the urgency of complex purification [28, 58, 59, 60, 61, 62].
Application of carbon soot in the synthesis of CDs have been reported by Tian et al., [63], the carbon source was from a carbon-processing reaction. Due to the simplicity to obtain the starting material, this method has been used widely by researchers. It also provides a new use for a complicated by-product. At the same time, it possesses disadvantages such as uncontrolled chemical surface, production of many byproducts that can harm human health with a broad dispersion [64].
Wang et al., [13] prepared CDs by microwave method. It proved reaction time can be shortened to 30–45 minutes with microwave-assisted technique. Similarly, Choi et al., [10] made effective use of lysine as a precursor to synthesize CDs within 5 minutes in a home type of microwave oven and the CDs were soluble in water with deep blue photoluminescence at a high mass yield of 23.3%.
Compared with other methods, the microwave route is more convenient since the heating of the carbon precursor is rapidly achieved within few minutes. It also exhibits high quantum yield and provides a long fluorescence lifetime. The procedure of microwave synthesis is much easier compared to others as it only utilizes heating via irradiation technique [65].
This method is mostly applied to produce CDs on an industrial scale. CDs can be obtained through oxidation treatment of carbon precursors by a strong oxidant. CDs from natural products have been researched and developed, by the synthesis of large scale CDs from human hair, coffee, and biomass by adding it into concentrated sulfuric acid and then heating at different temperatures. The time range is from hours to days [66]. By varying the temperature of synthesizing CDs, the quality of CDs such as diameter and quantum yields can be controlled [67, 68, 69].
The hydrothermal route of synthesizing CDs is considered as environmental-friendly, low cost and involves few synthesis steps that are non-toxic [2, 70, 71, 72, 73, 74]. Musa et al explored the hydrothermal method at a temperature range between 75°C to 175°C where the researchers reacted the precursor in a sealed hydrothermal reactor that resulted into a high yield photoluminescent quantum yield at 34.9% [2].
As illustrated in Figure 2, tapioca was added to an aldehyde solvent (acetone + sodium hydroxide) to improve the mobility of glucose molecules in starch [2]. The mixture underwent stages of reactions such as hydrolysis, adsorption, and gelatinization to particle disintegration simultaneously [2]. The carbonization temperature breaks the bond between the starch, making it available for the reactive solvent which leads to hydrolysis to form disaccharide and gelatinized glucose. The disaccharides polymerized into polysaccharides and the gelatinized glucose yielded CDs for functional group characterizations [9].
Mechanism for synthesis of carbon dots [2].
Like all-natural products, starch undergoes seasonal changes and particularly the amylose/amylopectin ratio is influenced by plant species and area of plant cultivation, which could influence the CDs formation. Independently of seasonal changes and origin, a starch will provide CDs with highly reproducible photoluminescent properties [2].
Substances such as glucose, citric acid, banana juice, and protein are examples of many precursors used to prepare CDs by adopting the hydrothermal route of synthesis [75]. Success has been reported in the synthesis of CDs through one-step hydrothermal carbonization using chitosan applied directly as a bioimaging agent [76]. The hydrothermal method is promising in producing CDs and is suitable for industrial or large scale production [75]. However, it is notable in 2010 where Zhang et al. [77] first reported a one-pot hydrothermal method to synthesize CDs from ascorbic acid in the presence of ethanol as solvent. Quantum yield and average particle sizes of their synthesized CDs were 6.79% and ~2 nm, respectively [77].
Several methods of synthesizing CDs has been explored in this section, to prevent the use of expensive precursor and energetic systems like in laser ablation. The hydrothermal synthesis route is being recommended as foremost for the sake of ecological sustainability [25]. Chemical oxidation and exfoliations provide an inexpensive alternative although it employs large amounts of strong acid which is hazardous and undesirable [77].
