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Goyal P, Belapurkar P, Kar A. A Review on In Vitro and In Vivo Bioremediation Potential of Environmental and Probiotic Species of Bacillus and Other Probiotic Microorganisms for two Heavy Metals, Cadmium and Nickel. Biosci Biotech Res Asia 2019;16(1).
Manuscript received on : 28-Jan-2019
Manuscript accepted on : 28-March-19
Published online on:  25-03-2019

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A Review on In Vitro and In Vivo Bioremediation Potential of Environmental and Probiotic Species of Bacillus and Other Probiotic Microorganisms for two Heavy Metals, Cadmium and Nickel

Pragya Goyal1, Pranoti Belapurkar*and Anand Kar3

1Department of Biotechnology, IPS Academy, Indore, Madhya Pradesh, India.

2Department of Biosciences, AIMSR, Mangliya, Indore, Madhya Pradesh, India.

3School of Life Sciences, Devi Ahilya Vishwavidyalaya, Indore, Madhya Pradesh, India.

Corresponding Author E-mail: pranotibelapurkar@acropolis.in

DOI : http://dx.doi.org/10.13005/bbra/2714

ABSTRACT: Microbial assisted remediation is the ray of hope in the current scenario of tremendous heavy metal pollution. The indiscriminate release of heavy metal laden industrial effluents in the water bodies and soil is now manifesting itself in the form of life threatening health hazards to humans. The conventional heavy metal remediation strategies are not only expensive but are ineffective in low metal concentrations. Microbial assisted remediation of heavy metals has come forward as the cheap and easy alternative. Amongst the various bacterial genera actively involved in bioremediation of cadmium and nickel in the environment, genus Bacillus has shown remarkable ability in this respect owing to its various biochemical and genetic pathways. It can perform bioremediation using multiple mechanisms including biosorption and bioaccumulation. This genus has also been able to reduce toxicity caused by cadmium and nickel in eukaryotic cell lines and in mice, a property also found in probiotic genera like Lactobacillus and Bifidobacterium. This paper reviews the role of environmentally present and known probiotic species of genus Bacillus along with different probiotic genera for their various mechanisms involved for remediation of cadmium and nickel.

KEYWORDS: Bacillus; Bioremediation; Cadmium; Nickel; Probiotic

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Goyal P, Belapurkar P, Kar A. A Review on In Vitro and In Vivo Bioremediation Potential of Environmental and Probiotic Species of Bacillus and Other Probiotic Microorganisms for two Heavy Metals, Cadmium and Nickel. Biosci Biotech Res Asia 2019;16(1).

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Goyal P, Belapurkar P, Kar A. A Review on In Vitro and In Vivo Bioremediation Potential of Environmental and Probiotic Species of Bacillus and Other Probiotic Microorganisms for two Heavy Metals, Cadmium and Nickel. Biosci Biotech Res Asia 2019;16(1). Available from: https://bit.ly/2VK8qNN

Introduction

Humans have been using various metals for their day-to-day activities for a very long time. However, it was the industrial revolution which caused the heavy metal contamination of water bodies and soil. This problem has been compounded by rapid urbanization and industrialization. Other sources of heavy metals such as nickel, chromium, cadmium, mercury, arsenic and lead include natural environmental causes like volcanic eruptions and agricultural residues (He et al., 2005). Their concentration is found highest at their point sources, i.e. all metal based industrial operations (Fergusson, 1990; Bradl, 2005; He et al., 2005). The presence of heavy metals is a cause of concern as they are highly toxic, non- biodegradable and have exceptionally long half-lives (Aiking et al., 1984). These heavy metals enter the food chain and reach top level by bioconcentration, bioaccumulation and biomagnification phenomena, thereby affecting the human health adversely (Ahmed et al., 2017). Their deleterious effects are found in both adults and children, and include disorders of heart, kidneys, reproductive system, nervous system and skeletal system (Jaishankar et al., 2014). In extreme cases, may also cause death.

