Bioresource Technology xxx (2014) xxx–xxx
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Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Evaluation of thermophilic fungal consortium for organic municipal solid waste composting Mukesh Kumar Awasthi a,b,c,⇑, Akhilesh Kumar Pandey d, Jamaluddin Khan e, Pushpendra Singh Bundela a, Jonathan W.C. Wong c, Ammaiyappan Selvam c a
Regional Office, Madhya Pradesh Pollution Control Board, Jabalpur, India Department of Biotechnology, Amicable Knowledge Solution University, Satna, India Sino-Forest Applied Research Centre for Pearl River Delta Environment, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China d Madhya Pradesh Private Universities Regulatory Commission, Bhopal, India e Mycological Research Laboratory, Department of Biological Sciences, Rani Durgavati University, Jabalpur, India b c
h i g h l i g h t s Composting of OFMSW employing fungal inoculum is a rapid and low cost technology. Inoculation of fungal consortium significantly improved compost humification. T. viride, A. niger and A. flavus are effective at a wide range of temperature. Weekly turning frequency is effective for OFMSW windrow composting.
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Article history: Available online xxxx Keywords: Composting Organic fraction of municipal solid waste Fungal consortium Inoculation Turning frequency
a b s t r a c t Influence of fungal consortium and different turning frequency on composting of organic fraction of municipal solid waste (OFMSW) was investigated to produce compost with higher agronomic value. Four piles of OFMSW were prepared: three piles were inoculated with fungal consortium containing 5 l each spore suspensions of Trichoderma viride, Aspergillus niger and Aspergillus flavus and with a turning frequency of weekly (Pile 1), twice a week (Pile 2) and daily (Pile 3), while Pile 4 with weekly turning and without fungal inoculation served as control. The fungal consortium with weekly (Pile 1) turning frequency significantly affected temperature, pH, TOC, TKN, C/N ratio and germination index. High degradation of organic matter and early maturity was observed in Pile 1. Results indicate that fungal consortium with weekly turning frequency of open windrows were more cost-effective in comparison with other technologies for efficient composting and yield safe end products. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Large quantities of municipal solid waste (MSW) are produced in modern society and its disposal poses serious environmental, social and economic problems. India nearly generates about 700 million tons of organic waste annually from cities alone (Pan et al., 2012). Rapid expansion of the cities/towns with massive migration of population from rural to urban centers caused considerable increases in per capita of MSW generation. The increasing rate of solid waste generation, limited landfill space and more stringent environmental regulations for new landfill sites and incinerators ⇑ Corresponding author at: Department of Biotechnology, Amicable Knowledge Solution University, Satna, India. Tel.: +91 7672 4037776/9981124776; fax: +91 7672 4037776. E-mail address: [email protected] (M.K. Awasthi).
have increased the waste disposal fees especially in developing countries. Therefore, municipalities and local governments are under heavy pressure to find sustainable and cost-effective solid waste management practices (Saha et al., 2010; Sharholy et al., 2008). In Jabalpur, Madhya Pradesh, India, about 450 tons of MSW consisting of household, market waste and yard wastes are generated; and 65% are disposed in the landfills while the remaining is disposal off in the open environments (Gautam et al., 2010). Biological treatment such as composting of the organic fraction of MSW (OFMSW) is an environmentally and economically viable solution (Tosun et al., 2008). Windrow composting is widely used for sanitary disposal of OFMSW. Several earlier researchers performed small-scale composting of OFMSW by windrow method, where it took between three and
http://dx.doi.org/10.1016/j.biortech.2014.01.048 0960-8524/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
four months to produce compost; but the quality and maturity were uncertain (Adam and Frostick, 2009). During composting, decomposition of organic matter (OM) was very high under thermophilic conditions as high rate of biooxidation of organic materials begins at 40 °C (Huang et al., 2006). The increase in temperature facilitates the destruction of the large number of pathogenic microbes and weed seeds (Chang et al., 2006; Said-Pullicino et al., 2007). Natural composting process takes long duration for degradation; however, the shortage of lands and large volume of OFMSW require these wastes to be treated more quickly. The inoculation with lignocellulolytic fungi could potentially enhance the organic degradation. Fungal species such as Trichoderma viride, Aspergillus niger and white-rot fungi are able to degrade the cellulolytic and lignolytic waste (Huang et al., 2006; Vargas-Gracia et al., 2010; Yu et al., 2007). These microorganisms considerably reduced the composting time of OFMSW (Crecchio et al., 2004; Zeng et al., 2010). Chemical and microbiological changes have been studied during OFMSW composting under field conditions in windrows and heaps (Adam and Frostick, 2009), and in a laboratory scale composting keeping temperature constant artificially (Zeng et al., 2010). Aeration and microbial inoculums are important factors of influencing composting because composting is basically an aerobic process, where O2 is consumed, and gaseous H2O and CO2 are produced. A few researches have demonstrated that single component cellulase or cellulase from pure cultures could not convert highly ordered polymer into monomer efficiently (Lin et al., 2011). Mixing of several types of enzymes like cellulase, protease, amylase and lipase acting synergistically has been proven to be an effective strategy for improving OFMSW composting (Echeverria et al., 2012). Since no single microorganism could produce all the necessary enzymes for complete decomposition of OFMSW, use of microbial consortia which act synergistically for rapid bioconversion of OFMSW biomass is attractive (Elango et al., 2009; Liu et al., 2011). Previously, many researchers reported the use of microbial consortium for organic waste composting; but they all were performed under laboratory conditions and not exactly applicable to windrow composting; thus optimizing the turning frequency was not a criterion (Raut et al., 2008; Lin et al., 2011; Echeverria et al., 2012). Nowadays, commercial interest is emerging for effective microbial starter cultures for efficient windrow composting. However, available literature indicates that no data have been published on the windrow composting of OFMSW inoculated with fungal consortium under different turning frequency. If these deficiencies are addressed in a windrow of reasonable size then the results will be of potential commercial value. Therefore, the objectives of this study were to evaluate the effectiveness of fungal consortium to reduce composting time and compare with different turning frequencies required for OFMSW windrow composting to achieve rapid, cost effective treatment and obtain products of high nutritional value. 