Compost Produced by Solid State Bioconversion of Biosolids: A ...

Communications in Soil Science and Plant Analysis, 36: 1435–1447, 2005 Copyright # Taylor & Francis, Inc. ISSN 0010-3624 print/1532-2416 online DOI: 10.1081/CSS-200058487

Compost Produced by Solid State Bioconversion of Biosolids: A Potential Resource for Plant Growth and Environmental Friendly Disposal Abul Hossain Molla Department of Chemical and Environmental Engineering, Universiti Putra Malaysia, Selangor DE, Malaysia and Department of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh

Ahmadun Fakhru’l-Razi Department of Chemical and Environmental Engineering, Universiti Putra Malaysia, 43400 UPM, Selangor DE, Malaysia

Mohamed Musa Hanafi Department of Land Management, Universiti Putra Malaysia, 43400 UPM, Selangor DE, Malaysia

Md. Zahangir Alam Department of Chemical and Environmental Engineering, Universiti Putra Malaysia, 43400 UPM, Selangor DE, Malaysia and Department of Biotechnology Engineering, International Islamic University Malaysia, Jalan Gombak, 53100 Kuala Lumpur, Malaysia

Abstract: Compost produced by solid-state bioconversion of the Indah Water Konsortium domestic wastewater treatment plant’s sludge/biosolids significantly influenced the plant growth and development of corn (Zea mays). The solid-state bioconversion refers to the control growth of microorganisms, generally on the surface of Received 14 July 2003, Accepted 3 November 2004 Address correspondence to Abul Hossain Molla, Biochemical Engineering Lab, Department of Chemical and Environmental Engineering, Faculty of Engineering, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor DE, Malaysia. Fax: þ6 03 8656 7120; E-mail: [email protected] 1435

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water-insoluble substances for biodegradation of biopolymers and bioremediation of chemical compounds. Compost of biosolids with rice straw significantly increased plant height, shoot, and root dry weight. Moreover, it promoted 100.51% dry-matter production compared to control. But the dry matter was recorded 46.80% only in urea (þN) application. The highest vegetative growth and delayed drying of basal leaves were attained using 1/2 of compost with 1/2 amount of urea, of the optimal dose of nitrogen (N) requirement for corn production. The recorded heavy metals concentration in plant tissues was quite low. Most of the heavy metals in composts of biosolids were on average 30 times lower compared to the standard limit of municipal solid waste in the United States. The compost of biosolids with rice straw provided superior performance in corn growth compared to the compost of biosolids with sawdust. Both evaluated composts produced by solid-state bioconversion process were nonhazardous and did not contribute any detrimental effect or symptoms on corn growth and development. Simultaneously, it would behave as a potential sustainable environmentally friendly route of biosolids management and disposal as value added organic fertilizer for agronomic/horticultural use. Keywords: Biosolids, compost, disposal, fungi, heavy metals, plant growth, solid-state bioconversion

INTRODUCTION Sewage sludge is a widespread waste generated all over the world and can cause severe environmental hazards. The proper, nonhazardous, environmentally friendly management and disposal of sludge is a great concern. There is need for relevant research in conventional as well as advanced techniques such as membrane filtration, flocculation, adsorption, and chemical treatment of wastewater/wastewater sludge. However, all these techniques or their by-products release contaminants to the environment (Eljarrat, Caixach, and Rivera 2001; Lorain et al. 2001; Oudeh, Khan, and Scullion 2002). Therefore, researchers have focused their attention on nonhazardous, environmentally friendly, and sustainable techniques such as bioremediation (i.e., biological-based treatment) for waste/contaminant remediation (Cameron, Timofeevski, and Aust 2000). Gradually, bioremediation/bioconversion is emerging as a promising, environmental friendly (Desai and Banat 1997) process to degrade environmental contaminant (Colwell 1994). It results in permanent organic waste elimination, reduces long-term liability, and has greater public acceptance (Boopathy 2000) compared to physical and chemical processes (Lee and Mat 1998). Therefore, biological treatment of wastewater and wastewater sludge is being studied as a sustainable, nonhazardous and environmentally friendly technique for ultimate safe disposal. Solid-state bioconversion (SSB) is a novel biological technique effectively used for biodegradation of plant polymers and bioremediation of man-made chemicals (Doelle, Mitchell, and Rolz 1992). Also it has been widely practiced in the production of enzymes, protein enrichment, and