Currently, the cause of worry is the fact that conventional technologies for removal of heavy metals from environment such as chemical precipitation, electrochemical treatment and ion exchange are not only proving expensive but are also not useful if the heavy metal concentration is low. The alternative technology to this is bioremediation which is proving beneficial due to its low cost of running and maintenance and ease of operation (Chaney et al., 1997; Chang et al., 1997; Chaney et al., 2000; Borma et al., 2003; Borrok et al., 2004). Overtime, microbes have developed different mechanisms to survive and tolerate heavy metals found in soil sediments and aquatic ecosystems. These mechanisms include bioaccumulation, biotransformation and biosorption amongst various other approaches. The predominant bacterial genera identified for bioremediation of heavy metals by various biochemical and genetic pathways are Bacillus, Pseudomonas and Enterobacter (Table 1). These microbes present to us important means of reducing heavy metal concentration and thus their toxicity in the environment.

In recent times microbiologists have reported that probiotic microorganisms like Lactobacillus sp. have the ability to detoxify heavy metals in vitro and in vivo (Table 2). This led to search for species of other bacterial genera having similar capacity. Genus Bacillus fits this criterion as some of its species have shown excellent heavy metal bioremediation potential in environment while others have exhibited probiotic property along with the ability to reduce heavy metal concentration in vitro as well as in vivo (Table 2). This review focuses on bioremediation of nickel and cadmium by Bacillus sp. and probiotic bacterial species.

Table 1: Various bacterial genera performing bioremediation of different heavy metals.

S. No. Genus Species Heavy metal References
1 Bacillus licheniformis Pb, Cr, Cu Syed and Chinthala, 2015
Cu, Cd, Zn Issazadeh et al., 2011
cereus Pb, Cr, Cu Syed and Chinthala, 2015
Cu, Cd, Zn Issazadeh et al., 2011
subtilis Pb, Cr, Cu Syed and Chinthala, 2015
Pb, Cu, Cd, Zn Issazadeh et al., 2011
Hg, Cd Imam et al., 2016
carotarum Pb, Zn, Cr Gupta et al., 2014
lentus Pb, Zn, Cr Gupta et al., 2014
thuriengiensis Zn, Pb Singh et al., 2015
amyloliquefacians Cd, Zn, Cu, Pb Issazadeh et al., 2011
sphaericus Cu, Ni, Cr Al-Daghistani, 2012
pumilus Cu, Ni, Cr Al-Daghistani, 2012
megaterium Cu, Fe, Zn, Mn Stefanescu, 2015
2 Escherichia coli Zn, Cu, Cd, Hg Vijayadeep and Sastry, 2014
Zn, Cd, Cr, Ni Oaikhena et al., 2016
3 Pseudomonas aeroginosa Cu, Cr, Fe, Zn Awasthi et al., 2015
Cu, Cr, Zn, Pb, Co, Cd, Hg, Ni Haroun et al., 2017
fluorescens Pb, Zn Meliani and Bensoltane, 2016
putida Zn, Cd, Co, Ni, Cu, Cd Bhojiya and Joshi, 2016
Fe, Mn Khedr et al., 2015
4 Proteus vulgaris Cd, Cr, Ni, Zn Oaikhena et al., 2016
5 Klebsiella pneumoniae Cd, Cr, Ni, Zn Oaikhena et al., 2016
6 Enterobacter cloacae Pb, Cd, Ni Banerjee et al., 2015
arburiae Cd, Ni Bhagat et al., 2016

Table 2: Various probiotic bacterial genera performing bioremediation of different heavy metals.

S. No. Genus Species Heavy metal References
1 Lactobacillus plantarum Cd, Pb Kirillova et al., 2017
Cr Wu et al., 2017
fermentum Cd, Pb Kirillova et al., 2017
casei Cd, Pb, Ni Ogunnusi and Oyetunji, 2017
paracasei Cd, Hg, Pb, Be, As Fang et al., 2018
acidophilus Cd, Hg, Pb, Be, As Fang et al., 2018
reuteri Cd, Hg, Pb, Be, As Fang et al., 2018
rhamnosus Cd, Hg, Pb, Be, As Fang et al., 2018
kefir Cd Gerbino et al., 2014
2 Bifidobacterium longum Cd, Hg, Pb, Be, As Fang et al., 2018
lactis Cd Halttunen et al., 2007
3 Bacillus coagulans Cr, Pb, Belapurkar et al., 2016
Ni Belapurkar et al., 2018
Cd Majlesi et al., 2016
clausii Pb, Zn Aleksey et al., 2014

 

Cadmium [Cd (II)]

