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Ecological Engineering 35 (2009) 1559–1563

Contents lists available at ScienceDirect

Ecological Engineering

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mpacts of monosodium glutamate industrial wastewater on plant growth andoil characteristics

atnam Singh a, P.D. Rekha b, A.B. Arun b, Chiu-Chung Young a,∗

Department of Soil and Environmental Sciences, College of Agriculture and Natural Resources, National Chung Hsing University,50, Kuo Kuang Rd., Taichung, 402, Taiwan, ROCYenepoya Research Centre, Yenepoya University, Deralakatte, Mangalore, India

r t i c l e i n f o

rticle history:eceived 18 December 2008eceived in revised form 21 May 2009ccepted 1 June 2009

eywords:onosodium glutamateastewater

lant nutritionitrogen

a b s t r a c t

Research into utilization of monosodium glutamate industrial wastewater (MSGW) as a plant nutrientsource was undertaken. The physico-chemical and microbiological characteristics of MSGW were analyzedin detail. Effect of MSGW on early growth of Chinese cabbage (Brassica rapa L. cv. Pekinensis) and maize(Zea mays L. cv. Bright Jean) was tested by the seed germination bioassay. Subsequently, in a greenhousepot experiment using the same plant species, effects of MSGW application rates on the plant biomassyield, nitrogen content and soil properties were analyzed. The MSGW was characterized by high levels ofN (56.7 g l−1), organic C (344.6 g l−1), total solids (600 g l−1) and other minerals. At MSGW concentrationsbelow 1%, germination indices for both the plant species were significantly (p < 0.01) higher than thecontrol. Further, the greenhouse study results indicated significant increase in the plant biomass yieldat MSGW application rates of 5000 and 7500 l ha−1. As the MSGW dose increased, the biomass yielddecreased, decreasing the N-use efficiency. Maize showed significantly higher wastewater N-use efficiencycompared to the Chinese cabbage. Although the total culturable bacterial and fungal counts in the raw

MSGW were low, addition of MSGW to the soil increased the soil microbial activities and soil respiration.Soil organic C was also increased by the addition of MSGW, due to the presence of significant amounts oforganic C in the wastewater. This preliminary study demonstrates that by proper management of the pHand optimization of application rate, MSGW can be utilized as a nutrient source for plant growth. Furtherlong-term field studies to evaluate the environmental impact of MSGW usage in agriculture are beingdesigned to reduce the environmental risks associated with the reuse of this underutilized wastewater inthe agriculture.

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. Introduction

Monosodium glutamate or MSG was developed in Japan and hasound extensive use as flavor enhancer in food products through-ut South East Asia as well as in other countries. MSG was originallybtained by extraction from beet sugar and is presently producedy microbial fermentation of cassava, wheat, potato starch, etc. Inhis method, bacteria (strains of Micrococcus glutamicus) havinghe ability to excrete glutamic acid are grown aerobically in a liq-id nutrient medium containing a carbon source (cassava, wheat,

otato starch), a nitrogen source (ammonium ions or urea), mineral

ons and growth factors. The glutamic acid is separated from theermentation broth by filtration, concentration, acidification, andrystallization, followed by conversion to its monosodium salt. The

∗ Corresponding author. Tel.: +886 4 22861495; fax: +886 4 22861495.E-mail address: ccyoung@mail.nchu.edu.tw (C.-C. Young).

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925-8574/$ – see front matter. Crown Copyright © 2009 Published by Elsevier B.V. All rigoi:10.1016/j.ecoleng.2009.06.002

Crown Copyright © 2009 Published by Elsevier B.V. All rights reserved.

ntire process generates large amounts of wastewater effluents. Theonosodium glutamate industrial wastewater (MSGW) contains

igh concentration of organic matter, COD, ammonium, sulphatend low pH (Yang et al., 2005) and hence biological wastewaterreatments processes are not effective. Removal of nutrients andrganics from the wastewater using algae (Gronlund et al., 2004)r aquatic plants (Upadhyay et al., 2007; Zimmels et al., 2008) areommon bio-filtration techniques, and are not suitable for MSGWue to the high solid content and extreme pH. Incidents of directisposal of MSGW into water-ways causing severe environmen-al problems were also reported recently (Overland, 2008). A fewesearch studies have focused on partial treatments such as colornd COD removal using different techniques (Yang et al., 2003; Jia

t al., 2007).

