Abstract
Arsenic (As) pollution, particularly in soil and water, is a very prominent environmental issue which seriously threatens plant growth, development, and productivity. Since As is ubiquitous in the natural environment, microorganisms have developed mechanisms to resist the toxic effects of this metalloid. A large number of microorganisms, viz. Acinetobacter, Aeromonas, Bacillus, Exiguobacterium, and Pseudomonas, are capable of growing in the presence of high concentrations of As. But relatively less information is available on accumulation, mobilization, distribution, and speciation of As by rhizospheric microbiota and their impact on plant growth and development. The use of As-resistant and plant growth promoting microorganisms (PGPMs) for the restoration of plants growing on contaminated soils is the need of the time. The use of PGPM occupies a small but growing niche in the development of organic agriculture and has attracted attention during the last decade only. There are several reports revealing the multifarious role of soil microbiota in amelioration of As toxicity and improving metal tolerance in plants. Colonization of PGPMs helps the host plant to overcome As-induced phosphate (P) deficiency and consequently maintain favorable P:As ratio. Further, they also improve nutritional status and reduce As uptake and translocation in plants. Inoculation of bacteria/fungi can exert protective effects on vascular plants under As contamination by transforming more toxic inorganic forms into less toxic organic forms or via reducing the concentration of As by enhancing plant biomass. The PGPMs also result in higher activities of the antioxidant enzymes (superoxide dismutase, catalase, ascorbate peroxidase, and guaiacol peroxidase) and accumulation of nonenzymatic antioxidants (carotenoids, ascorbic acid, proline, and α-tocopherol). Increased concentrations of cysteine, glutathione, and non-protein thiols, and activity of glutathione S-transferase have also been reported that facilitate sequestration of As into nontoxic complexes. Thus, application of As-resistant PGPMs could provide a low cost and eco-friendly mitigation approach to diminish As accumulation in plants, thereby promoting higher growth, development, and yield responses. There is also a need to improve our understanding of the mechanisms involved in extenuating toxic effects of As by rhizospheric microbiota and to improve the stabilization of plants in contaminated sites.
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8.1 Introduction
Arsenic (As) is a toxic metalloid of global concern, as it cannot be degraded to harmless products instead persists indefinitely in the environment. It occurs in trace quantities in rocks, soil, water, and air but can be intensified by anthropogenic activities (Garelick et al. 2008). Consequently, elevated levels of As have been reported in soils and groundwater worldwide. The amount of As in a plant depends on the amount of As it is exposed to. Terrestrial plants may accumulate As by root uptake from the soil (Li et al. 2015) or by adsorption of airborne As deposited on the leaves. Background As concentrations in terrestrial biota are usually less than 1 mg kg−1. The highest As concentration occurs in the roots of plants (Álvarez-Ayuso et al. 2015).
Arsenic is a nonessential element for plant and is expected to negatively affect growth responses. Plants cope with As toxicity by employing various detoxification mechanisms such as accumulation, sequestration, and compartmentalization. Nevertheless, failure of any once of these mechanisms leads to symptoms of phytotoxicity (Moreno-Jiménez et al. 2012). Alteration in plant growth usually occurs at higher levels of As application leading to different physiological and chemical changes in plants, such as necrosis and wilting, inhibition of seed germination, decrease in plant growth, restricted root and shoot length, lower fruit and grain yield, reduced enzymatic activity, and replacement of As with phosphorus in reactions (Zhao et al. 2009; Chandrakar et al. 2016). Bioavailability, uptake, and phytotoxicity of As in plants are influenced by factors like concentration and speciation of As, plant species, soil properties such as pH, redox potential, and soil phosphorus content (Fitz and Wenzel 2002).