Friendly Disposal of Biosolids as Compost by SSB

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metabolites (Mitchell and Lonsane 1992; Poonam 1994). SSB has been practiced in composting of agricultural wastes for mushroom cultivation and production of organic acids. Furthermore, the process offers faster degradation of substrates due to more or less homogenous distribution of excreted enzymes by filamentous fungi (Raimbault 1998). Considerable interest has been generated on SSB as nonhazardous disposal of wastewater sludge. SSB is a form of composting, an ancient biologically based technique of waste decomposition, but it is an environmentally sound and sustainable method of waste management (Georgacakis et al. 1996). It is also suitable for maintaining a healthy soil environment for plant growth (Mathur et al. 1993). Recently, researchers have turned their attention toward expediting the process of composting by utilizing the knowledge and techniques of solid-state bioconversion. Bioconversion or the biological treatment of wastewater is not well cited in literature. Recently, encouraging findings were reported on detoxification of wastewater from an olive mill by Penicillium strains (Robles et al. 2000) and bioconversion of domestic wastewater by Phanerochaete chrysosporium and Aspergillus spp (Alam et al. 2001; Fakhru’l-Razi et al. 2002). However, in previous studies on isolation and screening of proper microbes compatibility of mixed cultures, optimization, and evaluation of the process of SSB of biosolids into compost, significant fungal growth (i.e., dry biomass, soluble protein and total organic carbon) were observed (Molla 2002; Molla et al. 2001, 2002). But the process will not be accepted unless the end product has some potential for economic use. The economic use of the end product is an important factor, for if it does not have sufficient value, it will be treated as a waste. Therefore, the present study was designed to examine the role of the end product (compost) of SSB of biosolids in plant growth and development with emphasis on heavy metals uptake in plant systems.

MATERIALS AND METHODS An experiment was conducted in perforated black polyethylene planting bags (11.5 cm diameter 14.5 cm height, containing 2.67 kg dry soils) in a glasshouse of Universiti Putra Malaysia (UPM) in 2002. SSB products from Indah Water Konsortium (IWK) biosolids “compost” were evaluated for effects on corn (Zea mays) growth and development using Bungor soil (Typic Paleudult, sandy clayey kaolinite). The soils were collected from the surface of a nonagricultural area adjacent to a corn field. Total N (0.47%) and pH (5.2) of the soil were determined prior to use. Two composts, (1) compost of biosolids with sawdust (CSD) and (2) compost of biosolids with rice straw (CRS) were used after 72 hours curing at room temperature. Both composts were produced by using the novel process of solid-state bioconversion of biosolids with selected compatible mixed filamentous fungal cultures (Molla et al. 2001) of Trichoderma harzianum with