2. Methods 2.1. Organic municipal solid waste collection and processing Different putrescible components of the MSW including vegetables waste, food waste, garden waste and office waste were separately collected from eight different zones of Jabalpur city; wastes were chopped into 10–20 mm length using a mechanical chopper before used as substrate. Selected physicochemical properties of the raw materials prior to composting are presented in Table 1. 2.2. Composting pile establishment Four piles of 5 ton shredded OFMSW each were prepared by mixing of food, vegetable, garden and office wastes at 1:1:1:1 ratio
(w/w wet weight basis), and mixed with 250 kg of wood shaving to achieve the initial C/N ratio of 25 to 30 and bulk density of 0.5 kg/ L. Windrow composting piles approximately 5 m 1 m 1.5 m (length width height) each were formed using a front end loader, and were composted for 35 days (Fig. 1). All windrows were mechanically turned using a loading shovel, with different turning frequencies; Pile 1 once a week, Pile 2 twice a week and Pile 3 every day while the Pile 4 was turned weekly. Piles 1–3 were supplemented with fungal inoculum while the Pile 4 without fungal inoculation served as control for Pile 1. The moisture content was adjusted to about 60% at the beginning of composting and then periodically water was added during the turning of composting when necessary to increase the moisture content. During the composting, temperatures were measured at different locations (Fig. 1), including the top (125 cm from the base of the pile), the middle (85 cm from the base of the pile) using a Raytek infrared digital thermometer (range: 20–100 °C, measurement accuracy: ±0.5 °C). Triplicate composite samples were collected periodically on days 0, 5, 10, 15, 20, 25, 30 and 35. For each pile, samples were randomly collected from ten different places of the piles and mixed to obtain composite samples. The sampling locations are indicated in Fig. 1. 2.3. Chemical analyses The moisture content of samples was determined based on weight loss at 105 °C, while pH and electrical conductivity (EC) of the aqueous extract of fresh samples were (1:5, w/v, sample/ water ratio) measured using a pH electrode (PB-10, Sartorius) and conductivity electrode (LF91, Wiss. Techn. Werkstatten). Total organic carbon (TOC), total Kjeldhal nitrogen (TKN), total phosphorous (TP), total sodium (TNa), total potassium (TK)and heavy metals (Cd, Pb, Cu, Cr, Zn and Ni) were determined following the methods (04.01–04.06) of TMECC (2002). The C/N ratio was calculated as the ratio of TOC to TKN. E4/E6 ratio of humic and fulvic acids was determined in aqueous extract using spectrometry determination at 460 and 660 nm, respectively (Page et al., 1982). 2.4. Microbial source and inoculums preparation About 35 different fungal species were isolated and/or procured from the IMTECH, Chandigarh, India for screening. Selection of the strains for this study was made on the basis of enzymatic activity (cellualses, protease, amylase and lipases) at a wide range of temperature and pH, and substrate specific organic waste degradation at flask scale experiment (data not shown). Based on the performance of synergistic enzymatic activity the following species were selected for the inoculation in this study: Trichoderma viride MTCC 793, Aspergillus niger MTCC 1344 and Aspergillus flavus MTCC 1425. The selected strains were cultivated on potato dextrose agar, spores were collected from the agar surface plates with phosphate-buffered saline (PBS), quantified using microscope and suspended in 5 l autoclaved distilled water with PBS and 0.05% Tween 80. After that spore suspensions each of T. viride (6.8 106 spore/mL1), A. niger (4.5 104 spore/mL1) and A. flavus (4.5 104 spore/mL1) were mixed with 14 kg of air dried OFMSW with a particle size of 55 °C except the bottom, and the peak temperatures of Pile 1 and Pile 2 were observed on day 5 for all locations except in Pile 3, in which the temperature increased gradually and reached its peak on 14th day. The temperature of Pile 1 with weekly and Pile 2 twice in a week turning frequency decreased sharply after the thermophilic phase and entered a cooling phase after 28 days, while in Pile 3 with daily turning decreased sharply after the thermophilic phase and entered the cooling phase after 22 days. The decrease in the temperature of Piles 1 and 2 was attributed to the depletion of easily degradable organic materials, whereas the low temperature of Pile 3 at the later stage as well as the slow increase in temperature at the beginning of composting may be explained by a higher heat and water loss by evaporation and convection, respectively, caused by the higher frequency of turning (Castaldi et al., 2008; Wong et al., 2001). The piles inoculated with fungal consortia showed higher temperature due to the growth of microbes and more rapid decomposition of substrate, while control without inoculation (Pile 4) showed low temperatures throughout the composting. The microorganisms consumed the soluble organic matter, which then underwent aerobic degradation to generate heat, biomass and carbon dioxide. Most data in the literature indicate that the optimum temperature range for effective decomposition is 50–60 °C, while others reported that maximum decomposition of municipal solid waste occurs at temperatures between 65 and 70 °C that could destroy pathogenic organisms and undesirable weed seeds (Tosun et al., 2008; Crecchio et al., 2004).