Toxicity of Cadmium

Cadmium is a naturally occurring element existing in earth’s crust that is generally complexed with zinc or lead compounds (Hans Wedepohl, 1995). Commercially, it is used in the production of TV screens, batteries, paints, alloys etc. Industry workers are continually exposed to high levels of cadmium where it enters their body both by inhalation and ingestion (Nordberg et al., 2007). The effluents of these industries make their way to agricultural lands where it contaminates the crop and ultimately reach the rest of the human population (Rani et al., 2014). Another widespread source of cadmium is tobacco smoke (Friberg, 1983). The fact that the clearance half-life of cadmium from human body is 25 years (Bernhoft, 2013; Aflanie et al., 2015) makes it all the more hazardous.

Once cadmium enters into blood, it binds to sulfhydryl group- containing protein e.g. metallothionein (Bernhoft, 2013). Within the human body it causes various disorders related to its toxicity, ranging from oxidative stress (Cuypers et al., 2010; Matovi´c et al., 2011; Patra et al., 2011), depletion of glutathione to osteoporosis, anaemia, eosinophilia and cancer (Valko et al., 2005). In fact, cadmium has been classified as a type I carcinogen by International Agency for Cancer Research (IARC, 1993, Arroyo et al., 2012).

Microbial Bioremediation of Cadmium

Different species of genus Bacillus like B. subtilis (Gayathramma et al., 2013), B. cereus (Arivalagan et al., 2014), B. safensis (Priyalaxmi et al., 2014), B.licheniformis (Shameer, 2016), and B. thuriengiensis (Kumar et al., 2016) have been isolated from contaminated soils and water all over the world. The rate of bioremediation of cadmium is dependent on many factors- one of them being initial cadmium concentration. Reports have indicated that B. subtilis has a maximum cadmium reduction potential at 200 µg/ml but not beyond this (Gayathramma et al., 2013). This can be explained by saturation effect of metal binding sites and due to increased toxicity of cadmium above this level leading to decreased cellular growth of the organism (Pan et al., 2009). This has been proved by the results of the same study which showed a marked reduction in the bioremediation potential of B. subtilis for cadmium at increased concentration of 250 µg/ml. These results were corroborated in a study by Priyalaxmi et al., (2014), performed on B. safensis, isolated from mangrove sediments. It showed 83.5% reduction at 40 ppm concentration of cadmium while the reduction increased to 98% upon increasing the concentration of cadmium to 60 ppm.

pH is another factor playing an important role in bioremediation of heavy metals. Changes in surrounding pH affects the surface charge of cell wall by influencing the negatively charged functional groups and their dissociation (Özdemir et al., 2013). This has been well established in a study conducted by Arivalagan et al., 2014. B. cereus was isolated from soil near electroplating industry and grown in presence of cadmium, in vitro. At pH 2, the organism showed insignificant absorption (Vimala and Das, 2009), due to low ionization of functional groups (Al-Garni, 2007; Bulgariu and Bulgariu, 2012; Özdemir et al., 2013). Also, the high concentration of H+ at acidic pH competes for the available binding sites causing protonation of the cell wall (Yan and Viraraghavan, 2003). The study further reports that at moderately acidic pH 4, the negative charges on the cell wall increases and concentration of proton decreases (Rathinam et al., 2010) leading to more reduction of cadmium. Further at pH 6 maximum reduction of cadmium was reported as a result of complete deprotonation of functional groups like carboxyl and amino groups (Gupta and Rastogi, 2008; Xiao et al., 2010). Above this pH, a marked reduction in absorption was observed. This has been explained by increase in hydroxyl group which reacts with cadmium and precipitates it (Vimala and Das, 2009; Zhou et al., 2009; Xiao et al., 2010; Rathinam et al., 2010; Hossain and Aditya, 2013).