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Phanerochaete chrysosporium 2094 and by optimizing growth factors such as C/N ratio, initial pH, and suitable carbon-containing cosubstrate and bulking material. The bioconversion process was operated for 60 days after fungal inoculation of sterile (by prior autoclaving at 1218C) substrates. There were six treatments: (1) 2N (control, i.e., no urea), (2) þ N (urea), (3) CSD (compost of biosolids þ sawdust), (4) CRS (compost of biosolids þ rice straw), (5) 1/2 CSD þ 1/2N, and (6) 1/2 CRS þ 1/2 N. The dose 150 – 90– 90 kg/ha (1.21 – 0.93– 0.94 g/kg) of NPK fertilizers is standard for corn cultivation in Bungor soil. The plants were grown 45 days after sowing (DAS). During this period of experiment, the average maximum (34.68C) and minimum (21.88C) temperatures, relative humidity (76.7%), and sunshine (8.0 hours) were recorded in the glasshouse. Planting-Bag Preparation, Fertilizer, and Treatments Application In each planting bag, 2.67 kg soils (dried soils) were placed after 48 hours drying (in glasshouse) and sieving (2.5 mm mesh size). Respective treatments and required fertilizers were added to soils and mixed thoroughly before placing in planting bags. Triple superphosphate and muriate of potash (8.45 and 3.38 g per planting bag, respectively) were used in all treatments. For the N treatment, 6.11 g urea was applied in solution form to each planting bag (for 2.67 kg dried soils) in three equal installments (before sowing seeds, and 15 and 30 days after sowing [DAS]), 316.5 g CSD (2.87% N, 66.68% H2O), and 293.45 g CRS (3.10% N, 69.87% H2O) were applied to each planting bag as treatments of CSD and CRS, respectively. These amounts of composts provided the N equivalent to 6.11 g of urea. In treatments of 50% composts with 50% urea, the total amount of compost was applied at bag preparation, and the amount of urea was applied in three installments similar to þN treatment. Seed Sowing and Crop Management Equal-sized corn seeds were moistened overnight with distilled water. The following day, five seeds were sown in each planting bag. At 5 DAS, seedlings were thinned, leaving two equal-size seedlings in each planting bag, which were allowed to grow for 45 days. The planting bags were watered every day to maintain moisture level at field capacity. No disease or insect infestation was noticed. Parameters Considered for Evaluation Plant height, leaf number, shoot and root dry weight, SPAD value (i.e., leaf chlorophyll) (dimensionless indirect measurement, using SPAD meter, Minolta SPAD-502 Japan) were recorded. Uptake of major and trace elements were measured to further evaluate the effects of composts on corn


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growth. Plant samples were oven-dried at 708C for 3 days for dry weight measurement and chemical analysis. Chemical Analysis of Plant Materials Oven-dried ground samples (,1.5 mm) were used for chemical analysis. Total N was analyzed using the Micro-Kjeldahl method (Bremner 1960), and all others elements were analyzed using dry-ashing method (SIRIM 1980). Nitrogen and phosphorus were analyzed by using an autoanalyzer (XYZ Auto Sampler, ASX-500 series; LACHAT instrument), and other elements were analyzed using PERKIN-ELMER 5100 PC Atomic Absorption Spectrophotometer. Experimental Design and Statistical Analysis The experiment was conducted in a randomized completely block (RCB) design with five replications. Analysis of variance and comparison of means were conducted separately with the statistical package MSTAT-C (MSU 1989). The data were tested by Duncan’s Multiple Range Test (DMRT) with a statistical significance level of P 0.05 level. RESULTS AND DISCUSSION Biometric Measurements Corn growth at 45 DAS was influenced by biosolids composts. Between the two composts, the CRS influenced a majority of biometric measurements. The highest shoot and root dry matter (DM) were achieved in CRS (Table 1). Significantly higher (159.8 cm) plant height was also observed using CRS compared to CSD. Two other treatments, (1/2 CRS þ 1/2 N) and (1/2 CSD þ 1/2 N) had comparable plant heights. CSD did not perform as well, but when supplemented with 1/2 N (urea) a pronounced increased plant growth (i.e., plant height 167.25 cm) was noticed relative to CSD, 2N and þN treatments (Table 1 and Figure 1). Similarly the highest SPAD value (40.35) was also recorded in treatment 1/2 CSD þ 1/2 N (Table 1). The SPAD value represents the leaf greenness. Amir et al. (2001) found positive correlation (r2 ¼ 0.9046 ) of SPAD reading with total chlorophyll content in studies with oil palm. When the optimal dose of N for corn plantation was supplied by 50% N from compost and another 50% N from urea (i.e., the treatments 1/2 CRS þ 1/2 N and 1/2 CSD þ 1/2 N), the corn produced dark green leaves (Figure 1A). Comparatively superior results were also found in sole treatment of CSD and CRS compared to the treatment þN (urea) (Figure 1B). The sole CRS treatment provided significantly higher results (statistically) in all parameters

