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Chromium phytoaccumulation and its impact on growth and photosynthetic pigments of Spirodela polyrrhiza (L.) Schleid. on exposure to tannery effluent

  • Asha Singh
  • Piyush MalaviyaEmail author
Original Article
  • 82 Downloads

Abstract

Spirodela polyrrhiza (L.) Schleid. (giant duckweed)—a widespread aquatic macrophyte was found to be a potential chromium bioaccumulator in the present study. To assess the tolerance and hyperaccumulation of chromium by S. polyrrhiza, the plants were exposed to 25, 50, 75, and 100% concentrations of tannery effluent under laboratory conditions for 7 days. Significant toxic effects on the S. polyrrhiza plant were observed, as revealed by reduction in growth parameters as well as photosynthetic pigments in comparison to the control. Despite exhibiting severe phytotoxicity symptoms, the roots and fronds of S. polyrrhiza accumulated the highest amount of chromium on exposure to 100% tannery effluent (roots: 64,841.8 mg g−1; fronds: 10,478.4 mg g−1) after 7 days of exposure. Our results point to S. polyrrhiza as a proficient species to be used in the exploration of chromium hyperaccumulation as well as a prospective contender for tannery wastewater remediation.

Keywords

Bioaccumulation Chromium Phytoremediation Spirodela polyrrhiza Tannery effluent 

Introduction

Tanneries are one of the prime consumers of water, and spent chrome liquors. Wastewater discharged from this industry contains 2900–4500 mg L−1 and 10–50 mg L−1 of chromium (Cr), respectively (Sharma et al. 2008). Among different Cr oxidation states, Cr(III) and Cr(VI) are the two important oxidation states usually present in the environment. Cr(VI) is very toxic, potent epithelial irritant and a notable human carcinogen (EPA 1984; WHO 1988) that alters the DNA transcription process causing grave chromosomal aberrations. According to U.S. EPA, the Cr(VI) discharge to surface water is regulated below 0.05 mg L−1, while discharge of total Cr including Cr(III), Cr(VI) and its other forms is prescribed below 2 mg L−1 (Park et al. 2004). To be in conformity with this limit, it becomes crucial for different industries to treat their wastewaters for reduction of Cr to permissible limits. The traditional technique used for Cr removal is based on precipitation using chemicals coupled with reduction followed by filtration in order to concentrate the Cr species. The major drawback associated with the above-mentioned technique is the production of sludges containing toxic Cr compounds, which are ultimately disposed off in ordinary landfills. Use of other methods such as reverse osmosis, ultrafiltration and ion exchange have been found to be restricted, as they involve high capital as well as operational costs (Malaviya and Singh 2011, 2016). Even after these treatments, removal of Cr is incomplete and therefore, it is often necessary to employ further treatment and “polishing” so that the effluent may be discharged in accordance with the prescribed limits.

The detection of metal hyperaccumulating properties in some plants has led to the development of phytoremediation system as a substitute to the present physico-chemical technologies during the exploration for low cost and novel methods (Malaviya and Singh 2012a; Kumar et al. 2018, 2019). The premise of phytoremediation for tannery effluent is to find out a fast growing hyperaccumulator, which has a great capability to tolerate and accumulate Cr (Salt and Kramer 2000). However, for plants, Cr is a non-essential element which causes toxicity at higher concentrations (Shanker et al. 2005) and thus, toxicity tests are crucial in evaluating the capacity of the test plants for their booming application in phytoremediation technology (Malaviya and Sharma 2011). Most of the studies involving Cr hyperaccumulation have focused on plants exposed to Cr solutions (Adki et al. 2013; Augustynowicz et al. 2010; Di Luca et al. 2014; Kale et al. 2015; Lin et al. 2018; Monferrán et al. 2012; Sinha et al. 2009; Shukla et al. 2007; Vajpayee et al. 2000) and only few studies have been conducted on hyperaccumulation of Cr from tannery effluent (Calheiros et al. 2008; Sinha et al. 2002; Suseela et al. 2002; Vajpayee et al. 2001). On the same line, most of the studies involved the harmful effects of Cr containing solutions on growth and survival of plants used for phytoremediation with only a few conducted on toxicity of tannery effluent (Calheiros et al. 2008; Singh et al. 2016; Sinha et al. 2002; Vajpayee et al. 2001). The studies involving plants exposed to tannery effluent are very essential as they explain the viability of the remediation system under natural conditions by considering the effects of various physicochemical characteristics of effluent on the survival and efficiency of the test plants. Chromium in tannery effluent occurs in complex forms and differs in their availability to the plants used for phytoremediation (Gupta and Sinha 2007).