The other methods of synthesizing CDs need multi-step experimental operations and some of them require post-treatments to improve their water solubility, stability, and luminescent. Besides, several other methods suffer from drawbacks such as they require complex process and high temperature, time-consuming, harsh synthetic materials, and are expensive. This causes their applicability to be limited [78]. Several research successes proved that hydrothermal route to be a green method for the synthesis of CDs since the procedure produce soluble fluorescence CDs at reduce time and cost [2, 46, 79].
CDs derived from organic sources are excellent for the researcher and environment. Because the adoption of such material presents the choice to eliminate the need for metallic quantum dots, and any doping requirements, either through the use of sulfur (S) or nitrogen (N) agents. The use of metallic quantum dots and possible inclusion of S and N in enhancing their functionality contravenes the purpose of sustainable applications of nanomaterials in the modern field of nanotechnology [48].
Table 1 is a list of different synthesis techniques that have been attractive to researchers in recent years. The table provides a list of interesting techniques such as hydrothermal, microwave assisted, biogenic synthesis, thermal oxidation, ultrasonication, refluxing and chemical oxidation with excellent particle sizes [80, 81, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91]. The hydrothermal synthesis of CDs proves to be efficient and effective since it provides relatively smaller sizes of the nanoparticles as synthesized by Du et al., [81] at 1.8 nm, when compared to other methods such as chemical oxidation by Thambiraj and Shankaran [85] at 4.1 nm, biogenic synthesis by Phadke et al., [20] at 5–8 nm, and refluxing by Himaja et al., [84] at ~50 nm.
Method | Size (nm) | Reference |
---|---|---|
Microwave-assisted | 2.7 | [7] |
Microwave | 5–10 | [10] |
Biogenic synthesis | 5.0–8.0 | [20] |
Thermal oxidation | 5.0–10 | [22] |
Heating | 3.0 | [78] |
Hydrothermal | 2.3 | [80] |
Hydrothermal | 1.8 | [81] |
Ultrasonication | 5.0 | [82] |
“Oil bath” | 2.59 | [83] |
Refluxing | ~50 | [84] |
Chemical-oxidation | 4.1 | [85] |
Chemical oxidation | 2.5 | [86] |
Carbon dots sizes and synthesis techniques.
Note: n/a = not available.
One of the CDs properties is that it shows strong optical absorption in the UV region (200–800 nm) with a tail extending to the visible range, see Figure 3. CDs possess low toxicity with excellent photostability as compared to semi-conductor quantum dots [7, 23, 50, 71].
Optical properties of carbon dots at UV-visible absorption and emission spectra.
Absorption shoulders in the spectrum are due to the π-π* (pi to pi star transition) of C〓C bonds or n-π* (n to pi star transition) of C〓O and other fringe functional elements present [69, 92].
The uniqueness of CDs is the availability of wide surface area for trace detection of analytes and provision of adsorptive sites through the availability of heteroatomic carbon in nano-dimension along with photoluminescence emission. Based on past study, CDs is dependent on intensity and wavelength emission towards its excitation wavelength [93]. This is due to the different sizes of particles and surface chemistry and/or different emissive traps on CDs\' surface. The wavelength dependence behaviour makes CDs possible to be applied in multi-colour imaging and adsorptive purposes. Vinci et al., [93] suggest that CDs\' core, surface states, and size are responsible for their emission and adsorptive properties [93].
Table 2 shows the excitation wavelengths of CDs through the UV-lamp excitation process to obtain fluorescent characteristics [2].
Colour | Interval of wavelength (nm) |
---|---|
Red | 700–635 |
Orange | 635–590 |
Yellow | 590–560 |
Green | 560–520 |
Cyan | 520–490 |
Blue | 490–450 |
Violet | 450–400 |
The color range of visible light spectrum.
The colour of CDs most of the time is related to the surface groups which corresponds to particle sizes [93]. Normally CDs show strong photoluminescence from blue to green wavelength. To enhance the quantum yield (QY) of CDs or change photoluminescence (PL) emission to meet desired applications, surface passivation and functionality play a vital role. Besides, CDs show great photostability as there are no reductions in PL intensity with continuous exposure to excitation. In terms of chemical properties, different synthesis methods of CDs lead to different chemical structure and abundance of surface sites. They are usually connected or modified by polymer chains, oxygen-based, amino based groups, and others [93].