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Table 1. Biometric measurements of corn (at 45 DAS) under two different composts of wastewater sludge by SSB process using mixed fungal inocula T. harzianum with P. chrysosporium 2094a

Treatments 2N (control) þ N (urea) CSD 1/2 CSD & 1/2 N CRS 1/2 CRS & 1/2 N

Plant height Shoot DM (cm) (g bag21) 120.62 b 132.5 b 124.0 b 167.25 a 159.77 a 161.25 a

25.29 e 39.78 c 32.61 d 46.09 b 51.14a 47.54 b

Root DM (g bag21) 7.62 8.68 11.83 8.49 15.05 10.84

c c b c a b

SPAD value Promotion of (greenness) DM (%) 26.95 35.85 28.27 40.35 31.62 38.05

d b cd a b a

0.00 46.80 34.63 65.34 100.51 76.86

a DAS: days after sowing; SSB: solid-state bioconversion; CRS: compost of biosolids with rice straw; CSD: compost of biosolids with sawdust; and DM: dry matter. Common letters in column are not significant at P 0.05 by DMRT.

except SPAD (Table 1). Statistically higher shoot dry weight and SPAD values were achieved in þN treatment compared to CSD, but the plant height was insignificant. Increased root dry weight was observed in CSD versus þN treatment. The highest (100.51%) dry-matter increase relative to the control was achieved with the CRS treatment, followed by 76.86% and 65.34% for 1/2 CRS þ 1/2 N and 1/2 CSD þ 1/2 N treatments, respectively (Table 1). Total number of leaves was not changed in different treatments. But interesting results were noticed in the percent of dead leaves (Figure 2). Basal leaves remained green in þN and combined treatments (i.e., N plus CRS or CSD) compared to others. The highest percentages of dead leaves were produced in control, CSD, and CRS treatments. The lowest number (10%) of percent of dead leaves was achieved in treatment 1/2 CRS þ 1/2 N, but this was not statistically different from þN and 1/2 CSD þ 1/2 N treatments. The control treatment produced the highest percent of dead leaves (30%) compared to 15% in the þN (urea) treatment. The probable explanation of the obtained results might be that the composts plus urea (N) treatments act to slowly release nutrients (i.e., it maintains the continuous flow of nutrients). Nutrient and Heavy Metals Concentrations Nutrient uptake was not clearly related to applied treatments (Table 2). In general, however, the plants with the þN treatment contained comparatively higher concentrations of major elements, followed by the 1/2 CRS þ 1/2 N and 1/2 CSD þ 1/2 N treatments. Nitrogen influenced the uptake of other


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Figure 1. Vegetative growth and development of corn (at 45 DAS) in planting bag using N fertilizer (urea) vs. composts of biosolids produced by SSB process.

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Figure 2. Leaf characters of corn (at 45 DAS) in biosolids composts (CSD: biosolids with sawdust; and CRS: biosolids with rice straw) of IWK domestic wastewater treatment plant by SSB process (same capital and small letters are not statistically significant at P 0.05 by DMRT).

Table 2. Nutrient concentrations in dried corn plant (leaves and stem, at 45 DAS) grown in planting bag using composts of domestic wastewater sludge (Biosolids)a Nutrients

2N (control)

þN (urea)

N(%) 0.877 c 4.160 a P(%) 0.270 a 0.193 b K(%) 5.157 a 5.470 a Ca(%) 0.267 b 0.670 a Mg(%) 0.113 c 0.230 a Pb(mg kg21) 13.56 a 5.89 b Ni(mg kg21) 8.55 a 8.00 a Cu(mg kg21) 4.78 a 6.00 a Mn(mg kg21) 48.00 c 58.11 abc Cd(mg kg21) 1.14 a 0.95 a Zn(mg kg21) 41.33c 43.89 be Cr(mg kg21) 6.44 ab 5.33 b Na(mg kg21) 70.33 c 79.45 c Fe(mg kg21) 322.22 cd 455.56 ab a