Remediation of As-contaminated soils and groundwater is necessary for limiting the entry of this toxic metalloid in the food chain. The use of microorganisms in the bioremediation of contaminated ecosystems showed a great prospective for future developments due to its environmental compatibility and possible cost-effectiveness. Microorganisms have evolved dynamic mechanisms for facing the toxicity of As which enable them to survive in As-rich environments. The strategies developed by microbes to counteract As toxicity include the active exclusion of it from cells by establishing permeability barrier, intra- and extracellular sequestration, active efflux pumps, and microbial bioaccumulation (Tsai et al. 2009; Wang et al. 2013). Microorganisms are also known to survive As exposure by transforming it through oxidation-reduction reactions and methylation-demethylation processes into less toxic forms (Cai et al. 2009; Liao et al. 2011; Kuramata et al. 2015). A variety of microbes are known today which utilize As in their metabolism, using either arsenate [As(V)] as a terminal electron acceptor in anaerobic respiration or generating energy by oxidation of arsenite [As(III)] during chemolithoautotrophic growth (Kruger et al. 2013).
The application of metal-resistant and plant growth promoting soil microbes as bioinoculants for supplying nutrients and/or stimulating plant growth are gaining momentum. These microbes have an extensive range of growth modes and are capable of growing, utilizing a variety of organic substrates. These properties make them ideal for the treatment of contaminated soils, assisting in possible remediation. Several rhizospheric metal-resistant microbes are also known to have plant growth promoting abilities, viz. nitrogen fixation, phosphate solubilization, and production of siderophores and phytohormones, suggesting their substantial role in As-biogeochemistry and bioremediation (Beneduzi et al. 2012; Bhattacharyya and Jha 2012; Gupta et al. 2015; Batool et al. 2017).
8.2 Microbial Diversity in Arsenic-Contaminated Ecosystems
Diverse microbial community exists in As-contaminated sites that can uptake and transform As in the environment (Banerjee et al. 2011; Sarkar et al. 2013; Ao et al. 2014). Although As is toxic to microbes, certain bacteria and fungi survive its exposure by developing As detoxification mechanisms that permit the cell to neutralize its toxic effects (Srivastava et al. 2011; Kruger et al. 2013). Countless native, As-resistant, phylogenetically diverse, and metabolically versatile bacteria and fungi have been isolated from varied habitats, including soil, water, and sediments, contaminated with high levels of As (Tables 8.1 and 8.2). Presence of As-resistant microbial species in the As-rich environment is highly expected since high levels of metallic species are likely to exert a strong selective pressure thereby reducing the overall growth of sensitive microbial population (Sarkar et al. 2013). This favors the survival of indigenous As-resistant microorganisms in the As-rich habitats (Pepi et al. 2007). Long-term association of microorganisms with toxic metal within metal-rich sites often promotes adaptation of the microbes in such environmental conditions (Banerjee et al. 2013; Majumder et al. 2013).
Microbial activities account direct effect on the bioavailability of As in soil, water, and sediments (Sarkar et al. 2013). Studies on the existence and dispersal of innate metal-tolerant microbial flora bear tremendous applicability in microbial bionetwork to understand the degree of metal pollution of the ecosystem. Such potential microbes may be channelized not only in detecting environmental alterations but also in treating toxic substances. Development of advanced technologies involving complex microbial reactions is utmost important for the enhanced bioremediation of As-contaminated milieus (Kruger et al. 2013).
8.3 Mechanisms of Arsenic Resistance in Microorganisms
8.3.1 Bacteria
It is well established that a number of microorganisms possess metabolic mechanisms to resist the disruptive effects of As and to survive in its presence (Rosen 2002; Li et al. 2010). The greater part of As resistance and detoxification studies have been performed in bacteria, and their molecular mechanism has been elucidated precisely (Rahman and Hassler 2014). The strategies to manage or neutralize As toxicity mainly include accumulation (Wang et al. 2013; Rahman et al. 2014), active extrusion of As, extracellular precipitation, complexation into peptides (Kruger et al. 2013; Kuramata et al. 2015), and As transformation including methylation, demethylation (Bentley and Chasteen 2002), oxidation, and reduction (Liao et al. 2011). Some bacteria even use As compounds to fuel their energy metabolism, either as an electron donor or as an electron acceptor (Silver and Phung 2005).