Ecotechnology emphasizes reutilization of waste by suitableodifications. Nutrients present in organic-rich wastewaters and

ludge are being reused as source of plant nutrition (Zurita et al.,009). Consideration for the possible reuse of MSGW relies on the

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igh levels of nutrients present in this wastewater. An earlier studyointed out that MSGW was phytotoxic as it inhibited the germina-ion of tomato, wheat and Chinese cabbage seeds (Liu et al., 2007).ut this conclusion was based on MSGW concentrations above 2%.n the contrary, Yang et al. (2005) described MSGW as a wastewa-

er containing no harmful components and used as a raw materialor single-cell protein production. Exploitation of this nutrient-richrganic wastewater in various applications needs to be studiedo reduce the treatment costs and environmental pollution. Weypothesized that due to the presence of rich nutrients, at certainoncentrations, the MSGW could show stimulatory effects on thelant growth. Hence, the objectives of this study were: (1) to char-cterize in detail the properties of MSGW, (2) to optimize the dose athich beneficial effects on plant growth can be observed by a seed

ermination assay and (3) to evaluate its effects on plant growthnd some soil properties by a greenhouse pot experiment.

. Materials and methods

.1. Wastewater collection and characterization

The MSGW samples were collected from Vedan Enterpriseorp., Taichung, Taiwan, in 25-l plastic containers and stored at◦C. Detailed characterization of the wastewater was carried outccording to the standard methods for the analyses of waternd wastewater (APHA, 1998). For the microbiological analyses,amples were separately collected in 20-ml sterile screw-cappedlass tubes. Immediately after collection the samples were seri-lly diluted and plated on nutrient agar and potato dextrose agaredium (pH adjusted to 4.0, 5.5 and 6.8) in the laboratory. Agar

lates were incubated at 30 ◦C and counts of the bacteria wereecorded after 48 h for a week.

.2. Effect of MSGW on the seed germination

The effect of different concentrations of MSGW on seed germi-ation was evaluated by a bioassay using Chinese cabbage (Brassicaapa L. cv. Pekinensis) and maize (Zea mays L. cv. Bright Jean) seeds.he seeds were placed over two sheets of filter paper (Whatman No.2) wetted with 3 ml of MSGW at different dilutions (10%, 5%, 2.5%,.0%, 0.1%, and 0% (v/v) with deionized water). Four repeats of eachreatment were made and incubated under dark at 30 ◦C for 96 h.ermination was scored for the seeds which showed a primary rootlongation of 5 mm and root lengths were recorded. Germinationndex was calculated as follows.

Germination index = RSG × RRE/100, where RSG is relative seedermination and RRE is relative root elongation calculated from theollowing equations;

RSG = No. of seeds germinated in TestNo. of seeds germinated in Control

× 100 and

RRE = Root length in TestRoot length in Control

× 100

.3. Effect of the MSGW on plant growth and soil propertiesnder greenhouse conditions

Chinese cabbage and maize, same as in the seed germina-ion bioassay, were used as test crops for the greenhouse study.

xperimental soil was collected from the upper layer (0–30 cm)f an agriculture farm at Donghai, Taichung County, in Taiwan.oil texture was silty clay (42% clay, 40% silt and 18% sand), pH.45, electrical conductivity 125.3 mS m−1, SOC 23.39 g kg−1and N.24 g kg−1.

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ring 35 (2009) 1559–1563

One kilogram each air-dried and sieved (4 mm) soil was filledn 20 plastic pots (bulk density 2.24 × 106 ha−1). The MSGW waspplied at 5, 7.5, 10 and 15 thousand l ha−1, which contributeespectively to the calculated 284, 425, 567 and 850 kg ha−1 of Noadings. The control treatments received only distilled water. Forach treatment, four repetitions were used. Prior to application, theH of the wastewater was adjusted to 6.5 ± 0.2 using 0.5 M Ca (OH)2.he measured quantities of MSGW were applied directly on the soilurface and mixed well. The pots were randomly arranged, wateredo 30% moisture level and kept 5 days for stabilization. On the sixthay, five seeds each of Chinese cabbage and maize were sown 0.5 cmelow the soil surface. After complete emergence (4–5 days), plantsere trimmed to two per pot. Throughout the experiment all theots were uniformly watered to maintain soil moisture at 30%. Dur-

ng the experimental period the day length ranged between 12 and3 h with average day and night temperatures of 27 ◦C and 20 ◦Cespectively.