Characterization of CDs by high resolution transmission electron microscopy (HRTEM), Xray photoelectron spectroscopy (XPS), Fourier transform infrared (FTIR), Atomic force microscopy (AFM) and Zeta Potential provide deep insights into the attributes of CDs such as hybridization and coefficient between functional groups and carbon core that take parts in the provision of the abundance of surface sites and the photoluminescence behaviour [94]. In comparison to graphene and metallic quantum dots, the CDs serves as the way out of toxicity concerns in environmental monitoring and medical applications [95].
The sizes and texture of CDs are important for fundamental applications in the field of environmental science and nanotechnology. Figure 4(A–C), shows the HRTEM images of CDs at different resolutions between 1 nm to 10 nm. Synthesized CDs revealed amorphous quasi-spherical morphology with a lattice spacing of ca 0.24 nm (Figure 4A), CDs characteristics are suitable absorbent of pollutants that are larger than 0.24 nm [2, 71, 89].
High resolution transmission electron microscopic (HRTEM) (A) Lattice space of carbon dots (CDs) characterized in magnifications of 5 nm. (B) Images of CDs at 10 nm. (C) Size distribution of CDs within 10 nm magnification [2].
High-Resolution Transmission Electron Microscopic images of the CDs characterized in magnifications of 5 nm and 10 nm (Figure 4A and B respectively). Figure 4A is the lattice spacing for carbon dots at 5 nm magnification. While Figure 4B is the size distribution within 10 nm magnification. Figure 4C is the histogram chart, demonstrating the nanoparticle sizes of CDs. The synthesis of nanoparticle with low lattice space is needed for research applications of CDs in environmental chemistry, pollutant entrapment in aqueous media and water purification [74]. The interplanar distance (lattice spacing) of 0.24 nm (Figure 4) is lower than the lattice spacing planes of graphitic materials (0.34 nm), the larger interlayer spacing could be attributed to the abundant oxygen-containing groups. In other words, the oxygen-containing groups could expand the layer spacing. The synthesized CDs is in consonance with recent reports by Arumugam and colleagues, CDs was hydrothermally synthesized from broccoli [79], ginkgo fruits [87], and cabbage [8].
Fourier-transform Infrared spectroscopy (FTIR) portrays the functional structure of CDs. It reveals the intrinsic functional groups and other useful compounds present in CDs. Figure 5 provides functional groups that exist before and after the hydrothermal treatment of tapioca as a precursor for CDs.
FT-IR spectrum of the carbon dots and tapioca [2].
As shown in Figure 5(A) representing tapioca. Peaks associated with the stretching vibrations of hydroxyl (▬OH) and carboxylic (COO▬) groups are at 3353.45 and 2933.78 cm−1 [75]. Further stretching vibration of C▬H occurred from 1645.24 to 1341.82. The peaks at 1151.38, 1079.20, 1014.41 cm−1 can be due to the C▬O stretching vibrations and out-of-plane bending modes of sp2 and sp3 ▬CH group [75].
There were substantial changes observed in the spectra of CDs (Figure 5B). The hydroxyl (▬OH) group of 3389.71 cm−1 increased on the carbon structure as a result of hydrolysis. While the carboxylic (COO▬) group 2145.73 cm−1 reduced by thermal destruction of saccharides structure [34]. The peaks at 1695.27 cm−1 and 1644.62 cm−1 showed the increase in the C▬H stretching vibrations of the bending modes of the sp2 and sp3 ▬CH group. The peaks around 1427.63 cm−1 until 1369.43 cm−1 are due to C▬O▬C [34]. The peak at 1237.62 cm−1 corresponds to the C〓C stretching vibration while 1094.19 cm−1 and 996.19 cm−1 represents the C〓O stretching vibration and the last group at 706.78 cm−1 denotes the C〓C bond of the unsaturated glucose structure in the starch. These attributes were responsible for the water-soluble nature of CDs [34]. The FTIR graph shows the formation of unsaturated carbon. Along with oxygen-rich groups such as hydroxyl, carboxyl, and carbonyl situated on the CDs surface, which agree with the hydrothermal synthesized CDs from the organic origin [23, 25, 26, 81, 90].
