Bioremediation of tannery effluent by Cr- and salt

Environ Monit Assess (2018) 190:716 https://doi.org/10.1007/s10661-018-7098-0

Bioremediation of tannery effluent by Cr- and salt-tolerant bacterial strains Sobia Ashraf & Muhammad Naveed & Muhammad Afzal & Sana Ashraf & Khadeeja Rehman & Azhar Hussain & Zahir Ahmad Zahir

Received: 26 June 2018 / Accepted: 5 November 2018 # Springer Nature Switzerland AG 2018

Abstract Microorganisms have great potential to control environmental pollution, particularly industrial sources of water pollution. Currently, leather industry is regarded as the most polluting and suffering from negative impacts due to the pollution it adds to the environment. Chromium, one of the hazardous pollutants discharged from tanneries, is highly toxic and carcinogenic in nature. Effective treatment of tannery effluent is a dire need of the era as a part of environmental management. Among all the wastewater treatment technologies, bioremediation is the most effective and environment-friendly tool to manage the water pollution. The present study evaluated the potential of 11 previously isolated bacterial strains, tolerant to high concentrations of salts and Cr for the bioremediation of tannery effluent. Among all the tested strains, Enterobacter sp. HU38, Microbacterium arborescens HU33, and Pantoea stewartii ASI11 were found most effective in reducing biological oxygen demand (BOD), chemical oxygen demand (COD), total dissolved solids (TDS), total suspended solids (TSS), and chromium (Cr) 70, 63, 57, 87, and 54%, respectively, of tannery effluent and proliferated well under highly toxic conditions, at 9 days of incubation. The pollutant removal efficacy of these

bacterial strains can be improved by extending the incubation period or by increasing the amount of inoculum.

S. Ashraf : M. Naveed (*) : S. Ashraf : Z. A. Zahir Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad 38040, Pakistan e-mail: [email protected]

M. Afzal : K. Rehman National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

e-mail: [email protected]

Keywords Tanning industry . Remediation . Cr toxicity . Wastewater treatment . Industrial pollution

Introduction The tanning industry in Pakistan is not a new one; it has built up from its original form long ago. To fulfill the local demand for leather, locally available chemical reagents and tanning materials have long been used for curing, processing, and tanning hides. The main purpose of the tanning process is to convert animal skins into both physically and chemically stable and imputrescible product called leather. Animal hides have to go through four major groups of sub-processes to be stable and finished leather: beam-house operation, tanyard processes, re-tanning, and finishing processes (Cooman et al. 2003; Kanagaraj et al. 2015). The beam-house processes such as soaking, liming, and deliming results in the release of high amounts of sulfides, chlorides,

A. Hussain Department of Soil Science, University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur, Bahawalpur 63100, Pakistan

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lime, ammonium salts, sulfate, and protein in the effluent. Subsequently, the final liquid contains a high amount of biological oxygen demand (BOD) and chemical oxygen demand (COD) (Szpyrkowicz et al. 2001; Jahan et al. 2014; Vijayaraj et al. 2018). Unhairing and fleshing effluent is usually characterized by fatty fleshing matter in suspension (Stoop 2003; Thanikaivelan et al. 2004; Islam et al. 2014). The discharge of these highly oxygen demanding and colored wastewaters not only cause depletion of dissolved oxygen but also reduce the transparency of receiving water bodies thereby threating aquatic ecosystems (Bakshi and Panigrahi 2018). Chromium is one of the most hazardous pollutants found abundantly in the effluent discharged from tanneries (Agarwal and Pandey 2006; Gutterres et al. 2015). Its compounds can cause mutations leading to cancer and hinder enzymes and nucleic acid biosynthesis (Chaturvedi 2011). It can also cause severe diarrhea, ulcers, eye irritation, kidney failure, skin, and lung cancer (Malaviya and Singh 2011; Banerjee et al. 2019). There is huge pressure from the various pollution control bodies to regulate and minimize the amount of pollution produced by the tanning industries. The need to adopt alternatives to physico-chemical methods to cope with pollution problems has become a dire need to protect the industry and comply with environmental standards. Moreover, the use of physical and chemical methods for the bulk treatment of tannery effluent often fails to reduce the level to meet the environmental norms. Therefore, various physical or chemical or a combination of these methods are being used to treat tannery effluent (Schrank et al. 2005; Malaviya and Singh 2011; Jobby et al. 2018). These integrated treatment methods are efficient but not cost-effective in terms of energy and chemical consumption. Further, these methods produce a large quantity of sludge, which renders waste disposal problematic (Chu 2001; Sharma and Malaviya 2016). Currently, biological methods are emerging as a safe and cost-effective method for the treatment of industrial effluents. Therefore, bioremediation is recommended as a better alternative to other treatment methods for this purpose, as the chemical reagents are a source of environmental pollution while physical methods are costly. Previous studies have reported potential of certain species of bacteria like Arthrobacter, Bacillus, and Pseudomonas for the