.3.1. Plant biomass yield and nitrogen levelsPlants were harvested 35 days after sowing. For biomass mea-

urement, aboveground biomass was cut from each pot, washednd oven-dried at 70 ◦C to constant weight. Plant N was estimatedy Kjeldahl method. Wastewater-N use efficiency was calculatedccording to Anderson et al. (1997) by calculating the N from eachpplication rate of MSGW.

N-use efficiency

= Yeild in Wastewater treatment − Yield in ControlN applied

.3.2. Soil pH, nitrogen, organic C and dissolved organic CSoil samples were collected from the experimental pots within

ve minutes after the harvest for the analyses of some soil proper-ies. Soil pH was measured in 1:5 (soil:deionized water) soil extractssing a glass electrode. Kjeldahl digestion method (Kjeldahl, 1883)s described in Bremner (1996) was used for soil N estimation. Forhis, one gram of air-dried, finely ground soil sample was digested in0 ml of conc. H2SO4 and one gram metal catalyst (100 g K2SO4, 20 guSO4.5H2O, 2 g grey selenium powder) at 350–400 ◦C for 4 h. Theigested soil sample was cooled and distilled with 10 M NaOH solu-ion. The distillate was collected in 2% boric acid solution and theoncentration of N was determined by volumetric titration against.1 M H2SO4. Soil organic C (SOC) content was quantified by com-ustion at 430 ◦C (Ben-Dor and Banin, 1989). In brief, a weighedmount of oven-dried (105 ◦C, 24 h) soil sample was placed in aigh-form porcelain crucible and set in a muffle furnace for com-ustion at 430 ◦C for 4 h. Soil organic C was determined by theass difference. Dissolved organic carbon (DOC) was measured by

xtracting the soil with deionized water (1:10, w/v) for 6 h at roomemperature. The soil suspensions were filtered through 0.45 �

embrane filter fitted with a 5 ml syringe. The organic C in thextracts was quantified in a TOC analyzer (Analytik Jena, multi N/C100 S, Germany).

.3.3. Microbiological analyses of the soilSoil bacteria and fungi were enumerated by collecting soil sam-

les separately from each pot using 1-cm-diameter (>5 cm length)terile glass tubes. Known quantities of soil samples were dispensednto 10 ml sterile water, mixed and serially diluted. Diluted samples

ere spread onto nutrient agar (NA) media containing 100 mg l−1

yclohexamide (Sigma–Aldrich) as an antifungal agent and potatoextrose agar (PDA) containing 100 mg l−1 streptomycin sulphateSigma) as antibacterial agent, for enumerating culturable viableounts of bacteria and fungi, respectively. The sample inoculated

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gar plates were incubated at 30 ◦C. Colony-forming units (CFU)f bacteria and fungi were counted after 48 h for a week and arexpressed as log CFU g−1 soil d.w.

.4. Effect of wastewater on soil respiration

Effect of MSGW on soil respiration was evaluated in the labora-ory by monitoring the CO2 evolved from the MSGW added soil. Forhis, 100 g soil samples were incubated with MSGW at the doses asn the greenhouse study in two-liter mason jars at 30 ◦C. The controlreatment, similar to the greenhouse experiment, received distilledater. Soil moisture was maintained uniformly at 30% using dis-

illed water. The CO2 evolved was trapped in 20 ml of 0.1 M NaOH.lank treatment consisted of jars without any soil but with 20 mlf 0.1 M NaOH. At every 3-day intervals, the beakers containingaOH were removed from the jars, precipitated with 0.5 M BaCl2

olution and titrated against 0.1 M HCl using phenolphthalein indi-ator (Zibilske, 1994). Fresh NaOH was replaced and incubated untilo significant difference in the CO2 evolved for two consecutive

ntervals was observed.

.5. Statistical analyses

Mean and standard deviation values of the data were calcu-ated from 4 replicates. One-way analysis of variance (ANOVA)

as carried out to evaluate the significant differences betweenhe treatments Tukey’s HSD post hoc test was used for all multi-le comparisons using software package STATISTICA (Stat Soft Inc.998). Differences were declared significant at p value <0.01 unlesspecified.