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
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3.1.3. Changes in total organic carbon (TOC) and total Kjeldhal nitrogen (TKN) The TOC contents of the composting mass indifferent piles gradually decreased with composting time (Fig. 3a). The initial TOC content in the piles varied from 45.2%, 42.8%, 43.8% and 43.7% in the Piles1, 2, 3 and 4, respectively. If the organic carbon content of compost is higher than 40–43%, the composting is considered to be incomplete (Raut et al., 2008). In this study, the TOC content of compost from all piles was in the range of 25–30% except Pile 4, as presented in Fig. 3a. At the end of the composting process, the fungal consortium inoculated piles contained lower TOC contents (25.4%, 26.7% and 28.6% of Piles 1, 2 and 3, respectively), while the highest in control Pile 4 (33.8%). The high TOC of Pile 4 was mainly due to the delay in the thermophilic period, resulting in
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values >4 mS cm1 will adversely influence plant growth e.g. low germination rate, withering, etc. (Wong et al., 2001). While compost with low EC can be used directly, compost with high EC must be mixed well with soil or other materials with low EC before it can be used for growing crop. The EC values of the piles were higher at end of the composting process, however lower than the limit and will not affect plant growth (Fig. 2c). The initial EC values were 1.36, 1.24, 1.39 and 1.42 mS cm1 in the Piles 1, 2, 3 and 4 respectively; and then gradually increases. The initial increase in EC is caused by the biotransformation of complex materials to simple compounds such as mineral ions (e.g. phosphate, ammonium and potassium etc.) (Hassen et al., 2001).The EC of Piles 3 and 4 at end of composting was significantly lower (P > 0.05) than those treatments with twice a week and weekly turning.
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Fig. 2. Changes of temperature (a), pH (b) and electrical conductivity (EC) (c) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and error bars indicate standard deviation.
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3.1.2. pH and EC The pH of all the piles initially decreased gradually during composting due to the fermentative metabolism that results in the production of organic acids in high quantities; and then increased (Fig. 2b) similar to the results reported by Nakasaki et al. (2005). The pH of Piles 1, 2 and 3 decreased gradually in the first 5 days and then increased until the end of composting, while that of Pile 4 decreased until day 20 after that slightly increased. The increase in pH was attributed to the production of ammonia associated with protein degradation in the raw materials and to the decomposition of organic acids as reported previously (Warman and Tremmeer, 2005). The relatively low pH of Pile 4 (without fungal consortium) might be due to the slow rate of decomposition. Under aerobic conditions, organic N is transformed into NH3 or NHþ 4 during ammonification, increasing the pH of the pile (Wong et al., 2001). If the oxygen content is sufficient, ammonia oxidizing bacteria and nitrifying bacteria will transform NH3 into NO2 subsequently to NO3. This process is called nitrification and releases H+, reducing the pH of the environment (Nakasaki et al., 2005). The electrical conductivity (EC) indicates the total salt content of compost reflecting the quality of compost to be used as a fertilizer. High EC indicates the presence of more soluble products and
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Fig. 3. Changes of total organic carbon (a) and total Kjeldahl nitrogen (b) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and bars indicate standard deviation.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
slow and low decomposition. High CO2 was emitted during the thermophilic period because of the rapid degradation of easily degradable carbon under vigorous bacterial and fungal metabolism. During the curing period, CO2 emissions are related to the degradation of complex organic molecules such as lignin
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and lignocelluloses by some fungi and actinomycetes (Gracia et al., 1993; Elango et al., 2009). TKN contents was gradually decreased with time until day 20 and then increased continuously, except in Pile 4, where there was no obvious change over the time (Fig. 3b) that can mainly
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Time (Days) Fig. 4. Changes in the populations of total aerobic bacteria (a), filamentous eumycetes (b), actinomycetes (c), total aerobic cellulolytic bacteria (d), total aerobic cellulolytic fungi (e) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates ± standard deviation. Data area expressed as log CFU g1dw.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
The changes in the populations of culturable microbial biomass demonstrated an intensive microbial colonization of the substrate during the composting process; and differences in populations of bacteria were observed among all piles (Fig. 4a–e). The total bacterial and fungal populations of Pile 1 increased gradually and were found to be the highest on day 20, and then decreased gradually until the end of composting period. Total aerobic bacteria in Pile 2 peaked on 25th day but did not show a subsequent reduction; in contrast, the aerobic bacteria in Pile 3 increased slowly as compare to the bacteria in other piles. The three-day and weekly turned piles enhanced the aerobic bacterial population, while Pile 3 with every day turning did not significantly increase the bacterial population. Similarly, the highest filamentous eumycetes population was observed on 20th day in Pile 1, while it was observed after 25th day in Pile 2; and the population then decreased sharply in the both the piles. In contrast, in the Piles 3 and 4, the filamentous fungal population increased gradually and then remained at a relatively stable level until the end of the composting. In early stage of composting, bacteria were the dominant group responsible for the initial decomposition of organic matter and the generation of heat (Hassen et al., 2001). Liu et al. (2011) studied microbial succession during composting and reported that most of the fungi were eliminated when the temperature exceeded 50 °C but the population re-colonized when the temperature decreased to below 45 °C. However, a large population of fungi was observed during the active phase of composting. Similar results were also obtained by Goyal et al. (2005) who reported a high mesophilic population (4.4 106 cfu/g1dw). In the present study, there were no significant differences in the size of the actinomycetes community among the three piles during the initial stages of composting. In Pile 1, the population of actinomycetes increased quickly, and the peak values were observed during the active phase (20th day). In contrast to other microorganisms, the population of actinomycetes in all piles was lower than in Pile 1 on day 25. Cellulolytic microbial communities play a key role in the biodegradation during composting because cellulose are the main component of organic wastes (Vargas-Gracia et al., 2010). The communities involved in cellulose biotransformation were detected throughout the composting process. The succession of cellulolyitc bacteria reached the peak values in all three piles at different stages of the process although the rates of increase in Piles 1, 2 and 3 were very low during the initial phase of composting. These low rates might be due to the existence of copious water-soluble carbon fractions at the early stage of the process. Microorganisms preferentially use these soluble and easilydegradable carbon sources, which were present in the starting material; however, once the easily degraded compounds were exhausted, the complex substrates such as cellulosic materials
3.3. Maturity evaluation 3.3.1. Changes in C/N ratio The C/N ratio is an important parameter to indicate the compost maturity, which may generally be affected by variations of the organic matter and its characteristics. A C/N ratio equal to or less than 25 is the standard for mature compost. The C/N ratio usually shows a decreasing tendency as the composting progresses. The C/ N ratio of the initial raw material mixture were 36.12, 31.43, 31.49 and 34.54 in the Piles 1, 2, 3 and 4 respectively, which decreased gradually and reached 17.12, 17.52, 19.47 and 26.18 at the end of composting (Fig. 5a). Therefore, all treatments with different turning frequency reached maturity after 35 days, except Pile 4 due to slow rate of decomposition. Chang et al. (2006) pointed out that the C/N ratio of mature compost should be less than 30. Higher C/N ratios would cause nitrogen to volatize thus reducing the nitrogen content while lower C/N ratios would release a large
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3.2. Changes in the microbial population during the composting process
started to be degraded, resulting in the increase in cellulolytic microbial communities. The progression of cellulolytic fungi in the piles was different from those of cellulolytic bacterial populations. The population size of cellulolytic fungi increased gradually and the highest populations were observed on day 15 in Pile 1, while on day 10 for Piles 2 and 3.
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attributable to the low organic decomposition. Castaldi et al. (2008) observed that the easily degradable protienaceous components in OFMSW were readily solubilized during initial periods of composting. Decreasing TKN contents observed in this study was similar to previous results of Tosun et al. (2008). The decline in TKN could have mainly resulted from ammonia volatilization. The higher temperature and pH favored the formation of NH3, which would subsequently volatilize. High frequency of turning could also hastened the volatilization and increase TKN losses (Huang et al., 2006).The increase in the TKN content at the later period of composting was mainly due to the concentration effect. However, TKN also be increased by the activities of nitrogen-fixing bacteria as reported by Nakasaki et al. (2005).
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Time (Days) Fig. 5. Changes of C/N ratio (a), germination index (GI) (b) and E4/E6 (c) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and bars indicate standard deviation.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
7
M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx Table 2 Physicochemical characteristics of compost (dry weight basis). Parameters
Pile 1
Pile 2
Pile 3
Pile 4
FAI (2007)
TMECC (2002), CCME (2005)
Moisture content (%) pH Electrical conductivity (mS cm1) Total organic carbon (%) Total organic matter (%) Total phosphorus (%) TKN (%) C:N ratio Sodium (%) Potassium (%) Copper (mg/kg) Cadmium (mg/kg) Zinc (mg/kg) Nickel (mg/kg) Lead (mg/kg) Chromium (mg/kg)
37 ± 0.7 7.95 ± 0.02 3.48 ± 0.02 25.35 ± 1.34 24.38 ± 1.23 0.82 ± 0.01 1.48 ± 0.14 17.12 ± 1.21 2.4 ± 0.33 1.4 ± 0.25 87.16 ± 2.95 1.5 ± 0.34 132.0 ± 2.14 21.4 ± 0.31 19.2 ± 0.27 27.8 ± 1.78
39 ± 0.3 7.89 ± 0.04 3.35 ± 0.04 26.72 ± 0.70 25.46 ± 0.41 0.76 ± 0.04 1.52 ± 0.06 17.52 ± 2.42 2.7 ± 0.21 1.3 ± 0.43 72.8 ± 3.55 NA 146.0 ± 3.21 14.6 ± 0.06 22.1 ± 0.48 23.1 ± 2.25
35 ± 0.4 7.65 ± 0.02 3.46 ± 0.03 28.56 ± 1.15 24.63 ± 1.95 0.87 ± 0.02 1.46 ± 0.10 19.47 ± 1.07 3.1 ± 0.45 1.6 ± 0.06 104.6 ± 1.29 0.9 ± 0.12 81.27 ± 2.43 18.2 ± 0.42 13.7 ± 0.21 11.3 ± 0.85
43 ± 0.7 6.72 ± 0.05 2.42 ± 0.02 33.78 ± 1.53 32.49 ± 2.70 0.61 ± 0.02 1.29 ± 0.08 26.18 ± 1.16 1.8 ± 0.18 1.1 ± 0.03 78.3 ± 2.74 1.4 ± 0.05 127.0 ± 3.62 27.4 ± 0.16 19.6 ± 0.36 25.3 ± 1.42
35–55 6.5–8.5 2–6 P16 >30 0.4–1.1 1.0–3.0
Contents lists available at ScienceDirect
Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Evaluation of thermophilic fungal consortium for organic municipal solid waste composting Mukesh Kumar Awasthi a,b,c,⇑, Akhilesh Kumar Pandey d, Jamaluddin Khan e, Pushpendra Singh Bundela a, Jonathan W.C. Wong c, Ammaiyappan Selvam c a
Regional Office, Madhya Pradesh Pollution Control Board, Jabalpur, India Department of Biotechnology, Amicable Knowledge Solution University, Satna, India Sino-Forest Applied Research Centre for Pearl River Delta Environment, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China d Madhya Pradesh Private Universities Regulatory Commission, Bhopal, India e Mycological Research Laboratory, Department of Biological Sciences, Rani Durgavati University, Jabalpur, India b c
h i g h l i g h t s Composting of OFMSW employing fungal inoculum is a rapid and low cost technology. Inoculation of fungal consortium significantly improved compost humification. T. viride, A. niger and A. flavus are effective at a wide range of temperature. Weekly turning frequency is effective for OFMSW windrow composting.