The use of hydrophytes in effluent treatment studies has been considered significant because they can be directly exposed to wastewater (Malaviya and Singh 2012b). Spirodela polyrrhiza—a free floating aquatic macrophyte, is distinguished by its pervasiveness, and its competence to grow at wide temperature range. Its each frond along with roots absorbs metal ions from the aqueous phase thus increasing the surface area for absorption of the pollutants. It multiplies rapidly through vegetative means and its specific growth rate is very high viz. 0.1–0.35 g g−1 day−1 (Porath and Pollock 1982) that helps it to convert the contaminants into low fiber biomass, leading to reduction in the bulk mass to be disposed off. Even with its excellent capability for heavy metal removal, the use of S. polyrrhiza for Cr accumulation is limited to only few studies (Kumar and Chandra 2004; Singh and Malaviya 2013; Singh et al. 2016).

In this study, attempts have been made to demonstrate Cr hyperaccumulation potential of S. polyrrhiza and to assess resultant toxic effects on growth and photosynthetic pigments of S. polyrrhiza on exposure to tannery wastewater. To understand complex interactions of Cr and S. polyrrhiza, tannery wastewater in the form of chrome liquor was used in the present study. This was done without addition of nutrient supplements, as these (nutrients) could interact with the different phytoremediation processes of S. polyrrhiza. Thus, present study aims in designing an efficient phytoremediation system, as a low cost and novel method for polishing Cr rich tannery wastewater.

Materials and methods

Plant species

The test plant S. polyrrhiza (giant duckweed) belongs to the family Lemnaceae under the group monocotyledons. The leaves and stems of this plant are merged in a common structure typically called as frond with a shiny green and soft thallus on the upper surface and reddish purple below. Bunch of 4–16 fibrous roots hang below the water surface from each plant. For toxicological tests and metal uptake experiments, Spirodela plants were collected from a natural pond. After collection, Spirodela plants were carefully cleaned under running water, in order to remove sediments and particles and were further acclimatized in large trough for 2 days.

Collection of effluent samples

The spent chrome liquor samples used in the present study were collected in pre-cleaned plastic containers from the wet blue section of a tanning industry located in SIDCO industrial complex, Samba (J&K), India. The effluent samples collected from the tannery were brought to the laboratory and were stored at 4 °C in a refrigerator till further studies.

Experimental design

The experimental set-up was placed in outdoor conditions with ambient air temperature showing diurnal variation of 23–39 °C. For the experiment, plastic trays of 1350 mL capacity and surface area of 337 cm2 were used. Seven sets, each containing 1 L of different concentrations of chrome liquor i.e., 25, 50, 75, and 100% (diluted using tap water) and a control (Spirodela plants in tap water) were placed in outdoor conditions. Healthy acclimatized Spirodela plants having uniform size and weight (~ 11 g) were inoculated to different concentrations of chrome liquor. In order to compensate loss of water due to evaporation as well as transpiration, tap water was further added daily to maintain the initial volume level. Out of the seven sets, one set was harvested after every 24 h, so that all the seven sets were harvested at the end of the experiment for analyzing the Cr-accumulation potential of S. polyrrhiza and phytotoxicity of different concentrations of tannery effluent. All the phytoaccumulation experiments were conducted in triplicate over a period of 7 days.

All the Spirodela plants were harvested at the end of each experimental period. The collected plant samples were further rinsed with tap water, and then rewashed with distilled water to remove any adhering remains of effluent. These washings were added to the respective concentrations of the exposed effluent. Further, they were dried using absorbent paper and fresh weight of the plants was recorded using an electronic digital balance. Then the roots and the fronds of the treated plants as well as control were separated and oven dried at 105 °C until a constant weight was obtained. Frond area was calculated by tracing the outline of twenty-five fronds on a graph paper and then taking mean of the squares within that outline. Further, twenty-five plant samples were also measured for root length and mean was calculated.

Analytical methods

Chlorophyll and carotenoids were measured from extracts of fresh plants using chilled 80% acetone following the methods of Arnon (1949) and Duxbury and Yentsch (1956), respectively. Anthocyanin content in fresh fronds and roots of the Spirodela plant was measured following the methodology given by Beggs and Wellmann (1985).

Total Cr in dried roots and fronds was extracted using nitric/perchloric acid digestion method. The finely ground plant samples (0.5 g fronds and 0.04 g root material) were kept overnight in 10 mL HNO3:HClO4 (4:1, v/v) and digested at 70–80 °C on hot plate in a Erlenmeyer flask. The samples were allowed to digest until 1–2 mL of clear digested material was left. The digested liquid was diluted to 25 mL with distilled water, and then filtered (Whatman no. 1 filter paper). Finally, the filtrates were analyzed for Cr by an atomic absorption spectrophotometer (TJA Solutions, Solaar M Series, U.K.). The translocation factor for Cr in S. polyrrhiza was estimated as the of ratio of [Cr]frond/[Cr]root to estimate the amount of Cr translocation from roots to fronds (Das and Maiti 2007).

Based on Standard Methods (APHA 1998) the following parameters were determined in all the four effluent concentrations as well as tap water: pH, turbidity, electrical conductivity (EC), chemical oxygen demand (COD) (open reflux method), total suspended solids (TSS) (dried at 103–105 °C), chloride (argentometric method), sulphide (iodometric method). For total Cr analysis, 10 mL of tannery effluent was digested in triacid mixture i.e., HNO3:H2SO4:HClO4 (9:4:1; v/v) and was analyzed by Atomic Absorption Spectrophotometer.