CSD

1/2 CSD & 1/2 N

1.264 c 0.217 ab 4.880 a 0.143 c 0.113c 9.89 ab 9.22 a 6.55 a 50.67 bc 1.24 a 83.44 a 5.89 b 284.89 a 494.45 a

2.860 b 0.209 ab 5.073 a 0.580 a 0.227 ab 9.89 ab 7.78 a 4.33 a 67.00 a 1.24 a 61.56 b 9.34 a 77.56 c 366.67 bc

CRS

1/2 CRS & 1/2 N

1.477 c 3.126 b 0.238 ab 0.201 b 5.067 a 5.980 a 0.287 b 0.607 a 0.103d 0.223 b 8.89b 8.00 b 6.11 a 10.55 a 4.33 a 6.22 a 67.89 a 64.11 ab 0.97 a 0.96 a 59.22 bc 85.66 a 5.44 b 7.67 ab 64.67 c 164.56 b 227.78 d 516.66 a

DAS: days after sowing; CSD: compost of biosolids with sawdust; and CRS: compost of biosolids with rice straw produced by SSB (solid-state bioconversion) using two fungal mixed inocula, T. harzianum with P. chrysosporium 2094. Common letters in row are not significant at P 0.05 by DMRT.


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major nutrients. The nutrient concentrations of plants for CRS treatment were close to those of the treatment of 1/2 CRS þ 1/2 N and was higher than the CSD treatment except for some heavy metals. For the case of N uptake, the obtained results show that the highest uptake of N is found in þN treated plant tissues followed by 1/2 CRS þ 1/2 N and 1/2 CSD þ 1/2 N treatments. The lowest is in 2N treated plants. Generally the nutrients uptake mostly depends on their presence of available forms in soil solution. In the present experiment, the applied urea might play active roles of N’s availability. Generally due to slow-nutrients-release characteristics of compost, the rate of availability of N in soil solution might be poor in compost-treated cases within the experimental period (45 days). Therefore, this might be the probable reason of poor uptake of N in most of the compost-treated plants compared to þN treatment. The nutrient uptakes were not so significantly higher in compost plus N supplemented treatments in comparison to þN treated plants. But the biometric measurements (Table 1) and general appearance of the plants (Figure 1) in composts plus N supplemented treatments were clearly shown in the impressive plant growth than the others. It clearly implies that the composts conserved some favorable environments in the soil-plant system through maintaining better physical properties, aggregation and aeration ability (Kostov et al. 1996), increased total porosity, and saturated hydraulic conductivity of soils (Aggelides and Londra 2000), which ensure better water and nutrients regime at the period of plant growth for improved physiological activities such as higher dry-matter production through enhanced harvest of atmospheric CO2. The obtained results of chemical analysis of heavy metals in corn tissues in compost treatments were significantly lower than the levels that are recognized for use by several countries (Tables 2 and 3). Even the amounts of heavy metals present in composts (CRS and CSD) are lower than the standard limits of several countries, except chromium (Cr) and zinc (Zn) in some cases (Table 3). In the present study, the uptake of lead (Pb), cadmium (Cd), Cr, nickel (Ni), copper (Cu), and Zn by corn biomass were 20, 30, 120, 42, 225, and 30 times lower, respectively, compared to the levels, which are allowed by the United States in MSW compost. The Indah Water Konsortium wastewater sludge is only the urban sewage sludge that is free from industrial wastewater. Therefore, it contains comparatively lower amounts of heavy metals. Higher uptake of Pb, Cr, and Zn was observed in compost and compost plus N treated corn plants. With regard to heavy metals, Ishak et al. (1999) reported that significantly higher amounts of Cd and Zn were released in soil after direct application of the IWK wastewater sludge for corn cultivation. Approximately a two-fold increase in Zn concentration was observed in plants added with composts than the control and þN treatments. Also comparatively higher amounts of Cr, Pb, and manganese (Mn) were absorbed by plants in composts and composts plus N supplemented plants and might be the reasons for higher amounts of these metals originally present in composts.