Environ Monit Assess

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bioremediation of tannery effluent (Megharaj et al. 2003; Malachowski et al. 2004; Rajkumar et al. 2005; Khan et al. 2015). Bioremediation is a cost-effective, efficient, and ecofriendly strategy and therefore is highly suitable for the reduction of pollutants present in any effluent as microorganisms are gifted with enzyme systems for the oxidation of organic ingredients (Chaturvedi 1992; Divya et al. 2015; Igiri et al. 2018). Salinity status of tannery effluent causes hindrance towards its biological treatment. Therefore, the present study was aimed to evaluate the effectiveness of bacterial strains tolerant to high concentrations of salts and Cr to treat tannery effluent on lab scale.

Materials and methods Collection and analysis of tannery effluent The tannery effluent samples were collected at the inlet of the common effluent treatment plant (CETP) receiving wastewater generated during various stages of leather manufacturing process by two main drains from the Kasur Tanneries Complex in Kasur, Pakistan. The collected tannery effluent samples were brought to the laboratory and analyzed for various physico-chemical parameters using the standard methods (APHA 2005). Chromium concentration in tannery effluent samples was determined with the help of atomic absorption spectrophotometer (AAS).

Acquisition of bacterial strains Eleven Cr-tolerant bacterial strains also having plant growth-promoting activities were obtained from the Environmental Testing Services Laboratory, Environmental Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan (Table 1). These strains were previously isolated from rhizosphere and root and shoot interior of Prosopis juliflora, found growing in chromium-contaminated soils around the tanning industry area of Kasur (Khan et al. 2015).


(2018) 190:716

Preparation of inoculum A loopful of culture (all obtained strains) was inoculated individually in pre-sterilized a 100-mL Luria-Bertani (LB) broth (Afzal et al. 2012). The flasks were kept shaken in an orbital shaker (90 rpm) for 16 to 18 h at 37 °C. The culture broth was centrifuged at 10,000 rpm for 20 min. Cell suspension was prepared using sterile distilled water and adjusted to 0.7 OD using a UVvisible spectrophotometer. Then, 1% of the above suspension was used as inoculum for the bioremediation of tannery effluent. Experimentation Tannery effluent (100 mL) was placed in the 250-mL flasks in triplicate. These flasks were inoculated with all 11 strains and incubated at 37 °C with shaking at 90 rpm, for 9 days. Effluent sample without bacterial inoculation was considered as control. The effluent samples were collected and analyzed regularly, at 48-h intervals, for physico-chemical parameters and bacterial growth. Estimation of bacterial growth Growth and survival of inoculated bacteria in the tannery effluent in shake flasks was monitored by counting the number of colony-forming units (CFU) on alternate days. Effluent remediation Reduction in pollutant level of tannery effluent by each inoculum was determined by measuring biochemical oxygen demand (BOD), chemical oxygen demand (COD), total suspended solids (TSS), total dissolved solids (TDS), and Cr, at regular intervals. Statistical analysis of data The statistical calculations were performed following the standard methods (Steel et al. 1997). Principal component analysis (PCA) and factorial plane analysis (FPA) were performed using XL STAT software (XL STAT 2016). Significant statistical differences

Page 3 of 11 716

(p < 0.05) among tested bacterial strains to reduce pollutant level in the effluent were determined by one-way analysis of variance (ANOVA). The least significant difference (LSD) test was applied to compare the variations among the tested bacterial species to remediate effluent.