Statistical analysis

All the experiments were conducted in triplicate. The data obtained were statistically analysed using SPSS Inc. (v. 16.0) software for multiple analysis of variance to observe the significant effect of various concentrations of tannery effluent and different time durations on various parameters of S. polyrrhiza (L.) Schleid. The quantitative changes observed for various plant parameters due to various concentrations of tannery effluent were evaluated for the level of significance at 5% by Duncan’s multiple range test (DMRT).

Results and discussion

Physico-chemistry of tannery effluent

Various physicochemical characteristics of different concentrations of tannery effluent used in the Cr phytoaccumulation experiment are given in Table 1. The pH of different concentrations of effluent was observed to be in the acidic range viz. 2.0–2.4. Highest values of electrical conductivity (41.0 mS cm−1), TDS (26,240.0 mg L−1), chloride (7141.3 mg L−1), osmotic potential (16.4 atmospheres), sulphide (100.8 mg L−1), COD (2774.0 mg L−1) and total chromium (804 mg L−1) were observed for 100% effluent concentration. While, highest values of TSS (584 mg L−1) and turbidity (253 NTU) were observed for 25% effluent concentration owing to precipitation of Cr present in tannery effluent due to higher amount of tap water used for dilution in 25% effluent.
Table 1

Physicochemical characteristics of different concentrations of tannery effluent

Parameters

Tap water

Effluent concentrations

25%

50%

75%

100%

Colour

Colourless

Light bluish green

Dark bluish green

pH

9.4

2.4 ± 0.023

2.1 ± 0.035

2.0 ± 0.017

2.0 ± 0.012

EC(mS cm−1)

0.4

12.7 ± 0.029

23.5 ± 0.023

30.9 ± 0.035

41.0 ± 0.040

TDS (mg L−1)

256.0

8128.0 ± 18.5

15,008.0 ± 14.8

19,776.0 ± 22.2

26,240.0 ± 25.9

TSS (mg L−1)

Bdl

584 ± 8.21

532 ± 7.18

368 ± 12.90

278 ± 10.34

Turbidity (NTU)

2

253 ± 4.85

208 ± 6.24

96 ± 2.97

71 ± 5.18

Sulphide (mg L−1)

0.8

40.0 ± 4.21

64.0 ± 2.45

71.2 ± 5.13

100.8 ± 4.70

Chloride (mg L−1)

41.9

1698.5 ± 8.66

2948.4 ± 6.35

4047.7 ± 6.93

7141.3 ± 11.52

COD (mg L−1)

24.0

1285.0 ± 23.1

1632.0 ± 23.1

2392.0 ± 46.1

2774.0 ± 46.1

Osmotic potential (atmospheres)

0.16

5.08 ± 0.035

9.4 ± 0.026

12.36 ± 0.029

16.4 ± 0.023

Total chromium (mg L−1)

Bdl

193 ± 6.49

398 ± 5.80

596 ± 11.32

804 ± 10.94

Bdl below detectable limit

Changes in the growth parameters of S. polyrrhiza

Reduction in biomass of fronds and roots of Spirodela was observed with increasing tannery effluent concentration (Table 2). This was ascribed to the degradation of components of roots and fronds e.g., pigments and proteins (Keskitalo et al. 2005) as well as breaking of fronds and roots on exposure to all the four tannery effluent concentrations. In accordance with the present findings, reduction in dry weight of Cyanopsis tetragonoloba on exposure to tannery effluent was also reported by Pandi et al. (2005). In addition, Vajpayee et al. (2001) also reported reduction in dry weight of hydrophytes on Cr exposure.
Table 2

Changes in biomass of S. polyrrhiza on exposure to different concentrations of tannery effluent

Exposure

period

(days)

Effluent concentrations

Frond biomass (g)

Root biomass (mg)

