Biosurfactant and exopolysaccharide-assisted rhizobacterial technique for the remediation of heavy metal contaminated soil: An advancement in metal phytoremediation technology

Accepted Manuscript Biosurfactant and exopolysaccharide-assisted rhizobacterial technique for the remediation of heavy metal contaminated soil: An advancement in metal phytoremediation technology Shatrohan Lal, Sheel Ratna, Olfa Ben Said, Rajesh Kumar

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S2352-1864(17)30408-X https://doi.org/10.1016/j.eti.2018.02.011 ETI 212

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Environmental Technology & Innovation

Received date : 2 December 2017 Revised date : 20 February 2018 Accepted date : 25 February 2018 Please cite this article as: Lal S., Ratna S., Said O.B., Kumar R., Biosurfactant and exopolysaccharide-assisted rhizobacterial technique for the remediation of heavy metal contaminated soil: An advancement in metal phytoremediation technology. Environmental Technology & Innovation (2018), https://doi.org/10.1016/j.eti.2018.02.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Full title: Biosurfactant and Exopolysaccharide-assisted Rhizobacterial technique for the remediation of heavy metal contaminated soil: An advancement in metal Phytoremediation technology Authors: Shatrohan Lal1, Sheel Ratna1, Olfa Ben Said1, 2 and Rajesh Kumar1* Affiliations: 1. Rhizosphere Biology Laboratory, Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar (A Central) University, Vidya Vihar, Raebareli Road, Lucknow, 226 025, India 2. Laboratory of Environment Biomonitoring, Coastal Ecology and Ecotoxicology Unit, Faculty of Sciences of Bizerte, University of Carthage, Zarzouna 7021, Tunisia *Corresponding Author Dr Rajesh Kumar Professor (Full) Rhizosphere Biology Laboratory, Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar (A Central) University, Vidya Vihar, Raibareli Road, Lucknow, 226 025, India Phone No.: +91_ 9412090052 +91_9621329477 E-mail: [email protected] Alternate E-mail: [email protected]

Abstract Biosurfactant and exopolysaccharide producing plant growth promoting rhizobacteria can be a best tool for increasing the efficiency of plant assisted remediation of heavy metal contaminated soil; because they can thrive in the stressful environment in a luxuriant way, support plant growth and also contribute to the remediation process. Heavy metals are a noteworthy environmental pollutant and are regarded as biosphere hazard. Numerous chemically based techniques are used to enhance the efficacy of phytoremediation; however, most of them are ecotoxic, highly expensive and lead to incomplete removal of pollutants. To mitigate these technical inherent and to ensure complete removal of toxic heavy metals from soil, an advanced biological tool is the use of biosurfactant and exopolysaccharide-producing rhizobacteria. This can be a promising technique, that has been operative in nature and is cost effective, eco-friendly, efficient and having socio-economic importance over other conventional remediation techniques as well as sustainable for the environment. The present article critically reviews the potential role of root-associated metal resistant, exopolysaccharide and biosurfactant producing rhizospheric bacteria to remediate heavy metal contaminated soil and highlight some insight mechanisms for exploitation of plants and associated rhizobacterial interactions for enhancing heavy metal remediation. Keyword: Biosurfactants, Exopolysaccharide, Biosorption, Phytoremediation, Heavy Metals, PGPR.

1 

Biosurfactant and Exopolysaccharide-assisted Rhizobacterial technique for the remediation of heavy

2 

metal contaminated soil: An advancement in metal Phytoremediation technology

3 

Abstract

4 

Biosurfactant and exopolysaccharide producing plant growth promoting rhizobacteria can be a best tool for

5 

increasing the efficiency of plant assisted remediation of heavy metal contaminated soil; because they can thrive

6 

in the stressful environment in a luxuriant way, support plant growth and also contribute to the remediation

7 

process. Heavy metals are a noteworthy environmental pollutant and are regarded as biosphere hazard.

8 

Numerous chemically based techniques are used to enhance the efficacy of phytoremediation; however, most of

9 

them are ecotoxic, highly expensive and lead to incomplete removal of pollutants. To mitigate these technical

10 

inherent and to ensure complete removal of toxic heavy metals from soil, an advanced biological tool is the use

11 

of biosurfactant and exopolysaccharide-producing rhizobacteria. This can be a promising technique, that has

12 

been operative in nature and is cost effective, eco-friendly, efficient and having socio-economic importance over

13 

other conventional remediation techniques as well as sustainable for the environment. The present article

14 

critically reviews the potential role of root-associated metal resistant, exopolysaccharide and biosurfactant

15 

producing rhizospheric bacteria to remediate heavy metal contaminated soil and highlight some insight

16 

mechanisms for exploitation of plants and associated rhizobacterial interactions for enhancing heavy metal

17 

remediation.

18 

Keyword: Biosurfactants, Exo-polysaccharide, Biosorption, Phytoremediation, Heavy Metals, PGPR.

19  20  21  22  23  24  25  26  27 

1. Introduction

28 

Contamination of soil by heavy metals is toxic for living beings and environment because of their persistence in

29 

nature, low bioavailability, carcinogenic, mutagenic and teratogenic nature (Jomova and Valko, 2011; Adrees et

30 

al. 2015). The most seeming natural sources of heavy metals are weathering of minerals, erosion and volcanic

31 

activities, forest fires and particles released by vegetation; whereas anthropogenic sources include human

32 

activities such as mining, smelting, ore processing, irrigation by sewage water, injudicious use of chemical

33 

fertilizers and pesticides, pile up of municipal wastes, automobile exhaust, electroplating, leather tanning,

34 

textiles and dyeing, distilleries and other industrial and domestic activities pouring directly or indirectly into the

35 

environment increases the concentration of heavy metals (Dixit et al. 2015; Sarwar et al. 2017; Yang et al.

36 

2017). Due to non-biodegradable nature and high solubility in the aqueous environment, the toxicity and

37 

contamination by heavy metals is increasing day by day (Desai et al. 2008; Liu et al. 2012). The aqueous soil

38 

environment provides a dynamic medium for chemical reactions, transfer and circulation of heavy metals

1   

39 

through the soil to the organisms, and also to the aquatic environment (Violante et al. 2010). Heavy metal enters

40 

into the human body by ingestion, inhalation, through contaminated food or through skin contact; their presence

41 

in the body causes serious health problems (Alissa and Ferns, 2011). Hence, remediation of heavy metals from

42 

soil is needed to protect the adverse effect on human health and conserve the environment for future generations

43 

(Glick, 2010). Numerous physical and chemical techniques have been implemented for remediation or

44 

detoxification of heavy metals from soil, which is viewed as a challenging job with respect to cost and technical

45 

complexity (Das et al. 2017). So massive attention has been paid to the build-up of practices and a new

46 

biological technique, which should be convenient and operative, easily available, eco-friendly in nature, cost-

47 

effective over conventional techniques, and efficient at even trace level of contamination. In this regard, a recent

48 

eco-friendly microbe based technique in which application of heavy metal resistant exopolysaccharides (EPS)

49 

and biosurfactant producing plant growth promotory (PGPR) rhizobacteria in combination with plants is

50 

proposed. This technique could be highly beneficial for complete removal of toxic heavy metals from the soil.

51 

Heavy metal resistant rhizobacteria play important role in maintaining soil structure and fertility (Kumar et al.

52 

2015), because they respond quickly in adverse conditions and are very sensitive to subtle environmental

53 

changes (Yu et al. 2014). They have also been regarded as efficient bioindicators of soil quality (Valverde et al.

54 

2011). Therefore, we propose this review article in which main focus is on the toxic effect of heavy metals,

55 

particularly on environment and living beings and their removal techniques using most important physiological

56 

properties of rhizobacteria such as biosurfactant and exopolysaccharide in combination with plant and their

57 

evaluation for potential partnerships that can be used to enhance the efficiency of phytoremediation of heavy

58 

metal contaminated soil.

59 

2. Exposure effects of heavy metals on livings

60 

Metallic elements with insoluble sulphides and hydroxides, whose salts produce coloured solutions in water, and

61 

whose complexes are usually coloured” are known as heavy metal (Stephen J. Hawkes 1999). Most of the heavy

62 

metals are electronegative in nature with a density greater than 5gm cm-3 (Adrees et al. 2015; Abdusslam et al.