Of all the processes, enzymatic reduction of As(V) to As(III) mediated by the gene products of the widespread ars operon followed by efflux of As(III) from the cell is the most common one and is found in both gram positive and gram negative bacteria (Silver and Phung 2005; Vishnoi and Singh 2014). The As resistance gene systems which are responsible for the metabolism and detoxification of As may be found either in plasmids (Drewniak et al. 2013) or chromosomes (Bhat et al. 2011).
8.3.1.1 Arsenic Uptake Systems
Pathways for uptake of As into bacterial cells have only recently been discovered. The most common and abundantly existing forms of As oxyanions, arsenate and arsenite, use uptake systems that transport these compounds into cells (Fig. 8.1). Arsenate is a substrate analogue of phosphate and is taken up via the phosphate transporters by most of the organisms (Rosen 2002). Two phosphate transporters, Pit and Pst, have been identified in different bacterial groups, both of which catalyze As(V) uptake. Of the two transporters, Pit is the major transport system (Tsai et al. 2009).
Transporters for arsenic uptake in bacteria
Arsenite shows very strong similarity with the conformation of glycerol and is adventitiously taken up by a trivalent metalloid transporter identified as GlpF (Rosen and Liu 2009; Tsai et al. 2009) (Fig. 8.1). Transporter GlpF is an aquaglyceroporin and a member of the major intrinsic protein (MIP) superfamily that allows the transport of water and small solutes such as glycerol and urea by an energy-independent mechanism (Rosen 2002).
8.3.1.2 Arsenate Reduction: Detoxification
A wide range of microorganisms have evolved As resistance mechanisms to survive in As-contaminated environments (Tsai et al. 2009; Nagvenkar and Ramaiah 2010). One such process involves the reduction of As(V), which has the purpose of detoxification by converting As(V) to As(III) (Páez-Espino et al. 2009). Microorganisms combat the importation of As(V) by a two-step mechanism in which this compound is first reduced to As(III) by a cytoplasmic As(V) reductase (Rosen 2002). Although As(III) is a more potent toxicant than As(V), the former is selectively expelled from the interior of the cell via membrane efflux pump (Mateos et al. 2006).
8.3.1.3 Arsenate Reduction: Energy Generation
In addition to the detoxification of As(V), certain bacteria can reduce As(V) as the terminal electron acceptor during anaerobic respiration for generating energy (Hudson-Edwards and Santini 2013; Kruger et al. 2013). These are defined as dissimilatory As(V)-respiring bacteria (Oremland and Stolz 2005), in which respiration is recognized to be mediated by a specific enzyme or respiratory chains (Silver and Phung 2005). Arsenic respiration can influence both the speciation of As and its mobility. Dissimilatory As(V)-respiring bacteria are able to reduce both sorbed and dissolved As(V) to As(III) coupled to As(III) efflux systems, presumably because the enzymes responsible for As(V) reduction are located in the periplasmic membrane (Silver and Phung 2005).
8.3.1.4 Arsenite Oxidation: Detoxification and Energy Generation
Bacterial oxidation of As(III) to As(V) is very well documented, particularly with isolates from As-impacted environments (Bahar et al. 2012). Many heterotrophic bacteria oxidize As(III) to As(V) to speedily detoxify their surroundings, while others use As(III) as an electron donor. Over 30 strains representing at least 9 genera of As-oxidizing prokaryotes have been reported (Stolz et al. 2002). The transformation reaction involving the energy gain by conversion of more toxic As(III) into less toxic As(V) has increased the ecological significance of these bacteria over other microorganisms. Since As(V) is less soluble and is much more effectively removed by physicochemical methods, oxidation of As(III) can be important for As removal (Tsai et al. 2009).
8.3.1.5 Methylation
Methylation was formerly thought to be a detoxification step; however, recent information suggests that not all methylated As products are less toxic (Páez-Espino et al. 2009). Methylation process produces both volatile and nonvolatile methylated compounds of As (Qin et al. 2006). The major volatile methylated As compounds are mono-, di-, and trimethylarsine, while the major nonvolatile compounds are methylarsonate and dimethylarsinate (Fig. 8.2).