0%

25%

50%

75%

100%

0%

25%

50%

75%

100%

1d

0.8350a ± 0.00085

0.8055b ± 0.00030

0.7952c ± 0.00035

0.774d ± 0.00040

0.7714e ± 0.00051

70.4a ± 1.80216

65.6b ± 1.21244

63.8b ± 0.50442

63.2b ± 1.48137

62.8b ± 0.76884

2d

0.9432a ± 0.00050

0.8040b ± 0.00053

0.7937c ± 0.00054

0.7729d ± 0.00056

0.7705e ± 0.00045

77.2a ± 2.11686

65.0b ± 1.83303

63.2b ± 2.05264

62.0b ± 1.86577

61.8b ± 1.05987

3d

1.0021a ± 0.00056

0.8028b ± 0.00070

0.7922c ± 0.00068

0.7720d ± 0.00061

0.7694e ± 0.00074

98.7a ± 2.77549

64.6b ± 1.02632

62.5b ± 0.81156

61.2b ± 0.43662

61.0b ± 0.37687

4d

1.1000a ± 0.00074

0.8012b ± 0.00060

0.7907c ± 0.00045

0.7711d ± 0.00035

0.7680e ± 0.00045

136.4a ± 3.27414

64.0b ± 2.24796

62.1b ± 0.81445

60.4b ± 0.98489

60.1b ± 0.75498

5d

1.2908a ± 0.00061

0.8004b ± 0.00061

0.7894c ± 0.00055

0.7700d ± 0.00080

0.7668e ± 0.00051

157.5a ± 3.62261

63.7b ± 2.41316

61.3b ± 1.56312

59.9b ± 1.78979

59.0b ± 1.13725

6d

1.4014a ± 0.00080

0.7991b ± 0.00047

0.7879c ± 0.00085

0.7688d ± 0.00046

0.7665e ± 0.00047

185.2a ± 1.88090

63.1b ± 1.76918

60.8b ± 1.66433

59.1b ± 1.78543

58.3b ± 1.00167

7d

1.4970a ± 0.00087

0.7980b ± 0.00062

0.7862c ± 0.00056

0.7682d ± 0.00053

0.7650e ± 0.00047

204.5a ± 6.45316

62.5b ± 2.12211

60.3b ± 2.26495

58.2b ± 1.37477

57.6b ± 1.50997

Within each column values not followed by the same letter are significantly different at p < 0.05

Upon treatment with 25% tannery effluent concentration, fronds of S. polyrrhiza started showing toxicity symptoms, such as increased fragmentation and necrosis by the second day of exposure. After same duration, the fronds exposed to higher concentrations (> 25% tannery effluent), showed no growth, and harvested biomass was almost dead with hardly any green fronds. Slight reduction in frond area at these effluent concentrations was ascribed to decaying and breaking of the fronds of the test plant. Similar reasons were attributed to the reduction in root length of Spirodela in a concentration-duration dependant manner (Table 3). Reduction in the frond area of S. polyrrhiza from 139 mm2 (after 1 day) to 46 mm2 (after 7 days) at 25% effluent concentration (Table 3) could be attributed to the strategy of fragmentation by the surviving plants in highly toxic effluent. Colony disintegration is a survival strategy of duckweeds to escape heavy metal toxicity and is also supported by the observations of Li and Xiong (2004a, b). These changes may involve ethylene production by the plants as a response to stress (Li and Xiong 2004a).
Table 3

Changes in root length and frond area of S. polyrrhiza on exposure to different concentrations of tannery effluent

Exposure

period

(days)

Effluent concentrations

Root length (mm)

Frond area (mm2)

0%

25%

50%

75%

100%

0%

25%

50%

75%

100%

1d

10.84a ± 0.882

9.76ab ± 0.512

8.92bc ± 0.762

8.24bc ± 0.170

7.64c ± 0.062

140a ± 4.163

139a ± 5.508

125ab ± 5.686

121b ± 5.567

117b ± 4.726

2d

12.13a ± 1.897

8.84b ± 0.832

8.56b ± 0.584

8.00b ± 0.671

7.60b ± 0.462

145a ± 3.000

131b ± 3.606

118c ± 5.686

114c ± 4.000

114c ± 3.606

3d

13.06a ± 1.870

8.24b ± 1.086

8.18b ± 0.812

7.91b ± 0.437

7.42b ± 0.377

148a ± 3.056

96c ± 5.033

109b ± 3.786

110b ± 2.646

106bc ± 2.646

4d

14.41a ± 1.644

7.64b ± 0.448

7.62b ± 0.642

7.22b ± 0.200

7.18b ± 0.366

127a ± 3.606

92c ± 5.132

108b ± 3.606

102bc ± 1.528

101bc ± 2.082

5d

16.10a ± 0.771

7.61b ± 0.809

7.28b ± 0.616

7.19b ± 0.199

7.19b ± 0.101

74b ± 6.557

73b ± 4.041

105a ± 5.508

99a ± 2.309

94a ± 2.309

6d

16.72a ± 0.424

7.24b ± 0.590

7.08b ± 0.170

6.92b ± 0.160

6.32b ± 0.125

106a ± 2.646

49d ± 2.646

104ab ± 2.646

97b ± 2.517

89 89c ± 2.000

7d

17.60a ± 1.356

6.98b ± 0.511

6.92b ± 0.396

6.60b ± 0.359

6.12b ± 0.259

119a ± 5.508

46c ± 4.163

99b ± 3.512

87b ± 3.055

87b ± 1.528

Within each column values not followed by the same letter are significantly different at p < 0.05

Changes in the photosynthetic pigments of S. polyrrhiza

The effect of tannery effluent on different pigments present in S. polyrrhiza revealed a gradual decrease in a concentration-duration dependent manner of total chlorophyll, chlorophyll-a (chl-a), chlorophyll-b (chl-b) (Table 4), carotenoid, frond anthocyanin and root anthocyanin (Table 5). In accordance with the present findings, several workers have reported decrease in chlorophyll concentration of hydrophytes on exposure to different concentrations of tannery wastewater (Singh et al. 2016; Sinha et al. 2002; Vajpayee et al. 2001). Likewise, among the plants exposed to different concentrations of tannery effluent, chl a/b ratio was found to be in the range of 0.50–1.87 (Table 4). Greater reduction of chlorophyll-a than chlorophyll-b was explained by higher sensitivity of chlorophyll-a as compared to chlorophyll-b, which is in accordance with the findings of Vajpayee et al. (2000).
Table 4