63 

2015). Metals that have no metabolic activity in the living system and show toxic nature are known commonly

64 

as Potentially Toxic Elements (PTE) (Khan et al. 2015). The most common PTE are arsenic (As), cadmium

65 

(Cd), chromium (Cr), mercury (Hg), nickel (Ni), and lead (Pb) (Moore et al. 2016; Ali et al. 2013) (Table 1).

66 

They exist in nature in numerous forms such as elemental (or metallic); inorganic and organic compounds

67 

(Nagajyoti et al. 2010). The dynamism between the amount of heavy metals that exist in the soil and its uptake

68 

by plants is not linear because its bioavailability is affected by the combined effects of several variables for

69 

example cation-exchange capacity, soil organic matter, soil pH, soil aeration, clay content and plant species

70 

(Wilson et al. 2014 Chibuike and Obiora. 2014). Furthermore, their accumulation in plant body is also

71 

controlled by such variables as their species and/or the variety (Kibria 2008; Nouri et al. 2009). Besides this,

72 

toxicity of heavy metal also depends on its chemical forms, amount and exposure pathway and differences in

73 

vulnerability between exposed subjects (Gibb and O'Leary 2014; Rice et al. 2014;). Moreover, food crops/grains

74 

are one of the important parts of our diet, and they may contain a number of essential and toxic metals

75 

depending on the soil in which plant grows (Yang et al. 2011; Waqas et al. 2015). Vegetables are the major

76 

source for human exposure to heavy metal and contribute about 75% of the total metal intake, while the rest 25

77 

% intake occurs through dermal contacts and inhalation of contaminated dust (Martorell et al. 2011; Lal et al.

2   

78 

2013; Khan et al. 2014). Various deleterious effects in living beings by different heavy metals are discussed and

79 

well-illustrated in figure (1.a and b). One of the most  deleterious members of PTE group is Mercury (Hg);

80 

frequently known to be an

81 

environmental neuro-toxicant having adverse effect on health and causes many disorders, including

82 

neuropsychological dysfunctions; potentially cause impairment of pulmonary

83 

dyspnoea, learning and emotional disturbances in humans and adult rats (Kim et al. 2016). Mercury exposure is

84 

frequently responsible fordisorders in menstrual cycle and adverse effects on sperm mobility (Hatef et al. 2011;

85 

Neeti and Prakash 2013). Cadmium (Cd) is another potentially toxic element causes severe health problems; it is

86 

the main causative agent of Itai-Itai disease (Verougstraete et al. 2002). It's lower concentration may cause

87 

malfunctions of the kidney as proteinuria, hypercalciuria, glucosuria, phosphaturia and aminoaciduria renal

88 

toxicity, hepatotoxicity and carcinogenicity, lung cancer, and, damage to the respiratory system in humans

89 

(Filipic, 2012; Alslaibi et al. 2013). Chouchene et al. (2016) reported, Cd as a potent anti-estrogen in-vivo and

90 

in-vitro and provides evidence that Cd inhibits estrogen action in the developing Zebrafish brain, as

91 

demonstrated by inhibition of E2 (Estradiol) induction of Aro-B. Zhang et al. (2017) carried out a study to

92 

assess the long-term dietary Cd intake of school children aged 2–6 and 7–17 years from Jiangsu Province China,

93 

assuming lower bound and upper bound concentration. Regarding the evaluation of risk, the children with high-

94 

end exposure may suffer non-carcinogenic effects over a lifetime of exposure. Rice and rice products, wheat

95 

flour and wheat flour products, crustaceans, pak-choi, pig meat, beans and bean products were the major

96 

contributors to total Cd intake (Zhang et al. 2017). Lead (Pb) is the second most toxic metal in PTE group,

97 

having the capability to replace substitute for other bivalent cations like Ca2+, Mg2+, Fe2+, Zn2+ and monovalent

98 

cations like Na+ (Petrus and Warchol, 2003). In the human body, lead competes with Ca2+ which affects the inter

99 

and intracellular signalling, cell adhesion, protein folding and maturation, disrupts neurotransmitter release and

100 

bone mineral density (Flora et al. 2012; Beier et al. 2013; Clemens et al. 2016; Eqani et al. 2016). Other

101 

deleterious mechanism by Pb is the generation of free radical and adducts formation with amino levulinic acid

102 

(ALA), the heme precursor whose levels are elevated by lead exposure through feedback inhibition of the

103 

enzyme d-amino levulinic acid dehydrogenase (ALAD) (Kasperczyk et al. 2004; Flora et al. 2008). In the

104 

presence of lead (Pb), ALA has the tendency to bind to sulfhydryl group and thus results in overproduction of

105 

reactive oxygen species (ROS;Gillis et al. 2012; Breton et al. 2016). Several studies have demonstrated that liver

106 

is an organ capable of being injured by Cr (VI) (Wood et al. 1990). Cr (VI) hepatotoxicity is associated with

107 

increased reactive oxygen species (ROS) levels (Wang et al. 2006; Patlolla et al. 2009), lipid peroxidation

108 

(Bagchi et al. 1995a, 1995b), DNA damage (Henkler et al. 2010), inhibition of DNA, RNA and protein

109 

synthesis (Gunaratnam and Grant, 2008), reduction of the activity of the antioxidant enzymes ( Soudani et al.

110 

2013), mitochondrial damage (Pourahmad et al. 2005).The International Agency for Research on Cancer

111 

(IARC) classified all nickel compounds (except metallic nickel) as carcinogenic to humans (Cogliano et al.

112 

2011). Nickel (Ni), over its critical level might bring about serious effects in humans causing nausea; vomiting;

113 

diarrhoea; pulmonary fibrosis; renal edema; skin dermatitis; gastrointestinal distress, and stimulation of

114 

neoplastic transformation (Coman et al. 2013). Latvala et al. 2016 carried out a study on the occupational

115 

exposure of metallic nickel (Ni) and nickel oxide (NiO2) micro and nano-particles with special emphasis on

116 

cytotoxicity, genotoxicity and ROS generation. They reported that dose between 20 - 40μg cm-2 of metallic Ni

117 

and NiO2 nanoparticles was most potent in causing cellular ROS generation and DNA damage. Zhu et al. (2017)

3   

function, chest pain and

118 

investigated the subchronic pulmonary toxicity induced by nickel oxide (NiO2) nanoparticle and its potential

119 

mechanism in rats. The NiO2 (0.24 mg kg1 b.w.) nanoparticles depicted general toxicity by slow growth rate in

120 

body weight and decreased food utilization efficiency. Lung lesions induced by NiO2 nanoparticles could be

121 

related to oxidative stress and inflammatory response. Arsenic is a well-known, potentially toxic element with

122 

no known metabolic functions. Millions of people worldwide are exposed As from drinking water in India,

123 

China, Taiwan, and parts of US (Bjørklund et al. 2017). Ingestion of inorganic As via contaminated drinking

124 

water is associated with severe health consequences, that includes chronic diseases, pre-malignant skin lesions

125 

and cancers of the skin, lungs, bladder, liver, and kidneys, as well as non-carcinogenic outcomes including

126 

cardiovascular disease, diabetes mellitus, edema, weakness, conjunctival congestion, hypertension, respiratory

127 

problems, neurological deficits (Bjørklund et al. 2017). Inhalation of arsenic-contaminated water and food

128 

results in accumulation of arsenic in liver, spleen, kidneys, lungs, and gastrointestinal tract. Recently Mir et al.

129 

(2017) developed a cell line model to understand the molecular mechanisms involved in arsenic-mediated

130 

toxicity and carcinogenicity in human skin. They reported that oxidative stress was one of the most prominent

131 

mechanisms of toxicity and subsequent cause of carcinogenesis in human skin. Apart from the toxic effects,

132 

some heavy metals are essential for physiological functions of living tissues and regulate many biochemical

133 

processes, but the higher concentration can lead to notorious health problems and severe poisoning (Oves et al.

134 

2016). For instance, Zinc is a trace element that is essential for normal growth and reproduction but higher than

135 

permissible limit can cause stomach cramps, skin irritation, vomiting, nausea and anaemia (Oyaro et al. 2007).