There are numerous applications of carbon nanoparticles due to the abundant properties they possess [3]. These applications are being discussed in the subsequent sections of the report.
Carbon dots have shown great potential to act as a sensor and can be used for environmental monitoring and control of pollutants, more so in the medical field for biosensor applications. It can donate or accept electrons that make it suitable for detection of ions, vitamins, nucleic acid, protein, enzyme and biological pH value [7, 11, 96, 97, 98]. Even though different materials are used to detect specific ions, the detection mechanisms are identical [99].
The functional groups on the surface of CDs specify distinctive affinities to different target ions, through an electron or energy transfer process and high selectivity to other ions [100]. CDs has been involved in the detection of 2,4,6-tri-trotoluene (TNT) and also applied as a dual-sensing platform for fluorescent and electrochemical detection of TNT [101]. Other reports utilized CDs as pH sensors for in-vitro and in-vivo investigations [102].
Research showed CDs able to detect intracellular pH inside a living pathogenic fungal cell and has been developed to sense nucleic acid in the DNA [103]. In other cases, CDs have been used in bioimaging because of their low toxicity and excellent photostability compared to semi-conductor quantum dots that posed health problems and environmental concerns [8]. Its visible excitation, emission wavelengths, and high brightness confirm CDs as a suitable candidate in this area. Several studies have been conducted using CDs in cell imaging, including pig kidney cell line [104], Escherichia coli [105], Hela Cells [106], liver diseases [95], see Figure 6.
Graphical description of fluorescence images of carbon dots.
Chengkun et al., [98] discovered photoluminescence in CDs synthesized from Nescafe original instant coffee and applied it in the field of bioimaging. From their investigation, CDs from Nescafe are found to be amorphous and the cytotoxicity study revealed that the CDs did not cause any toxicity to human hepatocellular carcinoma cells at a concentration as high as 20 mg/ml. Yang et al., [107] also worked on novel green synthesis of high-fluorescent CDs from honey for sensing and imaging. It was an innovative and green approach towards a CDs of high fluorescent quantum yield and excellent photostability, employed for HeLa cells imaging and coding. Rui-jun et al., [108] produced photoluminescent CDs from polyethylene glycol (PEG) for cellular imaging. The PEG is a biocompatible non-conjugated polymer, used as both carbon source and passivating agent [108].
The application of CDs in the selective detection of heavy metals have been reported in several scientific and experimental research [34, 40, 79]. However, there are gaps and lapses needing redress, such applications are predominantly in photoluminescent quenching of heavy metals. whereas, current section looks into reliable and robust CDs for applications in electrochemical sensing of multiple ranges of heavy metal ions.
The development of a convenient and sustainable technique for detecting and identifying human and environmentally toxic metal ions is of great interest. The following are reports concerning CDs application in heavy metal detection.
Zhang and Chen [109] worked on nitrogen-doped carbon quantum dots application as a turn-off fluorescent probe for the detection of Hg2+ ions at a detection limit of 0.23 μM. The fluorescent quenching mechanism is attributed to the surface-state triggered by the mercury-induced conversion of special functional group (▬CONH▬) from spirolactam structure to an opened-ring amide [109].
Sandhya et al., [110] applied nanostructures for heavy metal ion sensing in water using surface plasmon resonance of metallic nanostructures. They reviewed on techniques to improve selectivity and sensitivity of surface plasmon response sensors with attention to homogeneity. Effects of particle size, shape, material type, and surrounding environment were found to be effectual in the surface plasmon surface frequency.