Effect of different concentrations of tannery effluent on the chlorophyll content of S. polyrrhiza

Effluent

concentrations

Exposure period (days)

1d

2d

3d

4d

5d

6d

7d

Total chlorophyll (mg g−1 fw)

 0%

0.528a ± 0.00529

0.529a ± 0.00611

0.534a ± 0.00451

0.551a ± 0.00416

0.529a ± 0.00551

0.520a ± 0.00282

0.511a ± 0.00265

 25%

0.233b ± 0.00 306

0.192b ± 0.00416

0.156b ± 0.00503

0.136b ± 0.00416

0.119b ± 0.00252

0.109b ± 0.00321

0.098b ± 0.00265

 50%

0.145c ± 0.00289

0.067c ± 0.00379

0.033c ± 0.00416

0.019c ± 0.00265

0.014c ± 0.00351

0.013c ± 0.00346

0.011c ± 0.00100

 75%

0.112d ± 0.00458

0.047d ± 0.00153

0.014d ± 0.00265

0.010cd ± 0.00100

0.006c ± 0.00100

0.005c ± 0.00100

0.005d ± 0.00058

 100%

0.064e ± 0.00503

0.024e ± 0.00265

0.008d ± 0.00115

0.006d ± 0.00058

0.004c ± 0.00000

0.003c ± 0.00000

0.003d ± 0.00058

Chlorophyll-a (mg g−1 fw)

 0%

0.347a ± 0.00436

0.366a ± 0.00338

0.376a ± 0.00306

0.374a ± 0.00416

0.299a ± 0.00379

0.281a ± 0.00265

0.251a ± 0.00265

 25%

0.152b ± 0.00173

0.120b ± 0.00240

0.096b ± 0.00611

0.082b ± 0.00321

0.065b ± 0.00451

0.058b ± 0.00462

0.048b ± 0.00173

 50%

0.089c ± 0.00346

0.041c ± 0.00265

0.019c ± 0.00208

0.010c ± 0.00100

0.007c ± 0.00115

0.006c ± 0.00100

0.005c ± 0.00000

 75%

0.058d ± 0.00265

0.024d ± 0.00351

0.007d ± 0.00115

0.004cd ± 0.00058

Bdl

Bdl

Bdl

 100%

0.033e ± 0.00153

0.012e ± 0.00173

0.003d ± 0.00100

0.002d ± 0.00058

Bdl

Bdl

Bdl

Chlorophyll-b (mg g−1 fw)

 0%

0.181a ± 0.00436

0.163a ± 0.00361

0.158a ± 0.00493

0.177a ± 0.00361

0.230a ± 0.00451

0.239a ± 0.00586

0.260a ± 0.00265

 25%

0.081b ± 0.00231

0.072b ± 0.00458

0.060b ± 0.00252

0.054b ± 0.00503

0.053b ± 0.00300

0.051b ± 0.00321

0.050b ± 0.00300

 50%

0.056c ± 0.00379

0.026c ± 0.00361

0.014c ± 0.00265

0.009c ± 0.00058

0.007c ± 0.00058

0.007c ± 0.00058

0.006c ± 0.00100

 75%

0.054c ± 0.00208

0.023c ± 0.00200

0.007c ± 0.00058

0.009c ± 0.00058

0.006c ± 0.00100

0.005c ± 0.00000

0.005c ± 0.00058

 100%

0.031d ± 0.00208

0.012d ± 0.00173

0.005c ± 0.00000

0.004c ± 0.00000

0.004c ± 0.00000

0.003c ± 0.00000

0.003c ± 0.00000

Chlorophyll a/b ratio

 0%

1.92

2.25

2.38

2.11

1.30

1.18

0.97

 25%

1.87

1.66

1.60

1.51

1.25

1.14

0.96

 50%

1.59

1.58

1.36

1.11

1.00

0.86

0.83

 75%

1.07

1.04

1.00

0.66

 100%

1.06

1.00

0.60

0.50

Within each row values not followed by the same letter are significantly different at p < 0.05

Bdl below detectable limit

Table 5

Effect of different concentrations of tannery effluent on carotenoid and anthocyanin content of S. polyrrhiza

Effluent

concentrations

Exposure period (days)

1d

2d

3d

4d

5d

6d

7d

Carotenoids (mg g−1 fw)