136 

Copper (Cu) is another essential element, which plays an important role in metabolism and acts as co-factors for

137 

various enzymes of redox cycling, but the excessive ingestion of copper brings about serious toxicological

138 

anxieties, such as vomiting, cramps, convulsions, or even death (Oves et al. 2016). Iron is an essential part of the

139 

proteins (Haemoglobin) that transports oxygen in human body and in chlorophyll of plant helping in the

140 

production of food but in excess concentration it gets deposited in the liver, heart and pancreas, where it can

141 

cause cirrhosis, liver cancer, cardiac arrhythmias and diabetes in humans (Lee et al. 2015; Dusek et al. 2015),

142 

whereas excess concentration of iron in plant causes bronzing and stippling of leaves (Suriyagoda et al. 2017;

143 

Saikia and Bhuyan 2017). Selenium is an essential element for humans and animals, take part in the formation

144 

of glutathione peroxidase (GPx) and thioredoxin reductases (TrxR), but at higher concentrations, selenium

145 

replaces sulphur from proteins, consequently changing the activity of many enzymes (Wu et al. 2015).

146 

3. How potential plants and their associated rhizobacterial community act for metal removal?

147 

Soil is the principal component of our environment, constituting ecosystem and is an important factor basis of

148 

human being survival and development. However, it also is a medium to contaminate food chain by heavy

149 

metals because soil is used as a carrier for waste management and waste dumping sites (Zhuang et al. 2009;

150 

Rogival et al. 2007). Various physical, chemical and biological techniques are used to remediate metal

151 

contaminated soil, but all of them have some drawbacks. Remediation of metal contaminated soil through

152 

physical methods has certain limitations, as they alter soil microflora, cause irreversible alterations in soil

153 

properties and are labour intensive and costly (Yao et al. 2012). In the same way, chemical processes for

154 

removal of toxic metals are very expensive, generate secondary pollutants, and produce large quantities of

155 

sludge (Tangahu et al. 2011; Yao et al. 2012; Zubair et al. 2016). These approaches only change the form of the

156 

problem and fail to remediate the pollutants thoroughly (Gomes et al. 2016). In this context, application of

4   

157 

plants with their associated rhizobacterial technique can be the best alternative. The rhizosphere represents a

158 

unique and dynamic zone of plant-microbe-soil interactions where intense biological activity and root exudation

159 

create gradients in soil physico-chemical and biological parameters (Kidd et al. 2017). Bacteria present in the

160 

rhizosphere, known as plant growth promoting rhizobacteria (PGPR) (Kloepper and Schroth, 1978), contribute

161 

to the remediation of heavy metals (Khan et al. 2009). Rhizobacterial assisted remediation of heavy metals is a

162 

biological technique in which heavy metals are eliminated from the environment (Chibuike and Obiora, 2014;

163 

Gomes et al. 2016). This process can be performed through various treatment methods such as bio-filters, in situ

164 

bioremediation like bioaugmentation and biostimulation, bioventing and ex-situ methods like composting,

165 

bioreactors, land farming etc. (Ullah et al. 2015a,b). Roman-Ponce et al. (2017) reported rhizobacterial strains

166 

Microbacterium sp. CE3R2, Microbacterium sp. NE1R5, Curtobacterium sp. NM1R1 and Microbacterium sp.

167 

NM3E9 efficiently remediate As(V), Pb(II), Cu(II), and Zn(II) in the agro-ecosystem. Phytoremediation (a type

168 

of bioremediation), a technique in which plants are used as a remediator or accumulating agents for the removal

169 

of toxic heavy metals (Ali et al. 2013). Plants used in this technique, have a strongly increased rate of heavy

170 

metal uptake, rapid translocation from root-to-shoot and excellent ability to detoxify and sequester heavy metals

171 

in aerial parts. Some plants are capable to accumulate a good amount of heavy metals in their tissues e.g.

172 

Eleocharis acicularis can accumulate As, Cu, Zn and Pb in their parenchymatous cells (Ha et al. 2011).

173 

Although remediation of heavy metals through the plant (phytoremediation) is easily applicable and cost-

174 

effective technique, it does have some inherent technical constraints like, it is restricted to the site and the food

175 

chain could be adversely affected if these plants are used as food or fodder (Das et al. 2016). Phytoremediation

176 

technology may become efficient if fast-growing plants are inoculated with plant growth stimulators along with

177 

significant metal chelators (Alkorta et al. 2004). Plant-associated rhizobacteria help in the mitigation of these

178 

constraints as they have plant growth promoting characteristics along with biochelators and also help in

179 

reduction, removal or stabilization of the contaminants in soil environment (Greipsson 2011). Plants and

180 

beneficial microbes have diverse mechanism for the removal of toxic heavy metals from contaminated soil

181 

through

182 

volatilization) process (Lebeau et al. 2008; Glick, 2010). Nowadays, attention of microbiologists towards their

183 

associated microbiome and their potential influence on plant metal uptake and accumulation is gaining attention.

184 

extraction

(phyto-extraction),

stabilization

(phyto-stabilization)

and

transformation

(phyto-

4. Plant and Rhizobacterial mechanisms involved in removal of toxic heavy metals

185 

Plants play a crucial role in the remediation of heavy metals, to understand the mechanism clearly underlying,

186 

their genetic basis can be an important aspect regulated by an inter-related network of physiological and

187 

molecular mechanisms. Various species of plants possess different kinds of mechanisms to tolerate heavy

188 

metals, although within one species more than one mechanism could be in operation (Hossain et al. 2012). For

189 

instance Noccaea (Thlaspi) caerulescens is a well-known metal hyper-accumulator plant and can grow in

190 

serpentine soils, accumulate high levels of heavy metals including Zn, Co, Pb, Cr, Cd and Ni (Baycu et al.

191 

2017). Interestingly, this plant is able to accumulate up to 30,000 and 1000 mg/kg of Zn and Cd, respectively in

192 

their mesophyll cells in non-toxic forms while its growth remains unaffected (Vogel-Mikuš et al. 2008; Baycu et

193 

al. 2017). Commonly plants shows two types of tolerance mechanism against heavy metals. First is constitutive

194 

and second is adaptive (Baycu et al. 2017). Adaptive is the most common mechanisms acquired by metal

195 

tolerant plants include immobilization, plasma membrane exclusion, synthesis of specific heavy metal

5   

196 

transporters, induction of stress proteins, restriction of uptake and transport, chelation and sequestration of

197 

heavy metals by particular ligands (PCs and MTs), biosynthesis of Pro, polyamines and signalling molecule

198 

such as salicylic acid and nitric oxide (Hossain et al. 2012). Amongst all adaptive mechanisms, phytochelation

199 

of heavy metals is one of the important mechanisms in which root exudates chelate heavy metals and these

200 

chelated metal binds easily to the cell wall and enter into the cell (Fig. 2). Inside the cells, a high-affinity peptide

201 

compound is produced, that binds heavy metals and hence controls their cytoplasmic concentration by

202 

transporting them across tonoplast and their subsequent sequestration in the vacuole (Saraswat and Rai, 2011).

203 

Mainly, two classes of peptides that play an important role as metal chelators are: phytochelatins (PCs) and

204 

metallothioneins (MTs). Phytochelatins (PCs) enzymatically synthesize cysteine-rich polypeptides with general

205 

structure (c-Glu-Cys) n-Gly that chelate heavy metals in the cytosol. Many researchers reported the role of PCs

206 

and MTs in the detoxification of heavy metals and metal tolerance in many plants (Guo et al. 2008; Yadav et al.

207 

2010; Shahid et al. 2016; Shahid et al. 2017). Cadmium toxicity induces the rapid synthesis of PC (thiol-based

208 

complex substance) that forms complexes with Cd and decreases its activity in the cytosol (Stolt et al. 2003;

209 

Sharma et al. 2017; Romano et al. 2017; Jacquart et al. 2017). Besides plant, PC’s have been reported in yeasts,

210 

protists and nematodes (Rigouin et al. 2013) but there is no evidence for its presence in humans or other

211 

mammals. Another important peptide by which plants combat abiotic heavy metal stresses is the metallothionein

212 

(MT) which are cysteine rich low molecular weight peptides and are involved in binding heavy metals (Sharma

213 

et al. 2017). MT’s have been implicated in homeostasis of essential heavy metals, protection against oxidative

214 

stress and for virulence of fungi (Garcia et al. 2016). Chen et al. (2017) reported two genes encoding

215 

metallothioneins OsMT-1 and OsMT-2 in paddy plantlet combating mercury toxicity. Another recent study

216 

carried by Ziller et al. (2017) reported five CRP (cysteine-rich protein) MT genes viz. CRP-1, CRP-2, CRP-3,

217 

CRP-4, and CRP-5 for chelating Cd, Zn and Cu in yeast.