. Results

.1. Characteristics of the wastewater

MSGW was dark brown in color and highly turbid with high lev-ls of total solids, N, organic C and very low pH (Table 1). The heavyetal contents were moderately low and within the permissible

imits for land application (USEPA, 1989). The U.S. standards limithe heavy metal levels for agricultural application to 170 kg Zn ha−1,8 kg Ni ha−1, and 46 kg Cu ha−1. Considering these qualities, thepplication rates for land use can be managed to avoid soil androundwater contamination.

Table 1Detailed characteristics of the monosodium glutamateindustrial wastewater.

Parameter Concentration

pH 3.6 ± 0.6Electrical conductivity (�S cm−1) 63.8 ± 2.2Total solids % 60.7 ± 1.3Organic C (g l−1) 344.6 ± 1.8Total-N (g l−1) 56.7 ± 0.8Ammonium-N (g l−1) 39.8 ± 1.0Total P (g l−1) 2.1 ± 0.2Total K (g l−1) 32.8 ± 2.2Sulphate (g l−1) 21.3 ± 1.2Calcium (CaO) (g l−1) 17.3 ± 0.7Magnesium (g/l) 12.10 ± 0.1Manganese (Mn) (mg l−1) 31.8 ± 0.6Copper (mg l−1) 9.22 ± 0.8Zinc (mg l−1) 36.28 ± 2.12Nickel (mg l−1) 3.41 ± 0.5Lead (mg l−1) <8.07Arsenic (mg l−1) <0.40Total culturable Bacteria (CFU ml−1) 2.4 × 103

Total culturable fungi (CFU ml−1) 1.8 × 103

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ays L. cv. Bright Jean) seeds. The error bars represent standard deviation (n = 4)ermination index = RSG × RRE/100, where RSG is relative seed germination andRE is relative root elongation calculated from the following equation; RSG =No of seeds germinated in Test

No of seeds germinated in Control × 100 and RRE = Root length in TestRoot length in Control × 100.

.2. Effect of wastewater on seed germination

Germination index calculated from the seed bioassay respondedignificantly to the concentration of the MSGW (Fig. 1). In 0.1, 0.2nd 0.5% concentrations, both Chinese cabbage and maize showedignificant increase in the germination index compared to theontrol. At concentrations above 1% the toxic effect of wastewa-er was evidenced by significant decline in the germination indexp < 0.001).

.2.1. Effect of wastewater on plant biomass yield and soilroperties

In the greenhouse pot experiment, plant response to MSGWmendment showed interesting results (Table 2). Plants wereealthy and did not show any symptoms of toxicity except mildymptoms such as curling of Chinese cabbage leaf in MSGW-15reatment. Plant biomass yield was significantly affected by theose of MSGW with highest biomass being observed at MSGW-7.5reatment. At concentrations above 7500 l ha−1 the plant biomassecreased significantly and at 15,000 l ha−1 the Chinese cabbageiomass was not significantly different from the control. Maizehowed higher tolerance to the MSGW concentrations where sig-ificantly higher biomass was produced even at the highest dosef wastewater compared to the control. On the contrary, N accu-ulation in the shoots of both plants increased with increased

oncentration of the MSGW. The overall N-use efficiency was signif-cantly higher for maize compared to the Chinese cabbage (Table 2).or maize, the highest N-use efficiency was observed at MSGW-, while for Chinese cabbage no significant difference betweenSGW-5 and MSGW-7.5 treatments was observed.

Soil pH ranged between 6.38 and 6.42 without being affectedy MSGW amendment, which is mainly due to use of pH adjustedSGW. Nitrogen levels were higher in all the Chinese cabbage

rown soils except MSGW-15, compared to the maize grown soilsTable 3). Decreased soil N in MSGW-15 of Chinese cabbage pots

ay be due to the N loss by microbial volatilization in the absencef plant absorption. A linear increase in the soil-N with increasedpplication rate of MSGW was observed due to the decreasing N-use

fficiency in both the test crops grown soils.