a r t i c l e
i n f o
Article history: Available online xxxx Keywords: Composting Organic fraction of municipal solid waste Fungal consortium Inoculation Turning frequency
a b s t r a c t Influence of fungal consortium and different turning frequency on composting of organic fraction of municipal solid waste (OFMSW) was investigated to produce compost with higher agronomic value. Four piles of OFMSW were prepared: three piles were inoculated with fungal consortium containing 5 l each spore suspensions of Trichoderma viride, Aspergillus niger and Aspergillus flavus and with a turning frequency of weekly (Pile 1), twice a week (Pile 2) and daily (Pile 3), while Pile 4 with weekly turning and without fungal inoculation served as control. The fungal consortium with weekly (Pile 1) turning frequency significantly affected temperature, pH, TOC, TKN, C/N ratio and germination index. High degradation of organic matter and early maturity was observed in Pile 1. Results indicate that fungal consortium with weekly turning frequency of open windrows were more cost-effective in comparison with other technologies for efficient composting and yield safe end products. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Large quantities of municipal solid waste (MSW) are produced in modern society and its disposal poses serious environmental, social and economic problems. India nearly generates about 700 million tons of organic waste annually from cities alone (Pan et al., 2012). Rapid expansion of the cities/towns with massive migration of population from rural to urban centers caused considerable increases in per capita of MSW generation. The increasing rate of solid waste generation, limited landfill space and more stringent environmental regulations for new landfill sites and incinerators ⇑ Corresponding author at: Department of Biotechnology, Amicable Knowledge Solution University, Satna, India. Tel.: +91 7672 4037776/9981124776; fax: +91 7672 4037776. E-mail address: [email protected] (M.K. Awasthi).
have increased the waste disposal fees especially in developing countries. Therefore, municipalities and local governments are under heavy pressure to find sustainable and cost-effective solid waste management practices (Saha et al., 2010; Sharholy et al., 2008). In Jabalpur, Madhya Pradesh, India, about 450 tons of MSW consisting of household, market waste and yard wastes are generated; and 65% are disposed in the landfills while the remaining is disposal off in the open environments (Gautam et al., 2010). Biological treatment such as composting of the organic fraction of MSW (OFMSW) is an environmentally and economically viable solution (Tosun et al., 2008). Windrow composting is widely used for sanitary disposal of OFMSW. Several earlier researchers performed small-scale composting of OFMSW by windrow method, where it took between three and
http://dx.doi.org/10.1016/j.biortech.2014.01.048 0960-8524/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
four months to produce compost; but the quality and maturity were uncertain (Adam and Frostick, 2009). During composting, decomposition of organic matter (OM) was very high under thermophilic conditions as high rate of biooxidation of organic materials begins at 40 °C (Huang et al., 2006). The increase in temperature facilitates the destruction of the large number of pathogenic microbes and weed seeds (Chang et al., 2006; Said-Pullicino et al., 2007). Natural composting process takes long duration for degradation; however, the shortage of lands and large volume of OFMSW require these wastes to be treated more quickly. The inoculation with lignocellulolytic fungi could potentially enhance the organic degradation. Fungal species such as Trichoderma viride, Aspergillus niger and white-rot fungi are able to degrade the cellulolytic and lignolytic waste (Huang et al., 2006; Vargas-Gracia et al., 2010; Yu et al., 2007). These microorganisms considerably reduced the composting time of OFMSW (Crecchio et al., 2004; Zeng et al., 2010). Chemical and microbiological changes have been studied during OFMSW composting under field conditions in windrows and heaps (Adam and Frostick, 2009), and in a laboratory scale composting keeping temperature constant artificially (Zeng et al., 2010). Aeration and microbial inoculums are important factors of influencing composting because composting is basically an aerobic process, where O2 is consumed, and gaseous H2O and CO2 are produced. A few researches have demonstrated that single component cellulase or cellulase from pure cultures could not convert highly ordered polymer into monomer efficiently (Lin et al., 2011). Mixing of several types of enzymes like cellulase, protease, amylase and lipase acting synergistically has been proven to be an effective strategy for improving OFMSW composting (Echeverria et al., 2012). Since no single microorganism could produce all the necessary enzymes for complete decomposition of OFMSW, use of microbial consortia which act synergistically for rapid bioconversion of OFMSW biomass is attractive (Elango et al., 2009; Liu et al., 2011). Previously, many researchers reported the use of microbial consortium for organic waste composting; but they all were performed under laboratory conditions and not exactly applicable to windrow composting; thus optimizing the turning frequency was not a criterion (Raut et al., 2008; Lin et al., 2011; Echeverria et al., 2012). Nowadays, commercial interest is emerging for effective microbial starter cultures for efficient windrow composting. However, available literature indicates that no data have been published on the windrow composting of OFMSW inoculated with fungal consortium under different turning frequency. If these deficiencies are addressed in a windrow of reasonable size then the results will be of potential commercial value. Therefore, the objectives of this study were to evaluate the effectiveness of fungal consortium to reduce composting time and compare with different turning frequencies required for OFMSW windrow composting to achieve rapid, cost effective treatment and obtain products of high nutritional value. 