218 

Role of MTs in metal detoxification has also been ascertained in animals and microbes. In animals, MTs have a

219 

protective role against Cd toxicity, but in plants, this role is mostly fulfilled by MTs and PCs together (Cobbet

220 

and Goldsbrough, 2002). However, because plants have the capacity to bind metal ions through the thiol groups

221 

of their cysteine residues, it has recently been suggested that MTs are involved in the metal tolerance or

222 

homeostasis and scavenging of ROS in plants (Grennan, 2011; Saraswat and Rai, 2011; Leitenmaier and

223 

Kupper, 2013). MTs from several microorganisms have been studied, but the most characterized are those from

224 

the ciliated protist Tetrahymena. There are at least 16 MTs isoforms in T. pyriformis, T. thermophila, T.

225 

tropicalis, T. rostrata, T. pigmentosa, T. vorax, T. mobilis, and T. hegewischi, which have been classified into

226 

two groups: Cd2+-induced isoforms and Cu2+ induced isoforms (Domènech et al. 2008; Gutiérrez et al. 2011).

227 

The majority of these MTs are Cd2+ induced isoforms, although they also respond to Zn2+, Hg2+, Pb2+, As3+, Ni2+

228 

and ROS (Gutiérrez et al.2011; Guo et al. 2008). Bacteria having the greater metal binding capacity through

229 

metallothioneins possess the potential to accumulate or sequester heavy metals (Sessitsch et al. 2013).

230 

Metallothioneins encoding genes have been expressed in a diverse group of rhizobacteria for increasing the

231 

accumulation of toxic heavy metals (Sessitsch et al. 2013). For instance, metallothionein genes from the humans

232 

are expressed in Mesorhizobium huakuii spp. sub sp. rengi that upon inoculation to Astragalus sinicus resulted

233 

in the two-fold increase in the uptake of Cd (Sriprang et al. 2002). Beside peptides (phytochelators), plants also

234 

produce biosurfactants which consist of glycosides and polyphenols, generally found in many plant species, play

235 

and important role in metal removal because of acidic characteristics and presence of numerous functional

6   

236 

groups. There are evidences in the literature wherein different classes of biosurfactants like rhamnolipids

237 

(mainly synthesised by rhizobacterial community), saponins have been used for removal of heavy metals like

238 

Cu, Cd, Zn, Pb and As. Saponins are a class of natural biosurfactants and widely distributed in plant kingdom.

239 

Some natural saponins have been traditionally used as detergent for fabric washing, hair and body cleaning and

240 

in folk medicine. Whereas, rhamnolipids a class of biosurfactant mainly synthesised by the pseudomonad group

241 

bacterial strains in the rhizosphere.

242 

5. Role of rhizobacterial community in phytoremediation of heavy  

243 

Every plant has its specific microflora in the rhizosphere and this microflora plays an important role in plant

244 

growth promotion and heavy metal detoxification/removal as well. Rhizobacteria present on root surface helps

245 

in mineral uptake, contribute in essential vitamins, stomatal regulation, osmotic modification, and adaptation of

246 

root morphology (Bauer et al. 2013; Vacheron et al. 2013). These bacteria are known as plant growth promoting

247 

(PGP) rhizobacteria, have the potential to enhance pollutant tolerance and removal ability of plants, enhance

248 

biomass production and prevent phytopathogens from infecting plants, (Luo et al. 2012). Heavy metals present

249 

in the rhizospheric zone affect nutrient uptake and retards plant growth (Ouzounidou et al. 2006). Under such

250 

nutrient limiting conditions, PGP bacteria help in providing essential nutrients to plants. For example,

251 

Rhizobium leguminosarum bv. trifolii can fix nitrogen in the presence of heavy metals and support plant growth

252 

(Nonnoi et al. 2012). Chromium resistant Cellulosimicrobium funkei isolated from Phaseolus vulgaris

253 

rhizosphere solubilize PO4, produce IAA, EPS, ammonia, catalase, biosurfactant, protease, amylase, and lipase

254 

in the presence of chromium. The root elongation assay with C. funkei significantly increased root length in the

255 

presence of chromium (Karthik and Arulselvi 2017). Bacteria that assist in the remediation/detoxification of

256 

heavy metals can contribute to this process directly or indirectly. Direct mechanisms involves production of

257 

EPS, siderophore, metallothioneins, biosurfactants, organic acid, and phytochelatins, increases the

258 

bioavailability, solubility and accumulation of metals and indirectly by the improvement of plant growth and

259 

protection against pathogens that further facilitate the accumulation of heavy metals (Ullah et al. 2015; Shi et al.

260 

2016; Gupta and Kumar 2017), and by indirect mechanisms such as phosphate solubilization, siderophore

261 

production and production of growth hormones. Plant-associated rhizobacteria can also reduce heavy metal

262 

stress through the synthesis of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase which reduces the

263 

high levels of ethylene by consuming its immediate precursor, the ACC.

264 

The mechanism that lies behind this is: S-adenosyl methionine synthetase converts L-methionine to S-adenosyl

265 

methionine which is converted to 1-aminocyclopropane-1-carboxylate (ACC) by the activity of ACC synthetase.

266 

ACC oxidase further converts it to ethylene. Ethylene is important for normal plant developments as well as for

267 

their response to stress (Deikman, 1997). Under stressed conditions, stress ethylene is synthesized by the plant

268 

in response to the stresses like heavy metals, organic or inorganic chemicals, physical and biological stresses.

269 

According to one model, stress ethylene is synthesized in two peaks wherein the first peak is only a small

270 

fraction of the magnitude of the second ethylene peak. But the first peak which consumes the existing pool of 1-

271 

aminocyclopropane-1-carboxylate plays an important role in initiating the transcription of genes that encode

272 

plant defensive or protective proteins (Robison et al. 2001a). The second peak of ethylene is generally bigger in

273 

magnitude and is detrimental for plant growth and is involved in initiating processes of senescence, chlorosis

274 

and leaf abscission. The high levels of stress plant ethylene that is formed can significantly exacerbate the

7   

275 

effects of the stress and any mechanisms that can lower down the level of second peak of stress ethylene will

276 

decrease the damage to the plant that occurs due to stress. ACC deaminase enzyme activity of the plant growth

277 

promotory rhizobacteria is one such property which is helpful in combating ethylene stress.

278 

5.1. Rhizobacteria as a strong biosorbents

279 

Rhizobacteria makes excellent biosorbents in context of their high surface volume and a great substance of

280 

potentially active chemosorption sites, for instance, teichoic acids (TA) and teichuronic acids (TUA) in the cell

281 

wall of gram positive bacteria contains active chemical agents with sites capable of passively sequestering heavy

282 

metals (Fig. 3) (Naja and Volesky, 2011). They also contribute to plant metal uptake through sorption,

283 

mineralization and transformation mechanism (Ayangbenro and Babalola 2017).. Sorption with particular

284 

reference to metal ions can be defined as the process involved in the association of metal ions (ranging from

285 

electrostatic to covalent) with outer boundary available as one or more functional groups on sorbent materials

286 

(Gupta and Diwan 2017). When the sorbent engaged with such reaction is a biological agent, the process is

287 

defined as biosorption (Gupta and Diwan 2017). Biosorption of toxic heavy metals by rhizobacteria has been

288 

extensively studied by several researchers (Kim et al. 2015; Paredes-Páliz et al. 2016; Haq et al. 2016;

289 

Ayangbenro and Babalola 2017). For instance, Haq et al. (2016) isolated endophytic bacterium Kocuria

290 

rhizophila from Oxalis corniculata hyperaccumulator plant which was capable to adsorb Cadmium (II) and

291 

Chromium (III) upto 9.07 and 14.4 mg g-1 respectively. Surface complexation with ion exchange and micro

292 

precipitation are some other potential substitute technique currently used for toxic metal removal (Naja and

293 

Volesky 2011). Preferable surface structures available in bacteria and archaea are a crystalline proteinaceous

294 

surface layer called as S-layer, which attenuates the sorption ability of Gram-positive bacteria (Naja and

295 

Volesky 2011). Some recent study reported the sorption mechanism of various organic and inorganic Arsenic

296 

(As) species using Bacillus sp. (Hossain and Anantharaman 2006; Giri et al. 2014)Rhodococcus sp.

