Indian Journal of Experimental Biology Vol. 57, November 2019, pp. 879-886

Indoor potted plant based biofilter: performance evaluation and kinetics study BS Giri1*,†, Asmita Sarowgi2,†, Yeshaswi Kaushik3,†, Anugunj Pal2,†, Abhishek Jaiswal1,†, Sangeeta Kumari2,

Harinder Singh4, Ravi Sonwani1, V Thivaharan5 & RS Singh1*

1Department of Chemical Engineering and Technology, Indian Institute of Technology-BHU, Varanasi-221 005, Uttar Pradesh, India 2Department of Botany, Institute of Science, Banaras Hindu University, Varanasi-221 005, Uttar Pradesh, India 3Department of Biotechnology, Thapar Institute of Engineering and Technology, Patiala, Punjab-147 004, India

4Department of Chemical Engineering, Motilal Nehru National Institute of Technology (MNNIT), Allahabad, Uttar Pradesh, India 5Department of Biotechnology, Manipal Institute of Technology, Manipal Academy of Higher Education, Manipal-576 104, Karnataka, India

Received 31 January 2019; revised 13 March 2019

Plant based biofilters associated with microorganisms have been gaining popularity in controlling odorous compounds like volatile organic compounds (VOCs) as they are cost effective and an environment friendly alternative to conventional air pollution control techniques. In this context, here, we tried to evaluate the performance of potted plants based Claire’s biofilter for biodegradation of benzene. A sealed perspex chamber with lid and fan was designed to ensure minimum leakage, proper aeration and distribution of benzene inside the chamber. Five different ornamental indoor plants were placed inside the chamber sequentially and exposed to a concentration of 5 ppm benzene for 30 h each. The leakage of benzene was checked beforehand. Epipremnum aureum (Money plant) showed maximum benzene degradation in the aforementioned time period with a removal efficiency of 98%. The µmax and Ks values for 100 ppm concentration of benzene were calculated to be 0.284 h-1 and 0.427 g/m3, respectively.

Keywords: Air pollution, Benzene biodegradation, Biofilter, Epipremnum aureum, Indoor air quality, Minimal salt media (MSM), Money plant, Ornamental plants, VOCs

In contrast to the lifestyle of our predecessors, the current generation is facing a major crisis in the form of environmental pollution. Owing to population explosion, rapid industrialization, urbanization, commercialization and other human activities for a luxurious lifestyle, the quality of water we consume, the air we breathe and the land we live on has deteriorated significantly. As compared to outdoor air pollutants, the risk of exposure to indoor pollutants is much higher1. This level of pollutants has proved to be hazardous to our health due to the amount of time spent indoors like offices, residential buildings, etc. Thus, it is of utmost importance to understand the role of clean air and adopt different techniques to purify the indoor air. One such class of indoor air pollutants is volatile organic compounds (VOCs). The high vapor pressure at ordinary room temperature is due to a low boiling point as a result of which the phenomenon of volatility takes place. For example,

the boiling point of formaldehyde is only –19°C (–2°F). The association of poor indoor air quality and these anthropogenic pollutants is relatively high2. The sources of VOCs range from pesticides, gasoline, perfumes, paint. Etc.3. A sub-group of VOCs include mono-aromatic hydrocarbons called BTEX (benzene, toluene, ethylbenzene and xylene) containing one substituted or methyl-substituted benzene ring. They can be found in the environment due to emissions from motor vehicles and aircraft exhaust, fuel operations, refineries, gasoline stations, and gasification sites4. Introduction into water can be due to industrial effluents and atmospheric pollution, spills of petrol and petroleum products or proximity to natural deposits of petroleum and natural gas. In the air surrounding areas with a high traffic density, the concentrations for BTEX are up to 349, 1310, 360 and 775 μg/m3. As compared to air, the concentration of BTEX in water is comparatively lower5. The health risks involved are drowsiness, dizziness, rapid heart rate, headaches, tremors, confusion, and unconsciousness. Cancer of blood-forming organs (leukaemia) can be a result of long-term exposure to benzene. Other health hazards associated with

–——— *Correspondence: E-mail: balendushekher23@gmail.com (BSG);

rssingh.che@iitbhu.ac.in (RSS) †These authors have contributed equally.

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benzene are vomiting, irritation of the stomach, dizziness, sleepiness, convulsions, rapid heart rate, coma, and sometimes death6. Toluene mainly affects the brain and nervous system which can be evident from symptoms such as fatigue and drowsiness7. Similarly, exposure to ethylbenzene causes enlargement of liver and kidney8. Xylene can cause damages to the nervous system like lack of muscle coordination, dizziness and confusion9,10. The harmful effects of BTEX have been reported in aquatic organisms too. Thus, due to the toxic nature of BTEX and VOCs to human health, it is of utmost importance to purify the air around us.