Similarly, Qu et al., [111] developed CDs to detect Fe3+ ions by using dopamine as a starting material with a detection limit of 0.32 μM. Quenching of photoluminescence intensity occurred when there was an interaction between CDs and ions. Meanwhile, Liu [44] reported a research work on one-step green synthesized fluorescent carbon nanodots from bamboo leaves for copper (ll) ion detection and demonstrated the exploration of bamboo leaves as a carbon source with high carbon constituent. Carbon quantum dots were synthesized hydrothermally with sensitive Cu2+ detection at limit of detection as low as 115 nM and a dynamic range from 0.333 to 66.6 μM. The zeta potential of the pristine carbon quantum dots was measured at −4.78 mV which improved to +13.8 mV after treatment with positively charged polyethyleneimine (a water-soluble cationic polymer). More so, Rao, et al., [112] reported on the ability of CDs generated from citrus acid anhydrous to detect heavy metal such as Fe3+, with a detection limit of 0.239 μM.
Methionine has been used as a material for the synthesis of CDs [113]. These CDs were co-doped with nitrogen and sulfur to enhance surface functionalization for the detection and environmental monitoring of heavy metal pollutants [113]. Similarly, Shen et al., [4] applied fresh pomelo in the synthesis of CDs co-doped with nitrogen and sulfur for the detection of chromium (Cr (VI)).
A fluorescent probe for selective detection of metal ions such as mercury (Hg2+, 1.00 × 10−8 − 1.50 × 10−3 M, 1.00 × 10−7 M) with wide linear range and satisfactory detection limits was discovered when citric acid monohydrate was used for the synthesis of fluorescent CDs [114]. More essentially and effective is the burning of ash from waste paper and further utilized as a source of CDs by Lin et al., [115]. They succeeded in synthesizing CDs without any surface modification and subsequently, the fluorescent CDs were quenched by Fe3+.
Simpson et al., [21] synthesized carbon nanoparticle from glycerol and phosphoric acid mixed in a Berghof high-pressure reactor at 250°C for 4 hours. Afterward, glassy carbon electrodes were fabricated by drop-casting the carbon nanoparticles, and further applied for heavy metal (Cu2+ and Pb2+) detection by square wave anodic stripping voltammetry [21]. Heavy metals such as Na+, K+, Mg2+, Ca2+, Cr3+, Co2+, Ag+, Hg2+, Cd2+, Pb2+, Ni2+, Cu2+, Zn2+, Al3+, Fe2+, and Fe3+ have been tested on CDs synthesized from carbon source of mangosteen pulp and a ground discovery was made. Among the listed heavy metals, Fe3+ was the favourite in detection with a detection limit of 52 nM. Further application was found for cell imaging, which reveals their diverse potential applications [89].
Abhishek et al., [14] made a paper strip based live cell ultrasensitive lead sensor using CDs synthesized from biological media. They reported a formulation of a sensor through microwave heating of potato-dextrose agar (PDA) for the detection of lead (pb2+) in solution but again involved a long and laborious process.
Pajewska et al. [116] explored the fluorescence of synthesized CDs from citric acid with glutathione for the sensing of mercury (Hg2+) ion. A high recovery of Hg2+ was achieved at 115.1%. The method of synthesizing CDs with low toxicity is embedded in the green chemistry principles. Thus, it fulfills the criteria of being eco-friendly. Table 2 provides a list of applications of CDs in the detection of heavy metals ions.
As seen in Table 3, the mechanism of action for the application of CDs largely depends on the analyte of concern. In the case of CDs from citric acid monohydrate for application in fluorescence quenching of Hg2+, it relies on Förster resonance energy transfer (FRET) [114]. This is similar to CDs synthesized from biomass [117], polyacrylamide [118], lotus root [119], degreased cotton [120], gold nanoclusters [111], and Petroleum coke [127].