297 

Halobacterium sp. (Williams et al. 2013). A study showed that the sorption of As(III) metal ions on the

298 

extracellular surface of bacterial cell was 1.870 mg g-1 of dry cell weight. The adsorption was pH and

299 

temperature dependent and the maximum adsorption was found at pH 7 and at 20-30 °C temperature (Miyatake

300 

and Hayashi 2011). In a study carried out with Pb-resistant bacterium Bacillus megaterium for the biosorption

301 

of Pb, the maximum biosorption capacity (503.86 mg g-1) was achieved at optimum pH 7.2 (Li et al. 2017).

302 

Upadhyay et al. (2017) reported biosorption of Zn2+ (< 250μg mg-1) by fluorescent Pseudomonas strain Psd

303 

isolated from contaminated soil showing multiple PGP properties. Another study carried for biosorption of Cd2+

304 

and Zn2+ using three strains Tsukamurella paurometabola A155, Pseudomonas aeruginosa B237, and

305 

Cupriavidus taiwanensis E324 showed that the maximum adsorption capacity for Cd2+ and Zn2+ was 16.89 and

306 

16.75 mg g−1, respectively, under optimal conditions. The bioaccumulation experiment revealed that Cd2+ and

307 

Zn2+ were mainly adsorbed on the cell walls of these bacteria rather than accumulating inside the cells

308 

(Limcharoensuk et al. 2015). Particularly in case of rhizobacteria, heavy metal ions in both soluble as well as in

309 

complex form can potentially be accumulated by intact bacterial cells (live or dead) and their by-product’s

310 

(Alam and Ahmad 2013). Whole unimpaired microbial cell (live or dead) or their metabolite

311 

(exopolysaccharide) intervened biosorption of toxic heavy metal occurs by the interaction between positively

312 

charged metal ions and their contrarily charged exopolysaccharide and cell surfaces (Gupta and Diwan 2017).

313 

6.

Role of Rhizobacterial Exopolysaccharides in heavy metals phytoremediation

8   

314 

Exopolysaccharides (EPS) are a complex blend of high molecular weight biopolymeric metabolite secreted by

315 

bacteria, fungi, few plants and microalgae for protection against environmental stress. They not only protect cell

316 

against dewatering or toxic substances but serves as a carbon and energy source too (Gadd 2004; Gupta and

317 

Diwan 2017). EPS produced by rhizobacteria mainly consists of polysaccharides, proteins, humic substances,

318 

uronic acid, nucleic acid, lipids and glycoproteins surrounding the cells which bind metals (Das et al. 2009;

319 

Sheng et al. 2010). Different investigators have reported about a variety of rhizobacterial species and a diverse

320 

range of EPS (Table 2). Rasulov et al. (2013) reported the remediation efficiency of EPS produced by

321 

Azotobacter chroococcum strain XU1  up to 33.5 mg g-1 for Pb, and 38.9 mg g-1 for Hg respectively. The metal

322 

absorption behaviour of alginate (EPS) produced by Azotobacter in soil

323 

metals by creating micro-environment of essential metal ions to maintain soil ecology and accelerate the

324 

growth of the plant (Rasulov et al. 2013). In another report on biosorption of Cu2+ and Ag+ by

325 

exopolysaccharide produced by four marine bacterial strains, the maximum remediation were 400 mg g-1 EPS

326 

(6.29 mmol g-1) and 333 mg g-1 EPS (3.09 mmol g-1) for Cu2+ and Ag+, respectively (Deschatre et al. 2013).

327 

Another recent study was carried by Li et al. (2017) in which they showed the role of EPS in Ni2+ biosorption

328 

onto aerobic/anaerobic granular sludge. The maximum biosorption was achieved 65.77mg g-1 for aerobic sludge

329 

and 54.18 mg g-1 for anaerobic sludge respectively. Moreover EPS producing rhizobacteria increases root and

330 

shoot growth of wheat under drought stress (Hussain et al. 2014). EPS produced by rhizobia helps in the

331 

synthesis of biofilm where they get protection from environmental anomalies and may help the plants by

332 

extracting more water and nutrients (Vanderlinde et al. 2010). EPS also plays a significant role in metal

333 

complexation thereby reducing their bio-accessibility and bioavailability by infiltration of heavy metals (Wei et

334 

al. 2011; Gupta and Diwan 2017). Joshi and Juwarkar (2009) reported that the immobilization of Cd and Cr

335 

after inoculation of EPS-producing Azotobacter spp. was 15.2 mg gm-1 of Cd and 21.9 mg gm-1 of Cr. The

336 

tactics for achieving a significant amount of toxic heavy metal removal through bacterial EPS must be focused

337 

on utilizing the non-neutral, negatively charged EPS (EPS packed with abundant anionic functional groups) to

338 

be incorporated as a suitable biosorbent. Some of the reported commercial bacterial EPS with the required

339 

anionicity are alginate (Pseudomonas aeruginosa, Azotobacter vinelandii,), gellan (Sphingomonas

340 

paucimobilis), hyaluronan (Pseudomonas aeruginosa, Pasteurella multocida, Streptococci attenuated strains),

341 

xanthan (Xanthomonas campestris), galactopol (Pseudomonas oleovorans), fucopol (Enterobacter A47)

342 

(Freitas, F., 2011; Öner, E. T. 2013). EPS with different chemical compositions were tested for their ability to

343 

sorbed mercury, and it was observed that the EPS containing hexosamines was most effective in removing

344 

mercury from the solution whereas EPS consisting neutral sugars removed the least amount of mercury from the

345 

solution (Cruz 2014). It was revealed that the EPS produced by Ni-resistant Cupriavidus pauculus bacteria

346 

isolated from serpentine soil was a homopolymer of rhamnose containing uronic acid, protein, and nucleic acid

347 

(Pal and Paul 2013). Unimpaired whole microbial cells and additionally cell bound EPS, have discovered broad

348 

application for metal remediation in industrial as well as environmental wastewater sources (Kumar 2016) (Fig.

349 

2).

350 

helps in the remediation of toxic

6.1. Interaction mechanism between exopolysaccharide and heavy metal ions

351 

The interaction between EPS and heavy metal appears very complex in the form of electrostatic attraction in

352 

which surface complex formation and chemical interaction between heavy metal ions and the functional groups

353 

of EPS occurs (Dobrowolski et al. 2017). It has been reported that due to the presence of acyl group, EPS shows

9   

354 

anionic property, which increases the interaction with other cationic heavy metals (Cd2+, Pb2+, Co2+ and Ni2+)

355 

and forms EPS-metal complex (Kaushal and Wani 2016). Generally, EPS produced by rhizobacteria depicts a

356 

strong binding capacity to heavy metals and entrap precipitated metal sulphides and oxides, leading to the

357 

development of EPS-metal complexes and subsequently enhancing the heavy metal remediation (Joshi and

358 

Juwarkar, 2009; Xu et al., 2012). In a study carried by Xu et al. (2012), EPS produced by Pseudomonas putida

359 

transformed the bioavailability of Cd2+ into organic species by means of complexation. Carboxyl and phosphate

360 

groups were mainly responsible for the Cd2+ binding ability of EPS produced by Pseudomonas putida (Wei et

361 

al. 2011). Moreover, electrostatic interaction seems to be the major mechanism through which EPS helps in the

362 

remediation of heavy metals. This interaction is mainly attributed to competition between divalent and trivalent

363 

cations; trivalent cations directly competed with divalent cations for EPS binding sites. Trivalent cations were

364 

more competitive than divalent cations for binding because they formed more strong bonds with EPS (Yan et al.

365 

2017). The strength of interactions between the particular surface groups (mainly hydroxyl, acetamido or amino

366 

groups) and the metal ions depends on the type and activity of adsorption centre and the ion properties

367 

(Dobrowolski et al. 2017). Recently a thermodynamic study carried out on the interaction between EPS and

368 

heavy metal ions showed that the binding between heavy metals and EPS was spontaneous and driven mainly by

369 

enthalpy change. Environmental factors have also significant impact on the adsorption performance (Yan et al.