 0%

0.157a ± 0.00473

0.135a ± 0.00306

0.141a ± 0.00346

0.141a ± 0.00265

0.142a ± 0.00153

0.154a ± 0.00208

0.163a ± 0.00208

 25%

0.101b ± 0.00231

0.051b ± 0.00361

0.045b ± 0.00265

0.042b ± 0.00173

0.038b ± 0.00115

0.037b ± 0.00306

0.036b ± 0.00153

 50%

0.024c ± 0.00200

0.009c ± 0.00058

0.004c ± 0.00058

0.004c ± 0.00058

0.003c ± 0.00000

0.003c ± 0.00058

0.002c ± 0.00000

 75%

0.022c ± 0.00153

0.005c ± 0.00100

0.003c ± 0.00000

0.002c ± 0.00000

0.002cd ± 0.00000

0.001c ± 0.00000

0.001c ± 0.00000

 100%

0.009d ± 0.00058

0.004c ± 0.00000

0.002c ± 0.00000

Bdl

Bdl

Bdl

Bdl

Frond anthocyanin (mg g−1 fw)

 0%

0.0414a ± 0.00031

0.0553a ± 0.00025

0.0632a ± 0.00035

0.0644a ± 0.00026

0.0687a ± 0.00025

0.0696a ± 0.00021

0.0732a ± 0.00036

 25%

0.0218b ± 0.00026

0.0179b ± 0.00029

0.0176b ± 0.00021

0.0174b ± 0.00025

0.0162b ± 0.00015

0.0159b ± 0.00025

0.0128b ± 0.00025

 50%

0.0188c ± 0.00015

0.0162c ± 0.00026

0.0161c ± 0.00031

0.0153c ± 0.00031

0.0149c ± 0.00015

0.0142c ± 0.00025

0.0111c ± 0.00035

 75%

0.0156d ± 0.00026

0.0096d ± 0.00025

0.0089d ± 0.00032

0.0081d ± 0.00006

0.0076d ± 0.00015

0.0069d ± 0.00031

0.0068d ± 0.00025

 100%

0.0105e ± 0.00021

0.0084e ± 0.00015

0.0080e ± 0.00021

0.0075d ± 0.00015

0.0071d ± 0.00010

0.0066d ± 0.00025

0.0062d ± 0.00021

Root anthocyanin (mg g−1 fw)

 0%

0.0081a ± 0.00021

0.0104a ± 0.00021

0.0180a ± 0.00028

0.0243a ± 0.00031

0.0341a ± 0.00023

0.0456a ± 0.00026

0.0622a ± 0.00021

 25%

0.0061b ± 0.00017

0.0029b ± 0.00017

0.0008b ± 0.00010

Bdl

Bdl

Bdl

Bdl

 50%

0.0014c ± 0.00015

0.0004c ± 0.00006

Bdl

Bdl

Bdl

Bdl

Bdl

 75%

0.0008d ± 0.00006

Bdl

Bdl

Bdl

Bdl

Bdl

Bdl

 100%

0.0002e ± 0.00000

Bdl

Bdl

Bdl

Bdl

Bdl

Bdl

Within each row values not followed by the same letter are significantly different at p < 0.05

Bdl below detectable limit

The depletion of chlorophyll concentration in different plants exposed to Cr may be ascribed to altered biosynthesis of chlorophyll due to the disruption of chloroplast phosphorylation (Chandra and Kulshreshtha 2004). Cr causes toxic effects on δ-aminolevulinic acid dehydratase i.e., ALAD (an enzyme involved in chlorophyll biosynthesis) by impairing δ-aminolevulinic acid utilization. δ-Aminolevulinic acid dehydratase is a metalloenzyme and its activity in plants depends upon the availability of magnesium (Hayat et al. 2012). Therefore, Cr also reduces activity of ALAD by exchanging magnesium at the active site. Additionally, Cr(VI) exposure causes oxidative damage and enhances the activity of succinic dehydrogenase (Satyakala and Jamil 1992). Cr also leads to alteration in the metalloenzymes of the plant by displacing or replacing the metal ions by its ability to generate reactive oxygen species such as HO· and H2O2 which thereby causes oxidative stress (Shanker et al. 2005).

The maximum decrease in carotenoid content of S. polyrrhiza was found to be 99.38% after 7 days at 75% tannery effluent concentration as compared to the control. Present results revealing Cr induced degradation of carotenoids in aquatic macrophytes are also supported by the observations of Appenroth et al. (2001), Nichols et al. (2000), and Sinha et al. (2009). Frond anthocyanin showed maximum decrease (91.53%) after 7 days at 100% tannery effluent concentration as compared to the control. Whereas, root anthocyanin was below detectable limit in all the four tannery effluent concentrations after 4 days owing to acute toxicity of Cr present in the tannery effluent.