Different types of bioreactors can be employed for the treatment of VOCs. The criteria for selection depend on loading capacity, physical and chemical properties of the target molecules along with the design, configuration, operational parameters of the bioreactor, etc.11. Examples of various bioreactors along with their advantages and disadvantages are mentioned in Table 1. Owing to its low cost and lack of secondary pollutant production, biofiltration is an attractive air treatment technology for the degradation of VOCs. Our experiments demonstrate that biofiltration using a potted plant-based Claire’s filter is a viable treatment technology for removing and degrading VOCs. Indoor plants play an important role in the removal of VOCs. The root zone of plant is very effective for removal of VOCs under controlled conditions. The pathways for the plant-mediated removal of VOCs are of four different ways12 which includes the removal by plant shoot system, microbes in the soil microcosm, plant root system and growth medium (substrate). Upadhyay & Kobayashi13 pointed out those plants with larger leaf surface area are more suitable for removing pollutants. A similar recommendation was also made by Clarsen et al.14 for removal of pollutants. It had also been stated that rhizosphere degradation (rhizoremediation) could play a major role in VOC removal by botanical biofiltration. Guieysee et al.15 found that the diversity of microbial species in the rhizosphere microcosm

appeared to be a key parameter in the reduction of VOCs. Microorganisms existing in the soil of potted plants possibly play an essential role in removal of VOCs from indoor air. It has been shown that roots can absorb pollutants by themselves but can also increase the availability of pollutant for the microorganisms. A plant’s ability to detoxify volatiles is determined by the uptake capacity of the plant cells and their ability to metabolize the pollutants while maintaining their normal metabolic processes.

In this study, potted plants are chosen as they are the simplest and most economical choice for indoor air purification, although they remove pollutants at a slower rate. If passive potted plant systems are designed to exhibit greater VOC removal rates, then their benefits will be experienced from people inhabiting locations with poor electricity access. Materials and Methods

Potted plants used The potted plants used for the study of VOC

removal9-11 were Chlorophytum comosum (Spider plant), Ocimum tenuiflorum (Holy basil or Tulsi), Dracaena deremensis (Janet Craig), Epipremnum aureum (Money plant) and Sansevieriatri fasciata (Snake plant).

Plant based Claire’s biofilter Five separate pots containing the aforementioned

plants were used for carrying out a comparative study of their ability to degrade VOCs. The soil present in the pot contained activated carbon for the adsorption of VOC. A fan was attached to the pot for proper circulation of air and it is ensured that the moisture content was maintained according to the need of the plant.

Chemicals and Growth media

Nutrient agar medium Minimal salt Medium (MSM) composed of (in g)

K2HPO4 (4.27), KH2PO4 (3.48), MgSO4.7H2O (0.46), (NH4)2SO4 (0.34), FeSO4 (0.001), CaCl2.2H2O (0.018) and the rest in mg: CuCl2.2H2O (0.01), CoCl2.6H2O (0.2), ZnSO4.7H2O (0.1), MnCl2.4H2O (0.03), Na2MoO4 (0.03) and NiCl2.6H2O (0.02) along with 1% glucose, all in 1L distilled water11. Benzene was procured from the Merc, India for the experimental studies.

Treatment chamber A sealed perspex chamber with removable lids

(fitted with screws) and a rubber gasket was designed to ensure minimum leakage of VOC. Perspex is a

Table 1—The dimensional details of the biofilter chamber Chamber Details Dimensions Dimensions (cm) 51.5 × 51.5 × 62.5 (l×b×h) Fan 0-12 V , 0-50 Ma No. of Sampling ports 5 (4 at corners and 1 in middle) Material of Construction Perspex Lower Base Support Aluminium Upper Lid Dimensions 53.5 cm each

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transparent thermoplastic often used as a lightweight or shatter-resistant alternative to glass. An injection-like tube was inserted for calculating the concentration of benzene (in ppm) using a sensor (Fig. 1).

Experimental set-up In order to initially verify the leakage of benzene,

0.9 µL of 5 ppm benzene was added in the perplex chamber and was sealed for a period of 30 h to check any possible decrease in the benzene concentration. After the leakage was checked, a potted plant was placed on an aluminium support in the centre and same concentration of benzene was injected into the chamber. The fan was switched on and other conditions like temperature and moisture content were regulated as per the needs of the plant. The set-up was kept for 30 h and the decrease in benzene concentration was noted once every 2 h using a sensor. The experiment was repeated for all the five plants for the same time period to perform a comparative study.