Source of carbon nanoparticles | Sensing mechanism | Type of metal ions and linear range | Sensing (LOD) | Reference |
---|---|---|---|---|
Biomass | Fluorescence | Hg2+/Fe3+ 0.002 mol L−1 | 10.3 and 60.9 nM | [117] |
Polyacrylamide | Fluorescence | Hg2+ 0.25–50 μM | 13.48 nM | [118] |
Lotus plant | Fluorescence | Hg2+ 0.1 to 60.0 μM | 18.7 nM | [119] |
Degrease cotton | Fluorescence | Cr(VI) 1.00–6.00 mmol/L | 0.12 μg/mL | [120] |
Gold nanoparticles | Luminescence | Pb2+ 1 × 10−5 M | n/a | [121] |
Biomass from peanut shells | Fluorescence | Cu+2 0–5 mM | 4.8 mM | [122] |
Metal oxides | Electrochemical oxidation. | Cu2+ 0.1 to 1.3 μM | 0.04 μM | [123] |
Metal nitrates | Isotherm | Cd2+ 10 mg/L | 12.60 mg/g | [124] |
Mushroom | Fluorescent | Hg2+ 0 to 100 nM | 4.13 nM | [125] |
Penaeus merguiensis enzyme | Isotherm | Cu+2 1–5 mM | 2 mM | [126] |
Coke | Fluorescent | Cu+2 0.25–10 μM | 0.0295 μM | [127] |
Carbon nanoparticles for heavy metal sensing.
Fluorescent carbon nanoparticle sensing is largely dependent on changes or disturbances that are caused by an analyte that interacts with a fluorescent probe. This shift mostly will lead to a measurable change in the emission characteristics of the probe (emission wavelength, intensity, lifetime, or anisotropy), which can be directly linked to analytes (e.g heavy metal) concentration. More so, fluorescence probe strategies are based on quenching (turn-off) or enhancing (turn-on) emission, and surface-enhanced Raman scattering (SERS) techniques [33, 125].
Other notable techniques for the detection and quantification of heavy metals ions include, inductively coupled plasma mass spectrometry (ICP-MS). This instrumentation is efficient among several other methods, but it is expensive. It was developed since the 1980s [128, 129, 130], used mostly by multivariate analysis along with the ICP-MS technique to unravel heavy metal elements present samples. However, inductively coupled plasma atomic emission spectroscopy (ICP-AES) have also been used to identify heavy metal pollutants. But, the method is expensive and requires sophisticated instrumentations and a highly trained technician [131].
Nowadays, marine pollution is becoming a global phenomenon and seafood safety has played a crucial role in human health [129]. Fatema et al., [132] applied atomic absorption spectroscopy (AAS) to measure the absorbed quantity of Pb+2, Cd+2, and Hg+3 in shrimps. Heavy metals have been detected by other means such as energy dispersive x-ray fluorescence (EDXRF), electrothermal atomic absorption method (ETAAS), and flame atomic absorption spectroscopy (FAAS) [133, 134]. But, all of the aforementioned techniques have disadvantages in the detection of heavy metals, such that they are expensive and require strenuous experimental steps [135]. Therefore, environmental researchers have continued to strive to develop a cheap, simple, sensitive, specific, accurate, user-friendly, and eco-friendly means of detection for heavy metal pollutants.
CDs are very useful in detecting non-metallic elements. Several types of research have been reported, CDs synthesized from potato are well able to detect phosphate [106]. Zhaoxia et al., [136] utilized CDs with turnable emission and controlled size for sensing hypochlorous acid. As a class of carbohydrate that is widely distributed in a living organism, sucrose was chosen as a carbon source with assistance of microwave irradiation. A strongly fluorescent CDs without post-passivation was produced. By increasing the concentration of phosphoric acid as fluorescence enhancer under UV lamp, various fluorescent emissions of CDs of variable sizes were obtained. It was found that green CDs have excellent sensitivity for the detection of hypochlorous acid.
Kuo et al., [85], experimented with percutaneous fiber-optic nanosensors for instant evaluation of chemotherapy efficacy for in-vivo strategy of assay design aimed at monitoring non-homogeneously distributed biomarkers. They identified optimal exogenous fluorophores for the cell distribution indicators that are independent of the treatment of the apoptotic initiator and without interfering with the optical characteristics of fluorophores.