Bioaccumulation of chromium in S. polyrrhiza

The concentration of Cr in the dry biomass of both the fronds and the roots of S. polyrrhiza showed an increase in a concentration-duration dependent manner at all the four concentrations of tannery effluent. The maximum values of Cr concentration in the fronds (10,478.4 mg kg−1 dw) and roots (64,841.8 mg kg−1 dw) of S. polyrrhiza were very high (Table 6) as compared to the accumulation reported in previous studies on tannery effluent (Calheiros et al. 2008; Mant et al. 2006; Sinha et al. 2002; Suseela et al. 2002;Vajpayee et al. 2001). Maximum bioaccumulation of Cr (1.43%) in the Spirodela plant was observed at 100% concentration after 7 days (Table 7). Cr bioaccumulation by S. polyrrhiza as reported in the present study was found to be well above the critical concentration standards (0.1% or 1000 mg kg−1 dw) specified for hyperaccumulation of Cr (Reeves and Baker 2000).
Table 6

Bioaccumulation of chromium (mg kg−1 dw) in S. polyrrhiza from different concentrations of tannery effluent

Exposure period (days)

Effluent concentrations

Frond

Root

0%

25%

50%

75%

100%

0%

25%

50%

75%

100%

1d

354.5e ± 2.55

2195.6d ± 6.40

2627.4c ± 5.03

3216.4b ± 6.60

3439.3a ± 7.78

759.3e ± 5.38

10,504.7d ± 5.06

12,558.4c ± 5.10

15,518.4b ± 4.07

16,839.4a ± 5.68

2d

328.4e ± 6.42

4328.8d ± 3.72

4549.8c ± 7.39

5309.1b ± 6.35

6628.2a ± 5.93

692.6e ± 3.86

16,289.6d ± 3.99

17,370.1c ± 3.97

20,037.2b ± 5.74

23,172.3a ± 8.96

3d

304.4e ± 3.57

6042.5d ± 4.46

6267.4c ± 5.17

7243.3b ± 7.79

8042.6a ± 3.87

538.5e ± 7.96

20,363.4d ± 6.12

23,172.2c ± 5.52

27,149.5b ± 6.77

31,203.8a ± 5.47

4d

278.4e ± 4.97

6981.2d ± 8.88

7406.4c ± 6.41

8498.4b ± 6.047

9338.5a ± 6.68

407.2e ± 4.64

26,149.3d ± 2.61

31,203.3c ± 6.10

35,289.5b ± 4.74

40,728.1a ± 4.91

5d

232.1e ± 3.58

8015.5d ± 7.34

8627.7c ± 5.35

9025.5b ± 8.24

9713.1a ± 5.73

356.1e ± 4.80

30,254.9d ± 3.29

39,476.4c ± 4.80

44,728.6b ± 5.67

47,147.3a ± 9.93

6d

215.6e ± 7.19

8901.0d ± 5.32

9110.4c ± 5.10

9633.0b ± 6.26

9958.8a ± 5.48

302.7e ± 6.11

36,563.1d ± 3.19

48,954.2c ± 7.95

54,410.4b ± 6.33

56,523.2a ± 5.03

7d

196.3e ± 6.91

9648.4d ± 4.71

9940.3c ± 6.90

10,428.3b ± 4.91

10478.4a ± 4.62

268.9e ± 5.28

40,588.6d ± 5.05

57,956.4c ± 5.47

57,956.4c ± 5.47

64,841.8a ± 5.39

Within each column values not followed by the same letter are significantly different at p < 0.05

Table 7

Percent bioaccumulation and translocation factors for S. polyrrhiza exposed to different concentrations of tannery effluent

Exposure period (days)

Effluent concentrations

% bioaccumulation

Translocation factor

0%

25%

50%

75%

100%

0%

25%

50%

75%

100%

1d

0.04

0.28

0.32

0.41

0.44

0.47

0.21

0.21

0.21

0.20

2d

0.04

0.52

0.55

0.64

0.79

0.47

0.27

0.26

0.26

0.29

3d

0.03

0.71

0.75

0.87

0.97

0.56

0.30

0.27

0.27

0.26

4d

0.03

0.85

0.91

1.04

1.16

0.68

0.27

0.24

0.24

0.23

5d

0.02

0.97

1.09

1.16

1.24

0.65

0.26

0.22

0.20

0.21

6d

0.02

1.09

1.19

1.28

1.33

0.71

0.24

0.19

0.18

0.18

7d

0.02

1.22

1.34

1.40

1.43

0.73

0.24

0.17

0.17

0.16

Regarding Cr(VI) removal by aquatic macrophytes, two processes have been observed, (1) an initial fast, reversible, metal binding process (biosorption) and (2) a slow, irreversible, ion-sequestration step (bioaccumulation) (Dan et al. 2016; Jena et al. 2016; GracePavithra et al. 2019). Thus, bioaccumulation and/or biosorption could be the mechanisms responsible for Cr removal by S. polyrrhiza.