370 

2017). Another study on the interaction of EPS and Ni2+ showed a stable operation of the granular sludge-based

371 

system, influencing the microbial activity and surface characteristics of sludge (Li N, et al. 2017). Moreover, it

372 

is well reported that EPS have a high binding ability for heavy metal due to their abundant functional groups

373 

(e.g., carboxyl and hydroxyl groups).

374 

7. Role of Rhizobacterial biosurfactants

375 

Biosurfactants (surface active agents contain hydrophilic and hydrophobic groups produced by a variety of

376 

microorganisms) have a wide application in metal remediation (Singh and Cameotra 2013; Mao et al. 2015;

377 

Camargo et al. 2016; Govarthanan et al. 2017; Mulligan, C. N. 2017). A majority of rhizobacteria produce

378 

biosurfactants and release to the host niches as metabolic products (Table 2) (Bolan et al. 2014; Das and Kumar

379 

2016; Agnello et al. 2016). The secreted biosurfactants initially interact and develop a complex with different

380 

insoluble heavy metals on the interface of rhizosphere soil particles, and then induce desorption of metals from

381 

soil matrix, leading to the alteration of metal mobility and bioavailability by increasing metal solubility in the

382 

soil environment (Rajkumar et al. 2009). In soil, biosurfactant debilitate the strong bonds between soil and

383 

metal, hence accelerates the desorption of heavy metals from solid phases either by complexation of free forms

384 

of metal residing in solution that decreases the solution phase activity of the metal and, therefore, promotes

385 

desorption (Le Chatelier’s principle) or reduced interfacial tension through solid solution interface that allows

386 

direct contact of biosurfactants to sorbed metal at solid solution (Ahemad 2015; Das et al. 2016) (Fig. 2). In

387 

addition, there are many factors present in soil environment that may affect the biosurfactant activity such as

388 

pore size, charge present on soil particles, soil pH, soil composition, particle size, time and type of

389 

contamination plays a major role in establishing the effectiveness of biosurfactants action (Sarubbo et al. 2015).

390 

Bioremediation of heavy metal-contaminated soil with the help of biosurfactants mainly depends on their ability

391 

to form complexes with metals. Heavy metal ions in soil surfaces can be eliminated by the biosurfactant

392 

micelles (Juwarkar et al. 2007; Asci et al. 2008). Some reports from the work done in last few years which

393 

annotate the significant contribution of biosurfactants in the bioremediation of heavy metal contaminated soils

10   

394 

are discussed here. A study carried by Barajas-Aceves et al. (2015) reported, irrigation with crude biosurfactants

395 

had no effect on heavy metal accumulation in the plants but they suggested that increasing the irrigation time

396 

with crude biosurfactants would have a positive effect on heavy metal accumulation in the roots or shoots. A

397 

study carried by Sheng et al. (2008) showed biosurfactant producing Bacillus sp. have the capability to promote

398 

plant growth and cadmium uptake of rape, maize, Sudangrass and tomato in soil contaminated with different

399 

levels of Cd. Singh and Cameotra (2013) reported similar investigation with Bacillus subtilis producing

400 

lipopeptide biosurfactants, that removed a significant amount of metals; Cadmium (44.2 %), Cobalt (35.4 %),

401 

Lead (40.3 %), Nickel (32.2 %), Copper (26.2 %) and Zinc (32.07 %). Dahrazma and Mulligan (2007), reported

402 

that rhamnolipids have the ability to remove the overwhelming amount of heavy metals from soil sediments; the

403 

removal percentage of various heavy metals were up to 37% of Cu, 13% of Zn, and 27% of Ni when the

404 

biosurfactants were applied in a continuous flow configuration. Presence of rhamnolipids, enhanced recovery of

405 

Cd2+ from kaolin, a soil component (Asci et al. 2008). Even the surfactant solution and rhamnolipid foam could

406 

remove 11% of Cd and 17% of Ni (Wang and Mulligan 2004).

407 

7.1 Biosurfactant and heavy metal interaction mechanisms

408 

Biosurfactant exhibit a tendency to interact with heavy metals in soil through van der Waals force (the

409 

attractive or repulsive interaction between metal ions and biosurfactant). Besides this, an

410 

electrostatic interaction between biosurfactant and heavy metals is involved in which counter ion

411 

binding, precipitation-dissolution, and ion exchange type of interactions occur. The basic

412 

phenomenon in metal contaminated soils is; biosurfactant form complex with heavy metals which

413 

in turn decreases the solution phase activity of the metal that promotes the desorption of metals

414 

(Le-Chatelier’s principle) consequently they may easily be available for the plant growth

415 

(Olaniran et al. 2013; Gupta and Kumar 2017). Another mechanism can be wherein biosurfactant

416 

can accumulate metals in contaminated soil under the conditions of reduced interfacial tension and

417 

can bind to heavy metals directly, and can accumulate metals at the solid-solution interface. This

418 

may allow direct contact between biosurfactant and heavy metal (Açıkel 2011). In addition, the

419 

ionic form of biosurfactant can increase the sorption capacity of heavy metal ions, for example,

420 

anionic surfactants have more capacity to form a complex with metal ions by surface sorption of

421 

complexation or precipitation of the complexes. While in case of cationic surfactants they

422 

decrease the metal-metal interaction by competition for some but not all anionic surfaces (Açıkel

423 

2011). In soil, biosurfactant may increase the entropy of soil-metal complex system consequently

424 

weakening the bond between metal and soil; hence increasing the metal bioavailability in soil

425 

wherein roots can absorb easily (Fig. 3). In addition, biosurfactant can also facilitate the transport

426 

of aquaphobic pollutants into aqueous phase through specific interaction by solubilization and

427 

micellization of contaminants (Costa et al. 2010). These micellized and solubilized contaminant

428 

subsequently allows removal of heavy metals either by soil flushing or makes them easily

429 

available for plants (Maier and Soberón-Chávez 2000). Moreover, some heteroatoms and active

430 

chemical groups, (e.g. hydroxyl, carbonyl, or amine) are generally present in the structure of

431 

biosurfactants which take part in the process of forming complexes with heavy metals. This

432 

procedure empowers removal of heavy metal ions and may upgrade their extraction efficiency by

11   

433 

utilizing biological methods (Lawniczak et al. 2013).7.2 Relevance of biosurfactant in heavy

434 

metal remediation

435 

Biosurfactant assisted remediation of heavy metals from metal contaminated soil has been proposed as a

436 

potential approach in recent years (Govarthanan et al. 2017). The phytoremediation ability of plants in the

437 

removal of heavy metals from contaminated sites can be enhanced by inoculation of heavy metal resistant plant

438 

growth promoting and biosurfactant producing rhizobacterial strains. In this context, studies were conducted by

439 

researchers. A study was conducted by  Chen et al. (2014) on  Solanum nigrum L. in cadmium contaminated soil

440 

to check the potential of endophytic Pseudomonas sp. Lk9 (biosurfactant producing) on cadmium uptake and

441 

growth promotion of Solanum nigrum L. The study showed that Lk9 inoculation enhances the cadmium

442 

availability and significantly increases S. nigrum shoot dry biomass by 14% and the total of Cd by 46.6% mg kg-

443 

1

444 

Pseudomonas koreensis AGB-1 was reported by Babu et al. (2015) on the growth promotion of Miscanthus

445 

sinensis and remediation of As, Cd, Cu, Pb, and Zn. The study revealed that Miscanthus sinensis inoculated by

446 

Pseudomonas koreensis AGB-1  increased biomass by 54% as well as enhanced metals concentrations in roots

447 

and shoots. Another similar study on rape, maize, sudangrass and tomato in cadmium contaminated soils was

448 

undertaken to investigate the potential of Bacillus sp. J119 (biosurfactant producing) on plant growth and

449 

cadmium uptake by the plants. The study showed that the bacteria successfully colonized in the rhizosphere of

450 

experimental plants, enhancing biomass production in all cases while cadmium uptake was reported only in case

451 

of tomato plant (Sheng et al. 2008). Another study was conducted on the metal speciation by biosurfactant

452 

producing Bacillus subtilis, Pseudomonas aeruginosa, and Pseudomonas fluorescence. The study revealed that

453 

the strain P. aeruginosa contained higher metal exchangeable fraction concentrations in comparison to other

454 

strains (Braud et al 2006). Hence, it can be considered that biosurfactant producing heavy metal resistant

455 

rhizobacterial strains are more suited for colonization of plant roots and metal remediation.