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Table 3. Comparison of composition of composts from biosolids with standard limits of heavy metals in municipal solid waste (MSW) compost (de Bertoldi et al. 1990; He et al., 1995; Wei et al., 2000) and typical value in soil (Adriano et al. 1980) Compostb Parametersa

CRS

Moisture(%) pH C/N ratio EC(dS m21) BD(kg m23) N(%) P(%) K(%) Ca(%) Mg(%) Pb(mg kg21) Ni(mg kg21) Cd(mg kg21) Cr(mg kg21) Cu(mg kg21) Mn (mg kg21) Zn(mg kg21) Na(mg kg21) Fe(mg kg21)

52.34 5.27 12.14 1.49 1099.22 3.10 0.84 3.13 0.10 0.21 36.27 10.53 2.24 508.33 75.53 165.67

CSD

Standard limit of MSW compost USA

EC

Australia

China

Typical value in soil

53.05 — — 25 – 35 25 – 35 — 5.15 — — 7.0– 8.5 6.5– 8.5 5.0 15.98 — — — — 11 0.35 — — — — — 953.26 — — — — 1300 2.87 — 0.6 05 – 1.5 0.5 0.4 0.62 — 0.5 0.4– 0.8 0.3 0.05 – 0.2 0.25 — 0.3 0.3– 1.0 1.0 0.04 – 3.0 0.05 — — — — 0.7 – 50 0.05 — — — — 0.06 – 6.0 33.73 300 750 200– 900 100 2 – 100 8.73 420 50 30 – 200 — — 1.99 39 5 1–6 3 0.01 – 7.0 450.0 1200 150 50 – 300 300 5 – 3000 63.53 1500 300 1000 — 2 – 100 34.93 — — 500– 1200 — 100– 4000

1200.0 1130.0 436.50 1364.5 9200 8066

2800 100 — — — —

300– 1500 — —

— — —

10 – 300 400– 30000 —

a EC: electrical conductivity, BD: bulk density (all nutrients were analyzed as dry basis). b CRS: compost of biosolids with rice straw; CSD: compost of biosolids with sawdust. Both prepared with mixed fungal cultures T. harzianum and P. chrysosporium 2094 inoculation in solid-state bioconversion process.

CONCLUSIONS Generally, compost possesses the potential physical properties, aggregation, and aeration ability that ensure adequate water and nutrients regime at the period of plant growth. Therefore, the compost produced from IWK biosolids enhanced superior crop growth compared to conventional fertilizer while supplemented with urea. Plant height was greatest in the compost plus N (urea) treatments than in those receiving only compost or urea. Undoubtedly, composts (CRS and CSD) could reduce the cost for N (urea) at optimal dose for corn cultivation. In the present study, around 65% to 100% promotion of dry-matter production in corn was attained by compost as well as compost plus 50% N (urea) application compared to -N (control), while urea only increased dry-matter production about 46.80% in 45 days.


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The compost CRS was superior for plant growth and development as compared to CSD due to its higher nutrient content. Though heavy metals are well-known problems of sewage sludge/biosolids, but the compost (CRS and CSD) produced from the IWK biosolids by SSB was free from that risk as compared to standard limits set by the United States, the European Community, Australia, and China. Therefore, the compost produced from biosolids can be used in agronomic and horticultural practices. The process could turn the direction of neglected nuisance wastes to a resource and could open an environmentally friendly, nonhazardous, sustainable route of ultimate disposal of wastewater sludge.

ACKNOWLEDGMENTS The authors are grateful and express their sincere thanks to the Indah Water Konsortium Sdn. Bhd., Malaysia and Universiti Putra Malaysia for extending their cooperation and assistance for conducting this study by providing financial support and facilities, respectively.

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