2. Methods 2.1. Organic municipal solid waste collection and processing Different putrescible components of the MSW including vegetables waste, food waste, garden waste and office waste were separately collected from eight different zones of Jabalpur city; wastes were chopped into 10–20 mm length using a mechanical chopper before used as substrate. Selected physicochemical properties of the raw materials prior to composting are presented in Table 1. 2.2. Composting pile establishment Four piles of 5 ton shredded OFMSW each were prepared by mixing of food, vegetable, garden and office wastes at 1:1:1:1 ratio
(w/w wet weight basis), and mixed with 250 kg of wood shaving to achieve the initial C/N ratio of 25 to 30 and bulk density of 0.5 kg/ L. Windrow composting piles approximately 5 m 1 m 1.5 m (length width height) each were formed using a front end loader, and were composted for 35 days (Fig. 1). All windrows were mechanically turned using a loading shovel, with different turning frequencies; Pile 1 once a week, Pile 2 twice a week and Pile 3 every day while the Pile 4 was turned weekly. Piles 1–3 were supplemented with fungal inoculum while the Pile 4 without fungal inoculation served as control for Pile 1. The moisture content was adjusted to about 60% at the beginning of composting and then periodically water was added during the turning of composting when necessary to increase the moisture content. During the composting, temperatures were measured at different locations (Fig. 1), including the top (125 cm from the base of the pile), the middle (85 cm from the base of the pile) using a Raytek infrared digital thermometer (range: 20–100 °C, measurement accuracy: ±0.5 °C). Triplicate composite samples were collected periodically on days 0, 5, 10, 15, 20, 25, 30 and 35. For each pile, samples were randomly collected from ten different places of the piles and mixed to obtain composite samples. The sampling locations are indicated in Fig. 1. 2.3. Chemical analyses The moisture content of samples was determined based on weight loss at 105 °C, while pH and electrical conductivity (EC) of the aqueous extract of fresh samples were (1:5, w/v, sample/ water ratio) measured using a pH electrode (PB-10, Sartorius) and conductivity electrode (LF91, Wiss. Techn. Werkstatten). Total organic carbon (TOC), total Kjeldhal nitrogen (TKN), total phosphorous (TP), total sodium (TNa), total potassium (TK)and heavy metals (Cd, Pb, Cu, Cr, Zn and Ni) were determined following the methods (04.01–04.06) of TMECC (2002). The C/N ratio was calculated as the ratio of TOC to TKN. E4/E6 ratio of humic and fulvic acids was determined in aqueous extract using spectrometry determination at 460 and 660 nm, respectively (Page et al., 1982). 2.4. Microbial source and inoculums preparation About 35 different fungal species were isolated and/or procured from the IMTECH, Chandigarh, India for screening. Selection of the strains for this study was made on the basis of enzymatic activity (cellualses, protease, amylase and lipases) at a wide range of temperature and pH, and substrate specific organic waste degradation at flask scale experiment (data not shown). Based on the performance of synergistic enzymatic activity the following species were selected for the inoculation in this study: Trichoderma viride MTCC 793, Aspergillus niger MTCC 1344 and Aspergillus flavus MTCC 1425. The selected strains were cultivated on potato dextrose agar, spores were collected from the agar surface plates with phosphate-buffered saline (PBS), quantified using microscope and suspended in 5 l autoclaved distilled water with PBS and 0.05% Tween 80. After that spore suspensions each of T. viride (6.8 106 spore/mL1), A. niger (4.5 104 spore/mL1) and A. flavus (4.5 104 spore/mL1) were mixed with 14 kg of air dried OFMSW with a particle size of 55 °C except the bottom, and the peak temperatures of Pile 1 and Pile 2 were observed on day 5 for all locations except in Pile 3, in which the temperature increased gradually and reached its peak on 14th day. The temperature of Pile 1 with weekly and Pile 2 twice in a week turning frequency decreased sharply after the thermophilic phase and entered a cooling phase after 28 days, while in Pile 3 with daily turning decreased sharply after the thermophilic phase and entered the cooling phase after 22 days. The decrease in the temperature of Piles 1 and 2 was attributed to the depletion of easily degradable organic materials, whereas the low temperature of Pile 3 at the later stage as well as the slow increase in temperature at the beginning of composting may be explained by a higher heat and water loss by evaporation and convection, respectively, caused by the higher frequency of turning (Castaldi et al., 2008; Wong et al., 2001). The piles inoculated with fungal consortia showed higher temperature due to the growth of microbes and more rapid decomposition of substrate, while control without inoculation (Pile 4) showed low temperatures throughout the composting. The microorganisms consumed the soluble organic matter, which then underwent aerobic degradation to generate heat, biomass and carbon dioxide. Most data in the literature indicate that the optimum temperature range for effective decomposition is 50–60 °C, while others reported that maximum decomposition of municipal solid waste occurs at temperatures between 65 and 70 °C that could destroy pathogenic organisms and undesirable weed seeds (Tosun et al., 2008; Crecchio et al., 2004).