As shown in Table 6, bioaccumulation of Cr in root tissues was higher as compared to the frond tissues. Earlier studies on Cr accumulation by aquatic macrophytes have also reported greater accumulation of Cr in roots in comparison to the aboveground parts of plants (Calheiros et al. 2008). The translocation factors (ratio of Cr concentrations in fronds to those in roots) for S. polyrrhiza were found to decrease with the increase in concentration of tannery effluent (Table 7) which was ascribed to the accumulation and immobilization of Cr in the roots at higher concentration due to the process of rhizofiltration (Rai 2019). The data obtained after statistical analysis for multiple analysis of variance to observe the significant effect of various concentrations of tannery effluent and different time durations on various parameters of S. polyrrhiza is given in Table 8.
Table 8

Variance ratio for growth parameters, pigment content and chromium bioaccumulation in S. polyrrhiza exposed to different concentrations of tannery effluent at different time intervals

Parameters

Exposure time

Treatment

Exposure time × treatment

Frond biomass

32,340.0***

550,600.0***

35,910.0***

Root biomass

94.893***

1602.0***

132.714***

Root length

0.157NS

112.067***

3.668***

Frond area

97.706***

66.994***

13.918***

Total chlorophyll

220.056***

14,240.0***

20.977***

Chlorophyll-a

512.951***

18,660.0***

70.461***

Chlorophyll-b

69.556***

5724.0***

62.957***

Carotenoid

127.092***

8411.0***

28.428***

Frond anthocyanin

26.442***

58,510.0***

567.300***

Root anthocyanin

462.805***

8346.0***

605.666***

Cr bioaccumulation in fronds

580,300.0***

2,027,000.0***

40,270.0***

Cr bioaccumulation in roots

23,160,000.0***

52,800,000.0***

1,739,000.0***

Levels of significance are *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001, NS: not significant (p > 0.05)

Storage of heavy metals in roots may be an exclusion strategy of plants as roots are located below the surface and are not involved in the photosynthetic activity (Weis and Weis 2004). Additionally, the presence of cellulose and hemicellulose is higher in roots in comparison to leaves; therefore, more hydroxyl groups in roots coordinate with Cr and further aid in its uptake inside root tissues (Gardea-Torresdey et al. 1998). Higher accumulation of Cr in roots is also explained by its immobilization inside the vacuoles of the root cells, which is a survival strategy of the plant against toxicity of Cr (Shanker et al. 2005; Chaudhary and Sharma 2019).

Other then translocation, Cr bioaccumulation in the fronds of S. polyrrhiza could also be explained by penetration of Cr cations in the fronds directly through the cuticle owing to its large surface area in direct contact with the tannery effluent (Greger 1999). Furthermore, from the external surface towards the cell walls, a distinct gradient ranging from low charge density to high charge density occurs, and along this gradient the cation penetration is preferred across the cuticle (Yamada et al. 1964). Still, even after direct absorption of Cr through the frond surface as well as translocation from the roots, bioaccumulation of Cr in the roots far exceeded its in comparison to that in the fronds.

Even after severe phytotoxic symptoms, plants exposed to higher effluent concentrations revealed elevated uptake of Cr which could be attributed to movement of Cr ions from the tannery effluent to the cell walls of the roots by a non-metabolic and passive process driven by diffusion due to higher concentration of metal in the effluent (Marschner 1995). Other possible mechanisms involving uptake of Cr include its ingress into the root symplast by crossing the plasma membrane of the root endodermal cells or its further entrance into the root apoplast through the space between the root cells. Once loaded into the xylem, the flow of the xylem sap conveys the Cr ions towards the leaves. After gaining its entry into the leaf tissues, Cr can be sequestered in several subcellular compartments viz. cell wall, vacuole or cytosol, and further, can be converted into less toxic forms through complexation or chemical conversion. Another explanation of Cr hyperaccumulation by stressed plants may be that living plants close the channels and carriers at increased intracellular concentrations of heavy metals (Marschner 1995). Further, it is likely that living plants excrete some compounds such as peptides, which form complexes with heavy metals like Cr in the external medium or effluent, thereby decreasing both intra as well as extracellular accumulation of heavy metals (Greger 2005).

Conclusion

S. polyrrhiza (L.) Schleid. was found to be a potential bioaccumulator of Cr from tannery wastewater. In the present work, reduction in the values of translocation factor by increasing Cr concentration indicated that the roots of S. polyrrhiza could accumulate significant amounts of Cr and restrict its entry towards the fronds, in an attempt to protect the fronds from Cr phytotoxicity. In the present study, despite low translocation of Cr in fronds, its accumulation in roots of a free floating macrophyte like S. polyrrhiza does not pose a big trouble, as whole plant body of giant duckweed along with the roots could be harvested very easily, thus help in removing Cr from the wastewater. Although the Cr levels in tannery effluent were high enough to cause severe toxicity to the test plant, such higher concentrations made Spirodela to hyperaccumulate Cr (maximum bioaccumulation: 1.43%), well above the specified critical concentration standards. Therefore, the Spirodela species used in the present study has the potential to be used for the in situ phytoaccumulation of Cr from tannery wastewater and the data thus obtained would be useful in designing an efficient treatment system for further polishing of Cr rich tannery effluent leading to the sustainability of aquatic ecosystems.

Notes

Acknowledgements

The corresponding author (PM) acknowledges the financial support in the form of a research project provided by the Department of Biotechnology (DBT), Government of India.

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Copyright information

© Society for Environmental Sustainability 2019

Authors and Affiliations

  1. 1.Department of Environmental ScienceUniversity of JammuJammuIndia

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