Biosorption is an energy dependent process and hence temperature plays an important role in the efficiency of metal removal by it (Congeevaram et al., 2007; Kao et al., 2009; Masoudzadeh et al., 2011). This efficiency increases or decreases with change in temperature that affects cell wall and its functional moieties by changing the stability and conformation of cell wall and the ionization state of functional groups (Li and Yuan, 2006; Congeevaram et al., 2007; Kao et al., 2009). Arivalagan and his team cultured B. cereus at 25, 35 and 45°C. Maximum cadmium removal was recorded at 35°C (72%) where a tremendous increase in biosorption efficacy was recorded as compared to 25°C (4%), the reason being increase in pore size as a result of which more surface is available for biosorption (Saleem et al., 2007; Rathinam et al., 2010). It also increases rate of diffusion and decreases viscosity of medium leading to increased efficacy of cadmium removal (Arivalagan et al., 2014). However, when the temperature increased from 35°C to 45°C, cadmium biosorption decreased. This may have happened due to destruction of the cadmium binding sites on cell wall by bond rupture leading to weaker cadmium binding potential (Meena et al., 2005; Dursun, 2006; Sari and Tuzen, 2008; Sulaymon et al.,2013).

Mechanism of Bioremediation of Cadmium

Due to their high surface area to volume ratio, bacteria have a remarkable capacity to adsorb metals from solution (Beveridge, 1989). They can perform this biosorption passively by mechanism such as surface precipitation, ion exchange or surface complexation (Le Cloirec and Andrès, 2005). Since this process is metabolism independent it can be performed by live as well as dead cells. This is in contrast to bioaccumulation where only live cells uptake the heavy metals actively rather than passively. Most of the studies on cadmium bioremediation have been conducted with live biomass but some others have proved that reduction in cadmium from cadmium-contaminated sites can be done with dead biomass too (Garcia et al., 2016). Since biosorption is a surface phenomenon, the cell wall of Bacillus sp. showed morphological and physiological changes after cadmium sorption. This was studied using SEM-EDX and FTIR (Nithya et al., 2011). A zeta potential analysis of B. cereus RC1 after cadmium adsorption determined that surface complexation and electrostatic interactions were important for biosorption (Huang et al., 2014). This biosorption capacity of Bacillus sp. is attributed to the various functional groups present on the cell wall. In addition to these functional groups, extracellular polymeric substance (EPS) also participates in biosorption. The constituents of EPS include carbohydrates and proteins and their derivatives in their homopolymeric or heteropolymeric form (Shameer, 2016). The advantages that bacterial cells gain from EPS production are many but essentially that of formation of biofilm which helps in metal and antibiotic resistance (Shameer, 2016). A study has proven that B. licheniformis NSPA5, B. cereus NSPA8 and B.subtilis NSPA13 produce EPS which gives these microorganisms resistance to cadmium and partakes in reduction of cadmium concentration (Shameer, 2016). These results have been corroborated by another study (Chauhan et al., 2017). In the same study, TEM analysis of EPS of unidentified isolates showed entrapment of cadmium within it. This could be due to the presence of active carboxylic groups as determined by FTIR of the extracellular polymeric substrate of Bacillus sp. (Suh et al., 1993; Ganesh et al., 2004; Shameer, 2016).

Metal resistant genes in microorganisms can be either plasmid borne or chromosomally encoded. Different studies have performed plasmid curing of cells of cadmium resistant Bacillus sp. showing no change in their biosorption potential. Hence, it was concluded that cadmium resistance in Bacillus sp. is due to genes present on its chromosome (Mahler et al., 1986; Nithya et al., 2011; Chauhan et al., 2017). An interesting observation was made in a study conducted by Huang et al., (2014) on B. cereus RC1. They reported that if concentration of Cd2+ was below 20mg/L then the predominant mechanism of bioremediation is bioaccumulation whilst above it, it is biosorption indicating that these mechanisms are dependent on initial concentration of cadmium.

Nickel [Ni (II)]

Toxicity of nickel

Nickel enters water, air and soil through natural sources like volcanic emissions, weathering of rocks and soil and solubilisation of nickel compounds from soil and through anthropogenic sources i.e. release of nickel containing effluents from industries like electroplating industry, battery industry, catalyst industry and electronic equipment industry (Duda-Chodak and Blaszczyk, 2008). This has hazardous effect on human health (Barceloux and Barceloux, 1999; Denkhaus and Salnikow, 2002). Nickel enters the human body via inhalation, ingestion and absorption through skin (Duda-Chodak and Blaszczyk, 2008). In blood, nickel is transported by binding mostly to albumin but also to histidine and α2- macroglobulin (Glennon and Sarkar, 1982; Kasprzak et al., 2003). The symptoms exhibited in nickel toxicity vary according to time and dose of exposure causing different health problems ranging from nausea, giddiness and vomiting (Duda-Chodak and Blaszczyk, 2008) to respiratory disorders and cardiovascular disorders and even death (Oller et al., 1997; McGregor et al. 2000; Seilkop and Oller 2003).