Huilin et al., [137], investigated on CDs as a fluorescent probe for off-on detection of sodium dodecyl-benzenesulfonate (SDBS) in aqueous solution. The pristine CDs were synthesized from sodium citrate through a simple, convenient, and one-step hydrothermal method. Fluorescent recovery was achieved with the application of SDBS. Detection of SDBS in real water samples was proportional to the concentration in the range of 0.10 to 7.50 ug/mL. Furthermore, fluorescence sensing probe has been used to detect kaempferol (flavonoid that is present in a variety of plants and plant-derived foods) using fluorescent CDs synthesized from chiefly acetic acid with a detection limit of 38.4 nM in the concentration range of 3.5–49 μM. Finally, organophosphorus as pesticides have been detected through the use of CDs as a detector for pollutants without surface modification [115].
CDs and carbon structured nanoparticles have attracted researchers to explore their effectiveness and optimization ability in the fields of pollution research [3]. Because of their excellent properties; carbon material performs concurrently as adsorbent and a transducing-agent [138, 139, 140, 141].
Due to abundant surface sites provided by CDs, it is a suitable candidate for studies in the detection and adsorption of heavy metals [142, 143]. For instance, Ghiloufi et al., [144] used gallium doped zinc oxide (ZnO) nanoparticle in the adsorption of heavy metals (Cd2+ and Cr6+) in aqueous solution. The adsorption of heavy metals was analyzed through the effect of pH and it revealed favourable adsorption at a low pH level, less than pH-3 and temperature of 298 K [144].
Table 4 provides harmonized presentation of nanomaterials applied for the purpose of absorbing environmental pollutants and contaminants in aqueous systems [145, 146, 147, 148, 149, 150, 151, 152, 153, 154].
Adsorbent material | Adsorbate/analyte | Reference |
---|---|---|
Gold nanoparticles (AuNPs) | 4-nitrophenol | [145] |
Carbon dots (sodium citrate) | Mercury (II) ions. | [146] |
Fluorescent carbon dots from o- phenylenediamine | Cell imaging and sensitive detection of Fe3+ and H2O2 | [18] |
Silica gel | Aromatic volatile organic compounds (VOCs) | [147] |
Graphene oxide | Nitrobenzene in sulfide | [148] |
TiO2, SiO2, and ZnO nanoparticles | Neptunium (V) | [149] |
Polystyrene latex nanoparticles | Alumina | [150] |
Graphene oxide | Radionuclide removal | [151] |
Polyaniline modified graphene oxide | Uranium(VI) | [152] |
Carbon nanotubes | Mingle-ringed N- and S-heterocyclic aromatics | [153] |
Graphene oxide | Minerals such as montmorillonite, kaolinite, and goethite, in aqueous phase | [154] |
Nanostructured materials in adsorption processes.
So far the concept of applying nanoparticles for environmental objectives have been successful. Meanwhile it is recommended that comparisons be made with bulk counterparts of the same substance to measure efficiency. On this note a study on the application of bulk agro material from jatropha curcas demonstrated efficiency in adsorption of pollutants and is recommended for comparison with its nano-dimension counterparts [155]. Similarly, a report on the application of sesame straw biochar in adsorption of heavy metal analyte concluded that further adsorption studies for nano-range agro-based materials are necessary for accurate estimation of adsorption in natural environments [156].
A suitable carbon source for CDs synthesis should be soluble in water (green chemistry), accessible worldwide (i.e. geographical abundance) with defined and well-known properties (i.e. functional attributes), should not be in direct competition with essential food production (i.e. sustainable), and it should be cost-effective (i.e. cheaply accessible). While the price of additives or carbon source plays a minor role in fundamental research, it may play a major role when large quantities are considered.
The authors would like to thank Universiti Putra Malaysia (UPM), Malaysia for funding this article.
The authors hereby declare that there is no conflict of interest.
M.Y.P., as the first author; made the study conception and design acquisition of reports and drafting of manuscript. Z.Z.A., contributed in the study conception and design, critical revision of major scientific ideas through clinical experience.
This research was funded by Universiti Putra Malaysia, grant number GP-IPS/2017/9556800.
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