The MSGW treatments showed higher SOC and DOC values com-ared to the control (Table 3). However, the soil DOC in MSGW-5aize pots was not significantly different from the control. The

otal viable counts of bacteria and fungi are presented in Fig. 2. The

1562 S. Singh et al. / Ecological Engineering 35 (2009) 1559–1563

Table 2Aboveground biomass yield, plant N content and N-use efficiency of Chinese cabbage (Brassica rapa L. cv. Pekinensis) and maize (Zea mays L. cv. Bright Jean) plants grown inthe wastewater treated soils under greenhouse condition. Values are mean ± standard deviation. Data following same comment letter (a–e) in a column are not significantlydifferent (p < 0.01) in one-way ANOVA.

Treatments Chinese cabbage Maize

Biomass (g pot−1) Plant-N (g kg−1) fN-use Efficiency Biomass (g pot−1) Plant-N (g kg−1) *N-Use Efficiency

Control 0.51 ± 0.2c 5.25 ± 0.4e – 3.46 ± 0.2c 4.42 ± 0.1d –MSGW-5 1.64 ± 0.4ab 6.30 ± 0.2d 8.89 ± 2.8a 7.64 ± 0.5a 5.12 ± 0.3c 32.97 ± 4.0a

MSGW-7.5 2.23 ± 0.2a 7.50 ± 0.4c 9.09 ± 0.9a 8.38 ± 0.4a 6.48 ± 0.2b 25.94 ± 2.1b

MSGW-10 1.16 ± 0.1b 10.05 ± 0.7b 2.59 ± 0.4b 7.59 ± 0.5a 7.24 ± 0.4b 16.31 ± 1.5c

MSGW-15 0.76 ± 0.1c 15.86 ± 0.4a 0.67 ± 0.1 c 5.24 ± 0.2b 9.52 ± 0.5a 4.69 ± 1.0d

fN-Use efficiency was calculated as Yeild in Wastewater treatment-Yield in ControlN applied .

Table 3Soil properties after the harvest of Chinese cabbage (Brassica rapa L. cv. Pekinensis) and maize (Zea mays L. cv. Bright Jean) plants from the wastewater treated soil used in thegreenhouse pot experiment. Values are mean ± standard deviation. Data following same comment letter (a–d) in a column are not significantly different (p < 0.01) in one-wayANOVA.

Treatments Chinese cabbage grown soil Maize grown soil

Total-N (mg kg−1) SOC (g kg−1) DOC (mg kg−1) Total-N (mg kg−1) SOC (g kg−1) DOC (mg kg−1)

Control 172.5 ± 36.9c 22.4 ± 0.3b 31.2 ± 1.6d 137.5 ± 10.4d 22.5 ± 0.1b 96.9 ± 6.8c

MSGW-5 273.3 ± 37.2b 23.4 ± 0.5a 56.1 ± 4.4c c a c

MSGW-7.5 310.0 ± 23.8b 23.6 ± 0.2a 77.9 ± 3.5b

MSGW-10 387.5 ± 26.3a 23.4 ± 0.5a 76.3 ± 5.3b

MSGW-15 413.3 ± 40.1a 23.3 ± 0.3a 94.3 ± 3.9a

Fig. 2. Total culturable bacteria and fungi present in the experimental pot soilstreated with monosodium glutamate industrial wastewater under greenhouse con-ditions. The error bars represent standard deviation (n = 4).

Fig. 3. Impact of monosodium glutamate industrial wastewater on the soil respira-tion tested under laboratory conditions. The error bars represent standard deviation(n = 4).

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243.8 ± 17.5 23.7 ± 0.2 103.2 ± 4.2297.5 ± 27.5bc 23.8 ± 0.3 a 119.5 ± 5.6b

337.5 ± 32.3b 24.0 ± 0.1a 131.4 ± 3.1a

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icrobial counts were significantly higher in all the MSGW treatedoils compared to the control due to the availability of nitrogen andther nutrients. In MSGW-10 treatment (in both Chinese cabbagend maize pots) viable counts of bacteria were significantly highesulting in significant decrease in the fungal counts, probably byhe competition for niche and nutrients.

.3. Effect of the wastewater on soil respiration

Soil respiration is one of the parameters that responds positivelyo the organic amendments. Significant increase in the soil respira-ion was observed in the MSGW treatments compared to the controlFig. 3). After two weeks of incubation in all the MSGW treatments,oil respiration decreased significantly from the respective initialalues. However, in treatments, MSGW-10 and MSGW-15, the soilespiration was higher even after 21 days of incubation comparedo the control, MSGW-5 and MSGW-7.5 treatments.