Microbial Bioremediation of Nickel

Nickel-resistant Bacillus sp. have been isolated from waste water treatment plant (Rajbanshi, 2008) and contaminated soils (Shoeb et al., 2010; Aryal, 2015; Taran et al., 2015). They have shown maximum nickel removal capacity from 50µg/ml to 150 µg/ml of initial nickel concentration (Abdel-Monem et al., 2010; Lei et al., 2014; Zhang et al., 2016; Uthra and Kadirvelu, 2017). Studies have shown that factors such as pH, temperature, contact time and initial nickel concentration affect the efficiency of nickel bioremediation by both dead and live cells of Bacillus sp. In these studies it was observed that maximum removal of nickel by live cells occured at neutral pH (Abdel-Monem et al., 2010; Salman, 2014; Taran et al., 2015; Naskar et al., 2016; Jain et al., 2017) while one has reported nickel removal at slightly acidic pH i.e. pH 5 (Aryal, 2015). Temperature too played a crucial role in bioremediation of nickel where optimum temperature was observed in the mesophilic range i.e. 25°C to 40°C (Salman, 2014; Aryal, 2015; Taran et al., 2015; Naskar et al., 2016) for live cells. Optimum contact time varied from 25 mins (Aryal, 2015) to 24 hrs (Taran et al., 2015). However, in case of nickel removal using dead cells of Bacillus sp. as adsorbent, optimum pH varied from pH 4 (Zhang et al., 2016) to pH 8 (Gheethi et al., 2017) while optimum temperature was from 30°C to 37°C (Gheethi et al., 2017; Uthra and Kadirvelu, 2017).

Mechanism of Bioremediation of Nickel

The studies performed by various scientists proved time to time that both dead and live cells of Bacillus sp. exhibit the capacity for nickel removal, thus highlighting the possibility that biosorption is the primary mechanism for nickel bioremediation. In 2015, Aryal et al. demonstrated with the help of FTIR, that –COOH and –NH2 groups of B. sphaericus are responsible for nickel binding. They further proved this by studying the effect of temperature on nickel removal. They observed that with increase in temperature from 20°C to 40°C the bioremediation potential of the organism too was elevated. However, on increasing the temperature further, this potential dropped due to decrease in surface activity. They concluded this study by reporting that nickel bioremediation by B. sphaericus is through biosorption and is also an exothermic process. Another published report has shown similar findings (Sari et al., 2008). After nickel exposure, change was observed in surface morphology of dead B. laterosporus MTCC 1628, with the help of SEM-EDX, further corroborating findings that nickel bioremediation is by biosorption. Similar changes were observed in B. licheniformis (Jain et al., 2017). These results are suggestive of a passive process i.e. biosorption which is a surface phenomenon.

The species of genus Bacillus are Gram positive, rod shaped spore formers. Their cell wall offers many negatively charged functional groups like hydroxyl, carboxylate, sulphate and amino groups (Vijayaraghavan and Yun, 2008). These groups exhibit ionic interaction with positively charged Ni2+ ions after initial metal complex formation and neutralization of chemically active sites (Beveridge, 1989). When cells of B. subtilis 117S were pretreated with sodium azide, mercuric chloride and formaldehyde, a decrease in nickel removal capacity of cells was observed. It occurred due to esterification of carboxyl groups and methylation of amino groups. This hereby concluded the importance of functional groups present on cell wall of Bacillus sp. in nickel bioremediation (Abdel-Monem et al., 2010).

In 2009, Shoeb et al. isolated B. cereus CMG2K4 from metal contaminated soil and by plasmid curing they were able to demonstrate that nickel bioremediation capacity of this organism is chromosomally borne. The organism also produced a 36KDa protein upon exposure to 1 mM NiCl2. This was identified as flagellin, a flagellar protein. It was hypothesised that it was overproduced under heavy metal stress to increase motility of B. cereus CMG2K4 to avoid areas with high nickel concentration and move to a potentially new site devoid of toxic substances (Ottemann and Miller, 1997). This suggests that not only one, but several mechanisms are responsible for bioremediation of heavy metals.