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
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3.1.3. Changes in total organic carbon (TOC) and total Kjeldhal nitrogen (TKN) The TOC contents of the composting mass indifferent piles gradually decreased with composting time (Fig. 3a). The initial TOC content in the piles varied from 45.2%, 42.8%, 43.8% and 43.7% in the Piles1, 2, 3 and 4, respectively. If the organic carbon content of compost is higher than 40–43%, the composting is considered to be incomplete (Raut et al., 2008). In this study, the TOC content of compost from all piles was in the range of 25–30% except Pile 4, as presented in Fig. 3a. At the end of the composting process, the fungal consortium inoculated piles contained lower TOC contents (25.4%, 26.7% and 28.6% of Piles 1, 2 and 3, respectively), while the highest in control Pile 4 (33.8%). The high TOC of Pile 4 was mainly due to the delay in the thermophilic period, resulting in
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EC (mS cm )
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values >4 mS cm1 will adversely influence plant growth e.g. low germination rate, withering, etc. (Wong et al., 2001). While compost with low EC can be used directly, compost with high EC must be mixed well with soil or other materials with low EC before it can be used for growing crop. The EC values of the piles were higher at end of the composting process, however lower than the limit and will not affect plant growth (Fig. 2c). The initial EC values were 1.36, 1.24, 1.39 and 1.42 mS cm1 in the Piles 1, 2, 3 and 4 respectively; and then gradually increases. The initial increase in EC is caused by the biotransformation of complex materials to simple compounds such as mineral ions (e.g. phosphate, ammonium and potassium etc.) (Hassen et al., 2001).The EC of Piles 3 and 4 at end of composting was significantly lower (P > 0.05) than those treatments with twice a week and weekly turning.
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Fig. 2. Changes of temperature (a), pH (b) and electrical conductivity (EC) (c) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and error bars indicate standard deviation.
Total organic carbon (%)
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3.1.2. pH and EC The pH of all the piles initially decreased gradually during composting due to the fermentative metabolism that results in the production of organic acids in high quantities; and then increased (Fig. 2b) similar to the results reported by Nakasaki et al. (2005). The pH of Piles 1, 2 and 3 decreased gradually in the first 5 days and then increased until the end of composting, while that of Pile 4 decreased until day 20 after that slightly increased. The increase in pH was attributed to the production of ammonia associated with protein degradation in the raw materials and to the decomposition of organic acids as reported previously (Warman and Tremmeer, 2005). The relatively low pH of Pile 4 (without fungal consortium) might be due to the slow rate of decomposition. Under aerobic conditions, organic N is transformed into NH3 or NHþ 4 during ammonification, increasing the pH of the pile (Wong et al., 2001). If the oxygen content is sufficient, ammonia oxidizing bacteria and nitrifying bacteria will transform NH3 into NO2 subsequently to NO3. This process is called nitrification and releases H+, reducing the pH of the environment (Nakasaki et al., 2005). The electrical conductivity (EC) indicates the total salt content of compost reflecting the quality of compost to be used as a fertilizer. High EC indicates the presence of more soluble products and
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Fig. 3. Changes of total organic carbon (a) and total Kjeldahl nitrogen (b) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and bars indicate standard deviation.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
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M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
slow and low decomposition. High CO2 was emitted during the thermophilic period because of the rapid degradation of easily degradable carbon under vigorous bacterial and fungal metabolism. During the curing period, CO2 emissions are related to the degradation of complex organic molecules such as lignin
10
and lignocelluloses by some fungi and actinomycetes (Gracia et al., 1993; Elango et al., 2009). TKN contents was gradually decreased with time until day 20 and then increased continuously, except in Pile 4, where there was no obvious change over the time (Fig. 3b) that can mainly
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Time (Days) Fig. 4. Changes in the populations of total aerobic bacteria (a), filamentous eumycetes (b), actinomycetes (c), total aerobic cellulolytic bacteria (d), total aerobic cellulolytic fungi (e) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates ± standard deviation. Data area expressed as log CFU g1dw.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx
The changes in the populations of culturable microbial biomass demonstrated an intensive microbial colonization of the substrate during the composting process; and differences in populations of bacteria were observed among all piles (Fig. 4a–e). The total bacterial and fungal populations of Pile 1 increased gradually and were found to be the highest on day 20, and then decreased gradually until the end of composting period. Total aerobic bacteria in Pile 2 peaked on 25th day but did not show a subsequent reduction; in contrast, the aerobic bacteria in Pile 3 increased slowly as compare to the bacteria in other piles. The three-day and weekly turned piles enhanced the aerobic bacterial population, while Pile 3 with every day turning did not significantly increase the bacterial population. Similarly, the highest filamentous eumycetes population was observed on 20th day in Pile 1, while it was observed after 25th day in Pile 2; and the population then decreased sharply in the both the piles. In contrast, in the Piles 3 and 4, the filamentous fungal population increased gradually and then remained at a