456 

Apart from this, biosurfactant producing PGP rhizobacteria also have been reported in regulating a number of

457 

physiochemical processes of plants including micronutrient uptake, osmotic modifications, stomatal regulation,

458 

and alterations in root morphology (Do Amaral et al. 2016; Ma et al. 2016a). Rhizospheric microorganisms

459 

possess potential to degrade inorganic and organic pollutants through rhizodegradation, transformation and

460 

volatilization (Ullah et al. 2015b). They can mobilize metals through biomethylation (transfer a methyl group to

461 

the metals) resulting in methylated metal species which may differ in volatility, solubility and toxicity and are

462 

often lost from the soil (Bolan et al. 2014). So, overall effect of rhizospheric microbial population on plant

463 

growth seems to be beneficial as well as in combating heavy metal stress in the environment.

464 

that is accumulated in aerial parts. Another study on biosurfactant producing multimetal resistant endophyte

7.

Conclusion and future prospects:

465 

The attribute of life on earth is linked insurmountable to the overall quality of the environment. Today various

466 

anthropogenic activities have added various heavy metals in our environment to the large scale. Exploitation of

467 

Plant-metal-microbe interaction technology by exploring the mechanisms behind the plant and rhizospheric

468 

microbes may be useful in the remediation of heavy metal contaminated soil. Moreover, rhizobacteria producing

469 

biosurfactant and exopolysaccharide have an interesting role in the remediation of heavy metal contaminated

470 

soil owing to their low-cost, less toxicity, biodegradability, and sustainable application and cost-effective

471 

production from renewable substrates (agro-industrial wastes). Apart from this, the technology may diminish the

472 

level of such toxic metal pollutants from the environment at mass scale using PGP bacteria and plant

12   

473 

interactions in nature everywhere. Using more emerging biotechnological tools we can develop a new model for

474 

the complete removal or detoxification of heavy metals. Hence, we can conclude that rhizobacterial mechanisms

475 

can open up a new vista in the remediation of heavy metals contaminated soils. Therefore, more research be

476 

carried out in this area for more successful implementation of rhizobacterial strains with these properties for

477 

heavy metal contaminated soil remediation.

478  479  480  481 

Acknowledgement: Research grant no. NFSC/2017-18/SC/UTT/29727 received from University Grant

482 

Commission, New Delhi, India to support this study is duly acknowledged.

483  484  485  486  487  488  489  490  491  492  493  494  495  496  497  498  499  500  501  502 

13   

503  504 

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32   

Table: 1. Different heavy metals and their effects on human health Heavy metals

EPA regulatory limit (ppm)

Arsenic (As)

0.01

Cadmium (Cd)

5.0

Chromium (Cr)

0.1

Copper (Cu)

0.3

Mercury (Hg)

2.0

Lead (Pb)

15.0

Zinc (Zn)

Nickel (Ni)

0.5

0.2 (WHO permissible limit)

Toxic Effects on Various body part affects through essential cellular processes such as oxidative phosphorylation and ATP synthesis and cause Brain damage, cardiovascular, conjunctivitis, dermatitis, perforation of nasal septum, respiration cancer, peripheral neuropathy, dermatosis, skin cancer Carcinogenic, mutagenic, and teratogenic; endocrine disruptor; interferes with calcium regulation in biological systems; causes renal failure, coughing, emphysema(COPD), headache, hypertension, itai-itai, lung and prostate cancer, lymphocytosis, microcytic hypochromic anemia, testicular atrophy, osteoporosis and fractures causes dizziness, fatigue, bronchopneumonia, chronic bronchitis, diarrhea, emphysema, headache, irritation of the skin, itching of the respiratory tract, liver diseases, lung cancer, nausea, renal failure, reproductive toxicity, vomiting Damage brain and kidney, liver cirrhosis and chronic anemia, stomach and intestinal irritation Ataxia, attention deficit, blindness, deafness, decrease rate of fertility, dementia, dizziness, dysphasia, gastrointestinal irritation, gingivitis, kidney problem, loss of memory, pulmonary edema, reduced immunity, sclerosis, damage to brain, kidney, and developing foetus causes impaired development, Anorexia, chronic nephropathy, damage to neurons, hyperactivity, insomnia, renal failure Overdosage causes dizziness, fatigue, ataxia, depression, gastrointestinal irritation, hematuria, icterus, impotence, kidney and liver failure, lethargy, macular degeneration, metal fume fever, prostate cancer, seizures, vomiting Allergic dermatitis known as nickel itch; inhalation can cause cancer of the lungs, nose, and sinuses; cancers of the throat and stomach have also been attributed to its inhalation; hepatotoxic, immunotoxic, neurotoxic, genotoxic, reproductive toxic, pulmonary toxic, nephrotoxic, and hepatotoxic; causes hair loss

References Tripathi et al. (2007), Singh et al. (2011)

Koedrith et al. (2013), Sughis et al. (2011), James and Meliker, (2013), Yang et al. (2013)

Salem et al. (2000), Bagchi et al.(2002) Salem et al. (2000), Wuana and Okieimen (2011), Singh et al. (2011) Johansson et al. (2007), Jaishkanker et al. (2014), Park, J.D., Zheng, W., 2012, Salem et al., (2000), Lam et al., (2007) Wuana and Okieimen (2011) Eisler (2000) DamekPoprawa, et al. (2003). Ayangbenro et al. (2017) Schaumlöffel (2012), Salem et al. (2000),   Das et al. (2008)

Table: 2. Exopolysaccharide producing bacteria from contaminated soil and rhizosphere Types of EPS   

Source/Origin  Soil 

Bacterial species Bacillus sp. CIK-516 and Stenotrophomonas sp. CIK-517Y 

Heavy metal Nickel

 

Mangrove rhizosphere 

Arsenic

alginate 

Soil 

Kocuria flava AB402 and Bacillus vietnamensis AB403 Fluorescent Pseudomonas strain Psd

Gram negative microbial consortia

Zinc Zinc, lead, Chromium, Nickel, Copper, Cadmium Cobalt Lead, Mercury

 

 

Azotobacter chroococcum 

 

 

Lactobacillus plantarum

Lead

 

 

Ensifer meliloti

Lead, Nickel, Zinc 

Homogenous consortial EPS 

Soil isolates 

Bacillus firmus

Lead, Copper, Zinc

GRAS status

Paenibacillus jamilae

Lead, Cadmium

PGPR consortia

Gordonia alkanivorans strains SMV185.1, SMV185.5, SMV207.37, Macrococcos caseolysticus and Lysinibacillus macrolides Cellulosimicrobium funkei AR8, Cellulosimicrobium funkei AR6,

Arsenic, Mercury

PGPR consotia

Chromium

EPS mediated synthesized CdS nanoparticle Agar Beads immobilized Hydrocarbon contaminated water microbial consortium 

Pseudomonas aeruginosa JP-11

Cadmium

Paenibacillus polymyxa

Lead

 

 

Paenibacillus polymyxa

   

 

  Paracoccus sp., Alteromonas sp., Vibrio sp., Vibrio diabolicus, Pseudoalteromonas sp., Alteromonas sp. 

 

Marine

Heterogenus

Activated

 

Microbial mats and Deep sea hydrothermal vents 

Zinc, Copper, Cadmium

Paracoccus sp., Alteromonas sp, Vibrio sp

sludge

Removal efficiency  Maximum accumulation of Ni 609 mg kg_1dry weight tolerate 35mM and 20mM of arsenite respectively 

Copper

Mercury

Copper and Silver

Zinc,

Copper,

75 to 78% reduction in metal load  40.48% Pb2+(33.5 mg Pb2+/g of EPS); 47.87% Hg2+ (38.9 mg of Hg/g EPS)  276.44 mg Pb2+/g EPS, at 1000 ppm initial metal load 89% Pb2+, 85% Ni2+, 66% Zn2+ reduction from 50 ppm initial load  1103 mg Pb2+/g EPS (98.3 %,), 860 mg Cu2+/g EPS (74.9%), 722 mg Zn2+/g EPS (61.8%) 200 - 300 mg Pb2+/g EPS, 21 mg Cd2+/g of EPS 85% for As5+, As3+, 45% for Hg2+

Reference Akhtar et al. (2018) 

Mallick et al. (2018) 

Upadhyay et al. (2017) Gawali et al. (2014)

Rasulov et al. (2013) 

Feng et al. (2012)

Lakzian et al. (2008) 

Salehizadeh, and Shojaosadati, (2003)

Morillo (2006)

et

al.