Results Analysis of effluent quality All the physico-chemical parameters such as EC, pH, BOD, COD, TDS, TSS, Cl, SO4, oil and grease, and Cr were found beyond the prescribed limits of the National Environmental Quality Standards (NEQS) for industrial discharge (NEQS 1999) as shown in Table 2. Bacterial growth The growth of all tested bacteria in tannery effluent at different time intervals is shown in Fig. 1. Microbacterium arborescens gave maximum growth (9.3 × 105 CFU/mL) at the ninth day of incubation followed by Enterobacter sp. with 8.5 × 105 CFU/mL and Pseudomonas stutzeri with the lowest growth (0.8 × 105 CFU/mL). Bioremediation of tannery effluent Highly significant variations were observed among the tested bacteria in reducing the BOD of effluent (Fig. 2). Microbacterium arborescens was the most active species in degrading organic pollutants, reducing BOD level of effluent up to 70% after 9 days of incubation. Other effective bacteria in removing BOD were P. stewartii and Enterobacter sp. which have a 10% reduction each after 1 day and 64 and 61% reduction, respectively, after 9 days of incubation. Figure 3 revealed the variation among effectiveness of bacterial strains for COD reduction from tannery effluent. The maximum reduction in COD was observed with M. arborescens where it was 38% on the third day of incubation and gradually increased to 63% at the ninth day of incubation while Bacillus aquimaris caused minimum reduction by 24% on the ninth day.

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– – – – – – – – – – – + + + + + + + + + + + – + – + – + – + – – – + + + + + + + + + + + + + + + + + + + + + +

+ + – + – + – – – – – – + + + + + – + – – –

Principal component analysis and factorial plane analysis of bacteria Principal component analysis (PCA) of all tested bacterial strains was performed on the basis of the studied parameters of tannery effluent (BOD, COD, TDS, TSS, and Cr removal and bacterial growth). The maximum PCA score (8.233) was indicated by M. arborescens. Pantoea stewartii was the second best strain in tannery effluent treatment on the basis of principal component score (6.354) followed by Enterobacter sp. with a 5.878 score (Table 3). Factorial plane analysis (FPA) also revealed the unique behavior of all tested strains. The projection of 11 tested bacterial strains on the F1/F2 plane for pollutant reduction and bacterial growth in tannery effluent indicated great variance (90%). On the basis of FP analysis, P. stewartii, M. arborescens, and Enterobacter sp. were determined to be the most effective strains with a maximum coordinate as shown in Fig. 7, encompassing the second main group (F1-positive, F2positive, and F2-negative values).

Discussion Adapted from Khan et al. 2015

SI RH SI SI SI SI SI SI SI SI RH Staphylococcus saprophyticus Pseudomonas aeruginosa Staphylococcus epidermidis Pantoea stewartii Ochrobactrum sp. Microbacterium arborescens Brevundimonas vesicularis Enterobacter sp. Bacillus aquimaris Pseudomonas sp. Pseudomonas stutzeri

KJ999602 KJ999614 KJ999613 KJ933399 KJ933400 KJ933403 KJ999609 KJ933404 KJ933405 KJ999612 KJ933402

+ + + + + + – + + + –

+ – – + + + – + + – –

– – + + – + + + – – –

+ + + + + + + + + + +

2 2000

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All the tested bacterial strains effectively reduced the TDS and TSS content of tannery effluent with an increase in incubation period (Figs. 4 and 5). Minimal TDS removal was observed in the control, i.e., where no inoculation was done. Microbacterium arborescens caused highest (56%) removal whereas Pseudomonas sp. caused least reduction (32%). Reduction in Cr level of tannery effluent due to the inoculation of different bacterial strains is given in Fig. 6. Maximum Cr removal was observed by M. arborescens (54%), followed by P. stewartii (52%) on the ninth day of incubation. The next effective treatment which was Enterobacter sp. caused a 50% reduction in Cr concentration at the same incubation period.