relatively stable level until the end of the composting. In early stage of composting, bacteria were the dominant group responsible for the initial decomposition of organic matter and the generation of heat (Hassen et al., 2001). Liu et al. (2011) studied microbial succession during composting and reported that most of the fungi were eliminated when the temperature exceeded 50 °C but the population re-colonized when the temperature decreased to below 45 °C. However, a large population of fungi was observed during the active phase of composting. Similar results were also obtained by Goyal et al. (2005) who reported a high mesophilic population (4.4 106 cfu/g1dw). In the present study, there were no significant differences in the size of the actinomycetes community among the three piles during the initial stages of composting. In Pile 1, the population of actinomycetes increased quickly, and the peak values were observed during the active phase (20th day). In contrast to other microorganisms, the population of actinomycetes in all piles was lower than in Pile 1 on day 25. Cellulolytic microbial communities play a key role in the biodegradation during composting because cellulose are the main component of organic wastes (Vargas-Gracia et al., 2010). The communities involved in cellulose biotransformation were detected throughout the composting process. The succession of cellulolyitc bacteria reached the peak values in all three piles at different stages of the process although the rates of increase in Piles 1, 2 and 3 were very low during the initial phase of composting. These low rates might be due to the existence of copious water-soluble carbon fractions at the early stage of the process. Microorganisms preferentially use these soluble and easilydegradable carbon sources, which were present in the starting material; however, once the easily degraded compounds were exhausted, the complex substrates such as cellulosic materials
3.3. Maturity evaluation 3.3.1. Changes in C/N ratio The C/N ratio is an important parameter to indicate the compost maturity, which may generally be affected by variations of the organic matter and its characteristics. A C/N ratio equal to or less than 25 is the standard for mature compost. The C/N ratio usually shows a decreasing tendency as the composting progresses. The C/ N ratio of the initial raw material mixture were 36.12, 31.43, 31.49 and 34.54 in the Piles 1, 2, 3 and 4 respectively, which decreased gradually and reached 17.12, 17.52, 19.47 and 26.18 at the end of composting (Fig. 5a). Therefore, all treatments with different turning frequency reached maturity after 35 days, except Pile 4 due to slow rate of decomposition. Chang et al. (2006) pointed out that the C/N ratio of mature compost should be less than 30. Higher C/N ratios would cause nitrogen to volatize thus reducing the nitrogen content while lower C/N ratios would release a large
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30 C/N ratio
3.2. Changes in the microbial population during the composting process
started to be degraded, resulting in the increase in cellulolytic microbial communities. The progression of cellulolytic fungi in the piles was different from those of cellulolytic bacterial populations. The population size of cellulolytic fungi increased gradually and the highest populations were observed on day 15 in Pile 1, while on day 10 for Piles 2 and 3.
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attributable to the low organic decomposition. Castaldi et al. (2008) observed that the easily degradable protienaceous components in OFMSW were readily solubilized during initial periods of composting. Decreasing TKN contents observed in this study was similar to previous results of Tosun et al. (2008). The decline in TKN could have mainly resulted from ammonia volatilization. The higher temperature and pH favored the formation of NH3, which would subsequently volatilize. High frequency of turning could also hastened the volatilization and increase TKN losses (Huang et al., 2006).The increase in the TKN content at the later period of composting was mainly due to the concentration effect. However, TKN also be increased by the activities of nitrogen-fixing bacteria as reported by Nakasaki et al. (2005).
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Time (Days) Fig. 5. Changes of C/N ratio (a), germination index (GI) (b) and E4/E6 (c) in composting piles with different turning frequency. Pile 1 – weekly, Pile 2 – twice a week and Pile 3 – daily turning and were inoculated with fungal consortium; whereas Pile 4 without fungal inoculum and turned weekly. Results are the mean of three replicates and bars indicate standard deviation.
Please cite this article in press as: Awasthi, M.K., et al. Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour. Technol. (2014), http://dx.doi.org/10.1016/j.biortech.2014.01.048
7
M.K. Awasthi et al. / Bioresource Technology xxx (2014) xxx–xxx Table 2 Physicochemical characteristics of compost (dry weight basis). Parameters
Pile 1
Pile 2
Pile 3
Pile 4
FAI (2007)
TMECC (2002), CCME (2005)
Moisture content (%) pH Electrical conductivity (mS cm1) Total organic carbon (%) Total organic matter (%) Total phosphorus (%) TKN (%) C:N ratio Sodium (%) Potassium (%) Copper (mg/kg) Cadmium (mg/kg) Zinc (mg/kg) Nickel (mg/kg) Lead (mg/kg) Chromium (mg/kg)
37 ± 0.7 7.95 ± 0.02 3.48 ± 0.02 25.35 ± 1.34 24.38 ± 1.23 0.82 ± 0.01 1.48 ± 0.14 17.12 ± 1.21 2.4 ± 0.33 1.4 ± 0.25 87.16 ± 2.95 1.5 ± 0.34 132.0 ± 2.14 21.4 ± 0.31 19.2 ± 0.27 27.8 ± 1.78
39 ± 0.3 7.89 ± 0.04 3.35 ± 0.04 26.72 ± 0.70 25.46 ± 0.41 0.76 ± 0.04 1.52 ± 0.06 17.52 ± 2.42 2.7 ± 0.21 1.3 ± 0.43 72.8 ± 3.55 NA 146.0 ± 3.21 14.6 ± 0.06 22.1 ± 0.48 23.1 ± 2.25
35 ± 0.4 7.65 ± 0.02 3.46 ± 0.03 28.56 ± 1.15 24.63 ± 1.95 0.87 ± 0.02 1.46 ± 0.10 19.47 ± 1.07 3.1 ± 0.45 1.6 ± 0.06 104.6 ± 1.29 0.9 ± 0.12 81.27 ± 2.43 18.2 ± 0.42 13.7 ± 0.21 11.3 ± 0.85
43 ± 0.7 6.72 ± 0.05 2.42 ± 0.02 33.78 ± 1.53 32.49 ± 2.70 0.61 ± 0.02 1.29 ± 0.08 26.18 ± 1.16 1.8 ± 0.18 1.1 ± 0.03 78.3 ± 2.74 1.4 ± 0.05 127.0 ± 3.62 27.4 ± 0.16 19.6 ± 0.36 25.3 ± 1.42
35–55 6.5–8.5 2–6 P16 >30 0.4–1.1 1.0–3.0