. Discussion and conclusion

This study shows that MSGW, an organic-rich wastewaternhanced the plant growth under moderate rates of application.ence, it can be reused as a potential source for plant nutrients.resence of pathogens such as fecal coliforms and Salmonella, iscommon problem in the wastewaters from domestic, municipal

nd animal husbandry limiting direct utilization of such residuesCasteel et al., 2006). But overall microbial counts in the MSGWt the source of discharge were very low, without any knownathogens. However, in soils constantly exposed to pathogens, theisk of pathogen recolonization is higher. Hence, studying the pat-erns of pathogen recolonization may help to minimize associatedisks.

Seed germination assays indicated that toxicity was dose-ependent at concentrations above 1% as observed by Liu et al.

2007). Interestingly, our study provides results for the first time onhe beneficial effects of MSGW on plant growth. It should be notedhat industrial byproducts can be suitable either at very low appli-ation rates or with proper modifications and hence should not besed deliberately without studying its impacts for long term. With

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he greenhouse study we could delineate the overall impacts of theastewater on plant growth and some soil properties. We observed

ncreased plant yield by applying MSGW at concentrations of 5 and.5 thousand l ha−1 in line with the germination bioassay results.

N-use efficiency of plants serves as a key indicator for resourcetilization of high N products. Maize plants showed higher N-usefficiency compared to the Chinese cabbage as the biomass yieldf maize resulting from the wastewater application was signifi-antly higher than that of Chinese cabbage. Hence, we suggest thatSGW can serve as a vital N source for growing high biomass yield-

ng short-term crops such as maize. In a recent study, Lin et al.2008) showed that a similar N-rich wastewater could increase theitrogen mineralization of sesbania green manure. MSGW can pro-ide ca. 56.7 kg N for every 1000 l in both ammonium and nitrateorms. So, higher doses of application will supply very high amountsf N and cause serious losses in the applied N either by leachingr by volatilization. In addition, nitrate uptake and distribution inrops is decisive with respect to quality of crop products and envi-onmental concerns (Chen et al., 2004). Increased N availability atigher rates of MSGW enhanced the N accumulation in the tissuesf Chinese cabbage, reducing the overall biomass yield. Such obser-ations were also made by Chen et al. (2004) for Chinese cabbage,here increased nitrate supply increased plant nitrate accumula-

ion which resulted in significant decrease in the biomass yield.hinese cabbage and some related leafy vegetables are known toccumulate higher levels of N as nitrate in the biomass, affectinghe quality of these vegetables for human consumption (Zhong etl., 2002).

The major disadvantage of MSGW is the highly acidic pH thateeds suitable interventions to neutralize the effect. Most common

ow cost practice for neutralizing the pH is the lime addition. But,n our previous trial experiments (data not shown) direct use of

SGW without pH adjustments at application rate of 5000 l ha−1

id not cause significant decrease in the soil pH. This could be dueo the soil buffering activities and soil resilience. Alternatively, were researching into the use of highly alkaline paper-mill wastew-ter generated from the kraft process for neutralizing the MSGWH. The alkaline paper-mill wastewater has been used as an alter-ate to lime for reclamation of the acid mine land (Shipitalo andonta, 2008). Systemic application of the wastewater in split doseslong with irrigation can also be a reliable practice to dilute andeduce the immediate effect of pH and excess nitrogen. The goal ofcological engineering is to attain high environmental quality, highields, low consumption, good quality, high efficiency productionnd full utilization of wastes (Rose, 1999). Hence, a suitable strate-ic approach can be undertaken for the safe utilization of MSGWor plant nutrition.

In conclusion, the MSGW can be reused as an attractive sourcef N and organic matter to grow high biomass yielding short-uration crops. Our further studies on MSGW are emphasizing

evelopment technologies for cleaner practices according to theegional demands of agriculture and ecosystem to minimize publicealth and environmental risks. This will assist in making informedecisions on application rates and other disaster management prac-ices.

Z

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ring 35 (2009) 1559–1563 1563

cknowledgements

This research was supported by grants from the NSC, Taiwan,.O.C. and Council of Agriculture, Executive Yuan, Taiwan, R.O.C.ingh S. is grateful for Taiwan Government scholarship.

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