+ + – – – + – – – – –

1 3000 1000 500

3

NaCl tolerance (M) 1 M = 58 gL−1 Siderophore production IAA production P solubilization ACC deaminase Source of isolation NCBI accession number Bacterial strains

Table 1 Plant growth-promoting and Cr-tolerant bacterial strains isolated from shoot interior (SI) and rhizosphere (RH) of Prosopis juliflora


Cr tolerance (mg L−1)

3.5

716

Remediation of industrial effluents particularly those contaminated with toxic metals is crucial for environmental protection (Al-Musharafi 2016). Effluents discharged from tanneries are considered the most hazardous ones due to their chromium toxicity, high organic content, and saline nature (Dixit et al. 2015; Saxena et al. 2016). Efficient removal of toxic pollutants from tannery effluents prior to their discharge to the natural

(2018) 190:716


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Table 2 Physico-chemical characterization of tannery effluent Parameters

Values

NEQS

Parameters

Values

NEQS

Black

Gray

TS (mg L−1)

Color intensity (m )

61.2 ± 1.2

13,710 ± 608

NG

NG

TSS (mg L−1)

2854 ± 230

Odor

150

Foul smell

NG

TSeS (mg L−1)

8 ± 0.1

NG

Temperature (°C)

31 ± 0.3

40

SO4 (mg L−1)

1789 ± 113

NG

pH

8.0 ± 0.4

6–10

Cl (mg L−1)

3315 ± 249

1000

16.5 ± 1.4

NG

Total Cr (mg L−1)

134 ± 5.8

1.0

TDS (mg L )

10,560 ± 978

3500

Cr+6 (mg L−1)

0.48 ± 0.15

0.25

COD (mg L−1)

5634 ± 245

150

Cr+3 (mg L−1)

133 ± 1.4

0.75

BOD (mg L−1)

2910 ± 341

80

Oil and grease (mg L−1)

145 ± 5.6

10

Color appearance −1

EC (dS m−1) −1

NEQS the National Environmental Quality Standards of Pakistan for industrial effluent discharge, NG not given, TDS total dissolved solids, TS total solids, TSS total suspended solids, TSeS total settleable solids

waterways can be accomplished by using a sustainableaffordable and easy-to-apply green technology such as bioremediation (Fernandez et al. 2018; Vijayaraj et al. 2018). Bioremediation involves pollutant removal from the environment through biological resources including both plants and microorganisms (Jacob et al. 2018). In the present study, tannery effluent was remediated by using bacteria adaptive to high concentrations of salts. Bioremediation, an effective environmentfriendly approach, is preferred over other conventional treatment methods owing to biodegradation of organics under highly saline conditions (Sivaprakasam et al. 2008; Ojuederie and Babalola 2017). In the present study, 11 pre-isolated Cr- and salt-tolerant bacteria (Khan et al. 2015) were used to treat tannery effluent,

for their ability to survive under highly saline conditions. Among all the tested bacteria, the growth of S. saprophyticus, P. aeruginosa, M. arborescens, S. epidermidis, P. stewartii, and Enterobacter sp. increased with increasing incubation time. The effluent was found loaded with high BOD and COD concentrations. The high BOD in the tannery effluent indicates the presence of a large amount of biodegradable materials while the high COD indicates that nonbiodegradable materials are much higher than the biodegradable (organic) matter (Tudunwada et al. 2007; Adamu et al. 2015). In the present study, all the tested strains significantly caused a reduction in BOD and COD of tannery effluent, which might be due to the utilization of dissolved organic substances by bacterial cultures for

10

9 CFU/mL* 105

8 7 6 5 4 3 2 1 0 0

1

3

5

7

9

Incubation period (days) Pseudomonas aeruginosa

Staphylococcus epidermidis

Ochrobactrum sp.

Microbacterium arborescens

Brevundimonas vesicularis

Bacillus aquimaris

Pseudomonas sp.

Pseudomonas stutzeri

Control

Staphylococcus saprophyticus

Pantoea stewartii Enterobacter sp.

Fig. 1 Growth of different bacterial strains in tannery effluent. Growth is expressed as change in colony-forming units (CFU) vs. time

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80

1 day

3 day

5 day

7 day

(2018) 190:716

9 day

BOD reduction (%)

70 60 50 40

30 20

Bacterial strains


Pseudomonas sp.