Franchi (2017)

et

al.

EPS to 14.79 and 5.89% in 50 lg/mL of Cr6+ treated AR6 and AR8 strains, respectively. 88.66% form aqueous solution

Karthik (2016)

et

al.

111.11 mg Pb2+/g EPS 87.12% Cd2+; 19.82% of Zn2+; 37.64% of Cu2+ reduction from 1 ppm initial metal load 1602 mg Cu2+/g EPS

Hassiba et (2014) Martins et al. (2008)

uptake capacities ranged from 0.005 to 0.454mM Hg/g for the different EPS(sorbed upto 82%) 400mg g-1 EPS (6.29 mM g-1) for Cu2+ and 333 mg g1 EPS (3.09 mM g1 ) for Ag2+ 85 to 95%

Raj et al. (2016)

al.

Acosta et al. (2005).    Cruz et al. (2017)

Deschatre et al. (2013)

Liu et al. (2001)

consortial EPS

mixed consortia

Dead biomass EPS

Dead biomass EPS

Bacillus cereus, Bacillus pumilus, Pantoea agglomerans

Chromium

Ochrobactrum anthropi

Chromium, Cadmium, Copper

Pseudomonas putida, Rhizobium alamii

Cadmium

Phosphorylated bacterial EPS (cellulose)

Acetobacter

Lead, Copper, Manganese, Zinc, Cobalt

Alginate bead immobilized

Chryseomonas luteola

Cadmium, Cobalt, Copper, Nickel

Activated isolate

sludge

Modified EPS

Immobilized EPS

Chromium Cadmium

reduction from initial metal load of 10-100 ppm 89.87%, 89.23%, 85.5% reduction from initial metal load of 50 ppm 57.8 mg Cr6+/g EPS at initial metal load of 280 ppm, 26 mg Cu2+/g EPS at initial metal load of 91.6 ppm 29.5 mg Cd2+/g EPS at 100.6 ppm initial metal load N.A.

90% reduction from initial metal load of 0.1mM/dm3 (Fe3+ > Cu2+> Mn2+ >Zn2+; Co2+) 64.10mg Cd2+/g EPS 55.25mg Co2+/g of EPS 1.989mM EPS Cu2+/g 1.224mM Ni2+/g EPS

Mubashar and Faisal (2012)

Ozdemir (2003)

et

al.

Xu et al. (2012), Wei et al. (2011), Schue et al. (2011). Oshima et al. (2008)

Ozdemir (2005a) Ozdemir (2005b)

et

al.

et

al.

Table: 3. List of biosurfactant producing rhizobacteria from contaminated environment Microorganism

Source Parthenium hysterophorus rhizosphere (Metal contaminated) heavy metal contaminated soil

References Singh and Cameotra (2013)

Pseudomonas aeruginosa

Indigenous flora of apple; petroleum contaminated soil

Abbasi et al. (2012); Kumar et al. (2012)

Bacillus cereus, Bacillus megaterium, B. thuringiensis

Land farming soil

Cerqueira et al. (2012)

Stenotrophomonas maltophilia Psuedomonas nitroreducens Acinetobacter sp. Staphylococcus sp. Pseudomonas sp.

Land farming soil Petroleum-contaminated soil Petroleum-contaminated soil Crude oil-contaminated soil Crude oil-contaminated soil

Cerqueira et al. (2012) Onwosi and Odibo (2012) Chen et al. (2012) Eddouaouda et al. (2012) Hua and Wang (2012)

Pseudomonas aeruginosa Bacillus cereus

Petrochemical waste-contaminated soil

Cerqueira et al. (2011)

Bacillus subtilis

Endosulfan sprayed cashew plantation soil containing hydrophobic substances

Sekhon et al. (2011)

Serratia marcescens

Hydrocarbon-contaminated soil

Roldán-Carrillo et al. (2011)

Enterobacter cloacae Pseudomonas sp.

Heavy crude oil-contaminated soil

Darvishi et al. (2011)

Streptomyces rochei Pseudomonas fluorescens Pseudomonas aeruginosa Rhodococcus fascaians Bacillus subtilis Bacillus mojavensis

Heavy crude oil-contaminated soil Rhizosphere of fique Petroleum-contaminated soil Antarctic soil Soil Endophytic bacteria from maize

Chaudhary et al. (2011) Sastoque-Cala et al. (2010) Nie et al. (2010) Gesheva et al. (2010) Kim et al. (2010) Snook et al. (2009) Coppotelli et al. (2010)

Pseudomonas aeruginosa A11 Fluorescent Pseudomonads

Sphingomonas paucimobilis

Phenanthrene-contaminated soil microcosm

Pseudomonas sp Pseudomonas sp. Pseudomonas putida Pseudomonas aeruginosa Burkholderia cenocepacia Rhodococcus wratislaviensis Nocardia otitidiscaviarium Pseudomonas aeuroginosa Pantoea sp. Pseudomonas aeruginosa Bacillus subtilis Pseudomonas sp. Pseudomonas chlororaphis Acinetobacter junii Pseudomonas fluorescens Flavobacterium sp. Bacillus sp. Pseudomonas fluorescens

Agriculture soil Oil-contaminated soil Rhizosphere of black pepper Oil-contaminated soil Fuel oil-contaminated soil Soil Contaminated soil Diesel-contaminated soil Ornithogenic soil of Antarctica Petroleum oil-contaminated soil Rhizosphere of white and red cocoyam plants Soil Long Beach Soil Sugar beet rhizosphere Hydrocarbon/metal-contaminated soil Soil Petroleum-contaminated soil

Verma et al. (2015)

Singh et al. (2009) Cameotra and Singh (2009) Kruijt et al. 2009 de Lima et al. (2009) Wattanaphon et al. (2008) Tuleva et al. (2008) Zeinali et al. (2007) Chen et al. (2007) Vasileva-Tonkova and Gesheva (2007) Das and Mukherjee (2007) Perneel et al. (2007) Gunther et al. (2005) Menezes Bento et al. (2005) Nielsen and Sorensen (2003) Bodour et al. (2003) Takeyama et al. (2002) Barathi and Vasudevan (2001)

    

MERCURY

     

Production of ROS O**, OH, NO, RO*, ONOO*, H2O2

   

SOD, GSH, GST, Catalase

NICKEL

 

Defence by Antioxidants

      Fig: 1a.Effect of heavy metals on cell and the balance between ROS production and the subsequent defence mechanism presented by antioxidants (Edited after Jaishankar et al. 2014).

               

   

H HM

   

Trannslation defeects decreasee protein sy ynthesis

IImpaired DN NA repair & maintenan ance of telomerrase altered d methylatioon

     

RN NA Hydrolyssis

Inhibitition of Proteein and iion channelss

MDA A Muutations altereed genne expressio on

Base adduct

Lipid d

RNA R

Oxidative dam mage

DNA

Protein n

Depletted antioxidants impairred ROS R detoxification

ROS S Oxidative stress s Fig: 1b. Different D routees of Heavy M Metal (HM) to oxicity in vario ous metabolic pathways

Fig: 2. M Microbial surffactants and ex xopolysaccharride assisted mechanism off heavy metal r emediation by b Plants.

Figure 3.. Rhizobacteria showing a strong biosoorbents: (A) SEM-EDS S image of rhizobbacteria produ ucing EPS showing Cd (Red circcle) biosorptio on (Different E EDS peak of Cadmium meetal in variouss shell). (B) SEM-EDS S image off rhizobacteriaa showing Leead (Pb in re d circle) biossorption at different compoonent of cell wall. (C) SEM-ED DS image speectra of rhizo obacteria show wing Chromiium (Cr in red circle)) bbiosorption in different componeents of their ceell wall

F Fig: 4. Mechannism of biosurrfactant activiity in metal-co ontaminated so oil (Source M ulligan 2004 4).