Microbial Bioremediation of Cadmium and Nickel by Lactic Acid Bacteria (Labs) and Other Probiotic Species of Genus Bacillus

In 2001, WHO defined probiotics as, “live microorganisms that when administered in adequate amount confer a health benefit to the host” (FAO/WHO, 2001). These health benefits in general include treatment of digestive disorders and strengthening of immune system (Huët and Puchooa, 2017). The probiotic microorganisms can be either inhabitants of gastrointestinal tract (GIT) like LABs or can be isolated from different sources in the environment like probiotic species of genus Bacillus.

LABs are a vast group of organisms, their main characteristic being production of lactic acid as major end-product of carbohydrate fermentation. They are generally Gram positive cocci and rods. Lactobacillus, Pediococcus, Streptococcus, Leuconostoc and Bifidobacterium are some of its important representative genera (Todar, 2004). They have unique properties of being able to reduce the concentration of toxic substance from GIT (Meriluoto et al., 2005) as well as bioremediation of heavy metals in vitro and in vivo (Halttunen et al., 2007; Zhai et al., 2017). They owe this ability to bind heavy metals due to specific constituents found in their cell wall like teichoic acid and lipoteichoic acid along with some polysaccharides and EPS (Delcour et al., 1999).

An extensive study was performed by Halttunen et al., (2007) on bioremediation of cadmium by 3 species of Bifidobacterium i.e. B. longum 2C, B. longum 46, and B. lactis Bb12, 3 species of Lactobacillus i.e. L. rhamnosus GG, L. casei Shirota and L. fermentum ME3 and 2 commercial starter cultures. For a contact time of 1 hr, B. longum 46 showed highest cadmium removal of 54.7 mg metal/ g dry biomass followed by L. fermentum ME3 and B. lactis Bb12. The test pH ranged from acidic to alkaline and interestingly, a pH drop was observed at all pH values except for highly acidic ones. This pH drop indicates that biosorption occurs by means of ion exchange, where H+ on cell wall is being replaced by Cd2+ and causes pH to decrease upon its release into the surrounding medium. With increase in pH, the binding capacity for cadmium increased till pH 6 where it was maximum (60-73%). This variation in biosorption potential results from competition between protons and heavy metal cations for the negatively charged binding sites (Huang et al., 1991).

When the bacterial concentration (biomass) was increased the binding efficacy also improved due to availability of binding sites in excess. This binding is quite strong in L. plantarum as it did not show any metal desorption upon multiple washings with Milli- Q water (Kumar et al., 2017). Another observation made was that temperature variations did not affect the bioremediation potential of these microorganisms; emphasizing that this process is temperature independent. Similar effect was observed when bacteria were killed by boiling them. This elucidates that the probable mechanism of bioremediation is passive i.e. biosorption rather than active i.e. bioaccumulation. These results, however contradict the reports of Hao et al., (1999a) where it was observed that when L. plantarum cells were poisoned or kept at low temperature no cadmium removal happened, suggesting that the nature of this mechanism is energy dependent.

Various metal ions interfere and inhibit uptake of other heavy metals. In L. plantarum Cd2+ removal was inhibited by Mn2+ but not by Zn2+, Cu2+, Co2+ etc. The high concentration of Mn2+ in L. plantarum helps to reduce toxicity of superoxide radical ions by scavenging them (Archibald and Fridovich, 1981a and b, Archibald and Fridovich, 1982a and b). The transport system of Mn2+ is linked to uptake of Cd2+ (Hao et al., 1999a). In this context, L. plantarum has showed the presence of two different cadmium uptake systems: one which is independent of Mn2+ starvation but has low affinity, while the other is with high affinity and induced by Mn2+ starvation but inhibited in presence of Mn2+ (Hao et al., 1999a). Upon characterization of genes involved in cadmium and manganese uptake, gene mntA was identified as the one encoding high affinity transporter system for Cd2+ and Mn2+ uptake. This gene belonged to a family of P-type ATPases (Hao et al., 1999b).

Lactobacillus strains L. kefir CIDCA 8348 and L. kefir JCM 5818 were evaluated for their ability to bind cadmium in vitro and protect eukaryotic HepG2 cell lines from cadmium toxicity. When HepG2 cell lines were exposed to cadmium pre-incubated with these strains, the viability of the cell line increased as compared to direct exposure of cadmium, where the efficiency of L. kefir JCM 5818 was higher. This was attributed to its non-aggregative nature as compared to L. kefir CIDCA 8348, thus providing more surface area and hence more binding sites for cadmium (Gerbino et al., 2014). Thus, the study proved ability of Lactobacillus sp. to bioremediate cadmium as well as reduce cadmium toxicity in eukaryotic cells.