Bacillus aquimaris

Enterobacter sp.



Ochrobactrum sp.

Pantoea stewartii


Pseudomonas aeruginosa


0

Control

10

Fig. 2 Reduction in biochemical oxygen demand (BOD) level of tannery effluent by different bacterial strains with respect to time. Error bars indicate standard deviation among three replicates

and Staphylococcus aureus due to their salt tolerance ability (Sivaprakasam et al. 2008). Gidhamaari et al. (2012) have also reported a decrease in BOD (75%) and COD (65%) of tannery effluent with the use of Pseudomonas sp. on the 15th day of incubation. In another study, Bacillus sp. degraded BOD of tannery effluent to 32 ± 3.16 mg L −1 with a

their growth (Smitha et al. 2012). Duangporn et al. (2005) reported a decrease in COD (7328 to 3371 mg L−1) and BOD (4967 to 1010 mg L−1) of tannery effluent after inoculation of Rhodopseudomonas blastica. More than 80% COD of tannery effluent was removed at 8% (w/v) salinity level by mixed consortia of Bacillus flexus, Exiguobacterium homiense, Pseudomonas aeruginosa,

1 day

3 day

5 day

7 day

9 day

70

COD reduction (%)

60 50 40 30 20

Pseudomonas sp.

Bacillus aquimaris

Enterobacter sp.


Bacterial strains



Ochrobactrum sp.

Pantoea stewartii




0

Control

10

Fig. 3 Reduction in chemical oxygen demand (COD) level of tannery effluent by different bacterial strains with respect to time. Error bars indicate standard deviation among three replicates


(2018) 190:716 1D

60 TDS reduction (%)

Page 7 of 11 716 3D

5D

7D

9D

50 40 30 20

Bacterial strains


Pseudomonas sp.

Bacillus aquimaris

Enterobacter sp.



Ochrobactrum sp.

Pantoea stewartii




0

Control

10

Fig. 4 Reduction in total dissolved solids (TDS) of tannery effluent by different bacterial strains with respect to time. Error bars indicate standard deviation among three replicates

percentage change at 95% and COD to 297 ± 3 mg L−1 with a percentage change at 88% (Noorjahan 2014). The reduction of various toxicants in tannery effluent during the bioremediation process by the use of indigenous bacteria was studied by Vijayaraj et al. (2018). Citrobacter freundii significantly reduced BOD and COD of tannery effluent and can be considered a

TSS reduction (%)

100

1D

prospective bioremediator for the safe disposal of tannery effluent to the environment. The amount of TDS (10,560 ± 978 mg L−1) and TSS (2854 ± 230 mg L−1) in the tannery effluent before microbial treatment was much higher than the permissible limits defined by NEQS of Pakistan for industrial discharge (NEQS 1999). High TDS concentration of

3D

5D

7D

9D

80

60 40


Pseudomonas sp.

Bacillus aquimaris

Enterobacter sp.


Bacterial strains


Ochrobactrum sp.

Pantoea stewartii




0

Control

20

Fig. 5 Reduction in total suspended solids (TSS) of tannery effluent by different bacterial strains with respect to time. Error bars indicate standard deviation among three replicates

716

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60

3 day

5 day

e

7 day

9 day

a

b

d

50 Cr reduction (%)

(2018) 190:716


c f

f

g

40

gh

hi

30

i j

20


Pseudomonas sp.

Bacillus aquimaris

Enterobacter sp.



Ochrobactrum sp.