The removal efficiency for each plant was calculated as follows5,9:

Removal Efficiency (%) = (Cin - Cout)/Cin× 100

where: Cin and Cout are the concentrations of benzene at inlet and outlet, respectively. Isolation, enrichment, and biochemical test for bacterial isolates

From the soil of each of the plants, before and after exposure to VOC, bacteria was isolated for estimating the total bacterial load present and the number of

bacteria capable of degrading benzene. For this, the soil samples were collected and diluted up to 10-6. About 100 µL of 10-4 and 10-5 dilutions were spread on NA plates and kept for overnight incubation at 35°C. The colonies thus formed were counted and expressed as CFU/mL, using the following formula:

CFU/mL = (Number of bacteria × Dilution factor) / (Volume of culture spread on the plate)

Few colonies were picked up and streaked onto MSM plates following which 1 mL of 100 ppm benzene was spread on top of the streaked plates and kept at 35°C for incubation for 3 days. The colonies that appear on the MSM plates were deemed to be resistant to benzene and could utilize it as a carbon source. Streaking of the obtained colonies was done on NA plates and stored for further use.

PCR amplification The extracted bacterial genomic DNA was

subjected to PCR amplification of 16S rRNA gene with universal primers. The amplification reaction was carried out in a thermo cycler (Bio-Rad Laboratories, Inc, Australia). Various steps involved in PCR reaction are mentioned in Table 2. The reaction mixture was prepared in a final volume of 50 µL containing tris-HCl, MgCl2, dNTPs, Taq DNA polymerase, universal primers and DNA template.

Agarose gel electrophoresis Agarose gel electrophoresis is used to separate

mixtures of DNA fragments on the basis of molecular weight and sizes. Agarose gel (1%, made in TAE buffer) was used to resolve DNA fragments. Ethidium bromide (EtBr) was added to the gel before casting to visualize the DNA fragments. The solidified gel was then loaded with DNA samples containing 6x gel loading dye and was allowed to run in 0.5% TAE buffer at 90V. The gel was finally visualized under UV-transilluminator. The microorganism was grown as pure culture and further sent for molecular characterization.

Growth curve of bacteria A growth curve of the benzene-degrading bacteria

was plotted by inoculating 200 mL of MSM broth

Fig. 1—Sealed Perspex chamber covered with a lid using nuts and bolts with a fan attached to one side of the chamber to ensure equal distribution of all components present in the air inside and sampling points for noting down the concentration of VOC at a given point of time.

Table 2—Steps involved in carrying out PCR reaction Step Temperature (oC) Time (mins)

Initial denaturation 95 5.00 Cycle denaturation 95 0.30 Annealing 55 0.30 Extension 72 1.00 min for 1 kb No. of cycles Step 2-4 31-33 cycles Final extension 72 10.00 Resting 4 until analysis

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with a loopful of culture and adding 100 ppm benzene. The OD value was taken after every 2.5 h. A similar growth curve was prepared by adding 150 ppm of benzene. A control was also made in which benzene was not added. The amount of substrate (benzene) degradation with respect to the growth of bacteria was also noted. The growth curve obtained is used for calculating the values of µmax and Ks using the Monod kinetics11,15.

Owing to the importance of biodegradation rates as a controlling factor for biofilters’ effectiveness, Monod kinetics is used as a measure of growth. It is expressed as a function of the existing concentrations of biomass and the concentration of contaminant. This equation used to understand the growth of microorganism is given as follows:

where, µ is the specific growth rate of the microorganisms (h-1), µmax is the maximum specific growth rate of the microorganisms (h-1), S is the concentration of the limiting substrate for growth (mg/L or g/m3 Ks is the "half-velocity constant"—the value of S when µ/µmax = 0.5.

The rate of substrate utilization is related to the specific growth rate as follows:

where, X and Y are total biomass and yield coefficient, respectively

In this case, the Monod kinetic model is used to investigate the kinetics of microbial growth and utilization of benzene. The formula used is as follows:

where, µ: specific growth rate (h-1); µmax: maximum specific growth rate (h-1); Ks: half saturation constant (mg L-1); X, S and t are microbial cell, initial substrate concentration (mg L-1) and time, respectively.

For a given initial microbial cell X0, the microbial cell concentration X and time t can be given by:

Thus, the above method was used for calculating the values of µmax and Ks using the data obtained from the growth curve.