Heavy metal stress also leads to synthesis of proteins which may mitigate the toxicity caused by heavy metals. One such glycoprotein isolated from L. plantarum L67 inhibits inflammatory factors such as AP-1, mitogen activated protein kinases and nitric oxide synthase expressed by RAW 264.7 cells under Cd2+ stress (Song et al., 2016).

Biological evidence has been provided by Zhai et al., (2013) where they have reported that L. plantarum CCFM8610 has reduced cadmium toxicity in vivo. This study was performed on male Kunming mice, where they were exposed to cadmium stress. In presence of dead and live L. plantarum, faecal matter showed increasing cadmium concentration as compared to control groups. Due to oxidative stress in body caused by acute cadmium exposure, liver too showed histopathological damage such as necrosis of hepatocytes (Tzirogiannis et al., 2003). This resulted in an increase in malondialdehyde (MDA-indicator of lipid peroxidation), decreased glutathione (GSH) (consumed to reduce reactive oxygen species (ROS) produced as a side effect of cadmium toxicity) (Bagchi et al., 1996), and decrease in activity of superoxide dismutase (SOD) and catalase (CAT) (both enzymes with antioxidant property) in liver and kidney (Thijssen et al., 2007). When mice were treated with L. plantarum all these symptoms were alleviated, more so with live cells as compared to dead cells. This specific antioxidant property of Lactobacillus has also been reported in other studies (Güven et al., 2003; Zhang et al., 2010).

Another mechanism is that this species reduces cadmium toxicity by reducing its absorption from the intestine. If cadmium is absorbed, it induces synthesis of metallothionein (MT) (Nordberg and Nordberg, 2000) and the Cd- MT complex is stored in liver. However, if cadmium concentration exceeds metallothionein production, then it damages liver and kidney (Nordberg and Nordberg, 1987; Klaassen and Liu, 1997). L. plantarum CCFM8610 rapidly binds cadmium before it can be absorbed in intestine and excretes it in faeces (Zhai et al., 2013).

Under in vitro conditions both live and dead L. plantarum CCFM8610 had similar cadmium binding ability but live L. plantarum proved more efficient in reducing cadmium concentration because it stimulated intestinal peristalsis and reduced oxidative stress caused by cadmium exposure (Zhai et al., 2013).

There are many species belonging to genus Bacillus including B. clausii and B. coagulans which have both the remarkable properties together i.e. they have probiotic potential as well as capacity for bioremediation of heavy metals (Belapurkar et al., 2016). When male Wistar rats were fed with a synbiotic diet i.e. probiotic microorganisms (B. coagulans and L. plantarum CNR 273) together with a prebiotic (inulin), their liver enzymes are improved post cadmium exposure. Some biochemical parameters such as aspartate aminotransferase (AST), alanine aminotransferase (ALT), bilirubin and blood urea nitrogen (BUN) that were enhanced by cadmium, decreased significantly and cadmium accumulation in liver and kidney was reduced when administered with this synbiotic diet (Jafarpour et al., 2017). Similar results were reported by a previous study (Majlesi et al., 2016).

Immobilized B. coagulans also exhibited a high adsorption capacity of 68.4 mg/ g of biomass in nickel bioremediation (Lei et al., 2014).

Conclusion

In today’s scenario of heavy metal pollution causing hazardous effects on human life, the role of microorganisms suggest an easy and cheap alternative for their remediation. The mechanism of bioaccumulation and biosorption have shown potential for bioremediation in environmental and probiotic species of genus Bacillus as well as in other probiotic genera. They have shown convincing ability of potential gut remediation of heavy metals cadmium and nickel, suggesting their pivotal role in solving the problem of heavy metal toxicity commonly seen as a side effect of industrialization.

Conflict of interest

There is no conflict of interest.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Acknowledgements

The authors are grateful to Ar. Achal Chaudhary, President, IPS Academy and Dr. Sanjay Nagar, Professor and Head, Department of Biotechnology, IPS Academy, for their encouragement and timely help in this review.

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