Pantoea stewartii




0

Control

10

Bacterial strains

Fig. 6 Reduction in Cr level of tannery effluent by different bacterial strains with respect to time. Error bars indicate standard deviation among three replicates. Labels (a–j) indicate statistically

significant differences (p < 0.05) among bacterial strains for Cr removal from tannery effluent after 9 days at a 5% level of significance

tannery effluents indicates the presence of high amounts of minerals, metallic ions, acids, and alkalis in the dissolved form (Das et al. 2017). In the present study, bacterial inoculation significantly reduced TDS and TSS levels as well. Similar reductions in solids content of tannery effluent have been reported by others (ElBestawy et al. 2013; Noorjahan 2014; Abdallh et al. 2016). Bacteria degrade dissolved and suspended organic materials of the effluent for their growth and

development as evidenced by earlier studies (Shruthi et al. 2012; Gaikwad et al. 2014; Porwal et al. 2015; Oljira et al. 2018). Tannery effluent heavily loaded with chromium pose a great threat to the environment and associated life due to its inherent toxicity (Srinath et al. 2002; Sarker et al. 2013). Its microbial treatment has effectively removed chromium (more than 90%) through biosorption and biotransformation, without adding secondary pollution

Table 3 Factor coordinates of tested bacterial strains based on BOD, COD, TDS, TSS, Cr removal, and bacterial growth by using principal component analysis (PCA) Observation

F1

F2

F3

F4

F5

Control

− 11.141

− 3.159

− 1.556

0.161

− 0.220


2.040

0.113

0.525

0.980

− 0.591 0.532


2.982

0.473

− 0.703

0.094


− 0.502

0.082

1.146

− 1.712

− 1.353

Pantoea stewartii

6.354

− 0.939

− 0.526

− 0.144

0.012

Ochrobactrum sp.

− 1.965

− 0.507

1.820

0.485

0.007


8.233

− 1.320

− 1.074

− 0.331

0.385


− 2.344

0.359

1.192

0.441

− 0.048

Enterobacter sp.

5.878

0.373

− 0.602

0.705

− 0.675

Bacillus aquimaris

− 4.294

2.016

− 0.038

1.148

0.267

Pseudomonas sp.

− 4.516

3.121

− 1.598

− 0.987

0.139


− 0.724

− 0.611

1.413

− 0.840

1.545


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Page 9 of 11 716 Observations (axes F1 and F2: 90%)

10

F2 (6.96 %)

5

Pseudomonas sp. B. aquimaris S.epidermidis P. aeroginosa Enterobacter sp. B. vesicularis S. saprophyticus M. arborescens Ochrobactrum sp. P. stutzeri P. stewartii

0 -5 -10 -15

Control

-10

-5

0

5

10

F1 (83.04 %)

Fig. 7 Factorial plane (F1 × F2) for tested bacterial strains based on BOD, COD, TDS, TSS, Cr removal, and bacterial growth

to the environment (Cheung and Gu 2003; Desjardin et al. 2003; Sivaprakasam et al. 2008; Durai and Rajasimman 2011; Nigam et al. 2015; Garg et al. 2018; Raman et al. 2018; Vijayaraj et al. 2018). The present study also revealed that selected strains have significant potential to remove Cr from tannery effluent, and further removal can be accomplished with increased incubation time. Many genera of microorganisms such as Pseudomonas, Bacillus, Escherichia, and Enterobacter (Benazir et al. 2010; Divya et al. 2015; Garg et al. 2018) and also some yeasts (Gupta and Ahuja 2002), algae (Das et al. 2018; Losada et al. 2018), and fungi (Prigione et al. 2018) are capable in bioremediation of Cr-contaminated soil and water through biosorption and bioaccumulation of Cr (Bento and Okeke 2003; Vijayanand and Hemapriya 2014; Sharma and Malaviya 2016).

Conclusion Bioremediation is an eco-friendly, cost-effective, and sustainable approach to remove pollutants from industrial effluents posing a severe threat to our environment. The versatility of bacterial strains is present in nature that has great potential to treat a variety of environmental pollutants. In the present study, three bacterial strains viz., Pantoea stewartii ASI11, Microbacterium arborescens HU33, and Enterobacter sp. HU38, were found most effective at removing BOD, COD, TDS, TSS, and Cr from tannery effluent. These pre-isolated bacteria from P. juliflora, showed the ability to survive under highly saline wastewater loaded with Cr and therefore can be used profitably on an industrial scale. In the current scenario of worldwide water shortage, bioremediation offers a

promising strategy to improve the quality of water for safer disposal to agriculture/aquatic industries. Acknowledgments The authors are thankful to the Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, 38040, Pakistan, and the National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan, for providing research facilities. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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