Optimization of growth conditions

Temperature The temperature value at which the

microorganism showed optimum growth was checked by allowing the organism to grow in a range of temperature values. Five flasks, each containing 200 mL of MSM broth were taken and 2 mL of 100 ppm of benzene was added to each flask. The flasks were inoculated with the organism and incubated at temperature values of 35, 45 and 55°C and room temperature of 25°C. The O.D. values were observed at 600 nm after every 3 h. pH

To determine the optimum pH value, the experiment was repeated in the manner mentioned above and the flask contents were maintained at pH values of 3.0, 5.0, 7.0, 8.0 and 9.0. The OD values were observed at 600 nm after every 4 h.

Growth inhibition The concentration of benzene at which bacterial

growth is inhibited can be elucidated by allowing the microbes to grow in different concentrations of benzene, viz., 100, 200, 400, 800 and 1000 ppm.

Analytical methods CHNS of the soil samples of various potted-plants

before and after benzene exposure was conducted to know the composition of elements namely carbon, hydrogen, nitrogen and sulphur present. SEM was carried out to determine the morphology of the sample. X-ray diffraction (XRD) is a rapid analytical technique primarily used for phase identification of a crystalline material and can provide information on unit cell dimensions. The analyzed material is finely ground, homogenized, and average bulk composition is determined. In FTIR, when IR radiation is passed through a sample, some radiation is absorbed by the sample and the rest is transmitted. The resulting signal at the detector is a spectrum representing a molecular ‘fingerprint’ of the sample.

Results and Discussion In this study, we developed a potted plant

(ornamental plant) based Claire’s biofilter to degrade volatile organic compounds. Of the five common indoor ornamental plants [Chlorophytum comosum (Spider plant), Ocimum tenuiflorum (Holy basil or Tulsi), Dracaena deremensis (Janet Craig), Epipremnum aureum (Money plant) and Sansevieriatri fasciata (Snake plant)] we tested, the Money plant emerged as a potential plant.

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Performance evaluation The comparative study of all the five plants was

done to check the removal efficiency of each plant. Our experiments showed that Epipremnum aureum possesses the highest removal efficiency of 98% in 30 h. The graph showing the rate of benzene degradation and the performance evaluation of each plant is shown in Fig. 2. A comparative study has been presented in the Table 3 in which the present findings have been compared with various other VOC removal studies, reported earlier.

The entry of the pollutants in the leaf tissue occurs either via the open stomata on the leaf epidermis or

by diffusion through the epidermis that is covered by a waxy cuticle16. Entry through stomata has been assessed by several studies addressing the impact of stomatal density on VOC removal efficiency of various plant species17,18. The alternative route of entry is through the cuticle, which is permeable to both lipophilic and hydrophilic molecules. The pollutants become adsorbed onto the lipophilic surface of the leaves’ waxy layer resulting in their accumulation on the cuticle to a certain extent that in turn allows their gradual penetration into the leaves16. Other avenues by which pollutants may enter the leaves have also been recognized. It was found that trichomal cells, which greatly increase the surface area of the leaves, may have a role in the uptake of chemicals. In the epiphytic plant Tillandsia velutina, superior formaldehyde uptake was observed to be aided by the trichomes19. The Ectodesmata have also been described as a route by which a toxic compound may enter the leaves16. After the entry of the pollutants through the stomata or cuticle, they reach the sieve tubes of the phloem that allow their translocation, together with photosynthates, to roots or the rest of the shoot tissue16. It was speculated that plant leaves can potentially absorb formaldehyde and xylene from the air and translocate them, via the phloem/xylem, to the plant roots where they are degraded by

Fig. 2— Performance evaluation of the five plants for benzene degradation with an initial concentration of 5 ppm.

Table 3—Comparative studies of different kind of bioreactors with plant potted biofilter23-25 Bioreactor Application Advantages Disadvantages

Bio filter Removal of odour and low VOC concentration. Target concentration is less than 1 gm/m³.

Low initial investment and subsequently operating cost is minimized. Degrades a wide range of components. Easy to operate and maintain. No unnecessary waste streams are produced.

Less treatment efficiency at high concentrations of pollutants. Extremely large size of bioreactor challenges space constraints. Close control of operating conditions is required.

Bio Trickling Filter

Low / medium VOC concentration Target concentration is less than 0.5 g/m³.

Less operating and capital constraints. Less relation time / high volume through put. Capability to treat acid degradation product of VOCs.

Accumulation of excess biomass in the filter bed. Requirement of design for fluctuating concentration. Complexity in construct and operation. Secondary waste stream.

Membrane Bioreactor

Medium/High VOC concentration. Target concentration is less than 10 g/m³.

No moving parts. Process easy to scale up. Flow of gas and liquid can be varied independently, without the problems of flooding, loading, or foaming.

High construction costs. Long-term operational stability. (needs investigation) Possible clogging of the liquid channels due the formation of excess biomass.

Bio scrubber Low/medium VOC concentrations. Target VOC concentration less than 5 g/ m³.

Able to deal with high flow rates and severe fluctuations. Operational stability and better control of operating parameters. Relatively low pressure drops.

Treats only water-soluble compounds. Can be complicated to operate and maintain. Extra air supply may be needed. Excess sludge will require to disposal.

Plant Based biofilter (Present study)

Low VOC concentrations Target VOC concentration less than 5 g/m3

The potted plant system is also portable and hence flexible, and of considerable species diversity, which presumably also reflects substrate microbial diversity

Lower rate of VOC degradation. It can be possible to develop improved indoor potted plant/growth media combinations with enhanced capacities for leaning indoor air

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microorganisms20. However, sterile plants were also found to metabolize VOCs arguing against the VOC degradation by microorganisms21,22.

Bacterial isolation and number In case of Spider plant, the bacterial count in the

soil decreased from 2.08×106 CFU/mL to 3.88×104 CFU/mL, before and after plant exposure to benzene. The molecular characterization results confirmed Bacillus sp.

Growth curve Bacterial growth curves were plotted for initial

benzene concentrations of 100 ppm and 150 ppm. A control growth curve was also plotted wherein the substrate was not added. The µmax and Ks value for 100 ppm were calculated using Monod equation and was found to be 0.284 h-1 and 0.427 g/m3, respectively. The growth curves obtained for the isolated bacteria (method already described) for concentrations of 100 and 150 ppm are shown below (Fig. 3A). The final graph shows the curve in which the substrate is not added (Fig. 3B). Kureel et al.23 has reported the kinetic values of Monod growth model was applied for the removal of benzene and values were found to be (Ks: 215.07 mg⋅L−1; µmax: 0.314 day−1).

Optimization of growth conditions

Effect of Temperature From the graph below (Fig. 4A), it was evident that

the optimum temperature for the growth of bacteria is 35°C while all the experiments were carried out in the range of 25-45°C. Several researchers have done the optimization studies for the benzene degrading microorganisms and reported that 35±2C is optimum temperature for the Bacillus group microorganisms24.

Fig. 3—Growth curve of bacteria (blue) and degradation of benzene (red). Growth curve (A) 150 ppm benzene; and (B) in the absence of benzene (control)

Fig. 4—Growth of bacteria at different (A) temperature; and (B) pH values; and (C) at different initial concentrations of Benzene. [The optimum temperature value was obtained at 35°C; and optimum pH value was obtained at pH 7. The concentration of benzene after which inhibition of growth occurred was 400 ppm]

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Effect of pH After allowing the bacteria to grow in a range of

pH values, the optimum pH for growth of the organism was found to be 7 (Fig. 4B). Giri et al.11 has reported the best pH conditions for the VOCs degrading microorganisms are 7.0±0.5. The major microorganisms are Bacillus subtilis, Bacillus megaterium and Bacillus polymix3,24. Few researchers in recent past have studied the removal of extremally high VOCs concentration using biofilter and the activated carbon as a packing media at the pH 7.5 and temperature 352C 25-27. Effect of substrate concentration

Fig. 4C shows the effect of different substrate concentration at 100, 200, 400, 800 and 1000 ppm. At a benzene concentration of 400 ppm, bacterial growth is found to be inhibited.

Kumar et al.26 has studied toluene removal of VOCs in a cooler based biofilter in which Pseudomonas species and Bacillus species were used for Toluene biodegradable. The biofilter was inoculated with Pseudomonas sp. RSST (MG 279053). The performance of this biofilter, assessed in terms of toluene removal efficiency (and elimination capacity), was as high as 99% at a loading rate of 6 g/h·m2. The toluene removal efficiency decreased in an exponential manner with the increase in the loading rate. The cooler model-based biofilter was able to remove more than 99% of toluene. Conclusion

Out of the five plants (Spider plant, Snake plant, Janet Craig, Holy basil and Money plant) used, the money plant showed the maximum removal efficiency of 98%. Benzene at 5 ppm was degraded at a higher rate by this plant as compared to others. During the experiments, optimum temperature, pH and moisture conditions need to be maintained to ensure maximum growth of VOC degrading organisms. Studies with potted plants in closed chambers are useful for isolating factors that may enhance the efficiency of removal toxic contaminants, and therefore contribute towards improvement of Quality of Life.

Conflict of Interest The authors declare is no conflict of interest.

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