Bacterial methylation of arsenic
The methylation reaction follows the reduction of As(V) and subsequent oxidative addition of methyl groups, thus generating arsines and methyl arsenicals (Páez-Espino et al. 2009; Kruger et al. 2013). The volatile methylated forms of As are readily released into the environment where oxidation might convert them back to the oxidized form, As(V). A variety of microorganisms have been implicated as the major contributors of As methylation (Wang et al. 2015) and are included in the genera: E. Coli (Yuan et al. 2008), Pseudomonas (Chen et al. 2014), Streptomyces (Kuramata et al. 2015), and Clostridium (Wang et al. 2015). Understanding of these mechanisms will not only shed light on the As mobilization but may also open up new horizons in metabolic pathway engineering to exploit those for As remediation (Huang et al. 2015).
8.3.2 Yeast and Fungi
Arsenate [As(V)/H2AsO4 −] is a chemical analogue of phosphate and hence gets transported by high-affinity phosphate uptake system Pho87. Moreover, As(III) (H3AsO3) is not a phosphate analog and therefore is transported into the cell either through GlpF or passive diffusion (Sharples et al. 2000). Although the mechanisms of As detoxification remain unstudied in fungi, several pathways mediating detoxification of As have been elucidated in the yeast Saccharomyces cerevisiae. It is now an established fact that the most common mechanism of resistance in yeast is mediated by the products of three adjacent genes ACR1, ACR2, and ACR3. The putative product of the ACR1 gene showed similarity with the yeast transcriptional regulatory proteins, encoded by YAP1 and YAP2 genes. Gene ACR2 encodes arsenate reductase enzyme which is known to mediate a rapid internal reduction of As(V) to As(III), which then initiates efflux of As(III) from the hyphae (Mukhopadhyay et al. 2000). Reduction of As(V) to As(III) is also mediated by P37 in species like Aspergillus; however, it does not methylate As to any significant extent (Ca’novas et al. 2004).
Arsenite efflux has As(V) resistance in S. cerevisiae and many other fungi and is mediated by an As(III) transporter gene ACR3. Likewise, ACR3 encodes a putative plasma membrane As(III) efflux transporter protein that pumps As(III) out of the cell, whose expression is strongly induced by the presence of both As(III) and As(V) (Wysocki et al. 1997). In addition, conjugation of As(III) with glutathione by GstA and its subsequent transport into vacuoles by an ABC metal ion transporter is also one of the methods of detoxification. Moreover, biovolatilization via methylation by Cyt19 for detoxification purposes has been further proposed to increase As resistance in fungi (Ghosh et al. 1999; Choe et al. 2012).
8.4 Influence of Microorganisms on the Speciation and Bioavailability of Arsenic
The accumulation of different As species in various ecosystem compartments is regulated by different microbial processes. Microorganisms play an important role in the speciation and cycling of environmental As with a variety of mechanisms affecting As transformation between soluble and insoluble forms. Although As is highly toxic to most of the life forms, some microorganisms have developed As resistance mechanisms while some even thrive on the metalloid, using it as a source of energy for growth (Wang et al. 2011; Kruger et al. 2013). The actual state of As strongly depends on microbial transformations in soils, including reduction, oxidation, and methylation processes. Microbial enzymatic activities catalyze the conversion of the As species into forms having a different solubility, mobility, bioavailability, and toxicity (Lièvremont et al. 2009). The inorganic As forms, especially As(V) and As(III), are subjected to microbiologically mediated oxidation-reduction reactions. Microbes could even derive metabolic energy by the oxidation of As(III) or could use it as the sole energy source. Arsenate, on the other hand, is reduced by dissimilatory reduction and utilized as a terminal electron acceptor for anaerobic respiration. In addition, microorganisms may possess As(V) reduction mechanisms that are not coupled to respiration but instead are thought to impart As resistance. The detoxifying reductases present in the cytoplasm reduce As(V) to As(III) for its rapid extrusion from the cell. Even microbes capable of both As(III) oxidation and As(V) reduction are recognized (Pandey and Bhatt 2016). Soil microbes are also able to biomethylate inorganic arsenicals to monomethyl arsenic acid (MMAA) and dimethylarsenic acid (DMAA), and to other organic arsenicals (e.g., arsenocholine, arsenobetaine, arsenosugars, arsenolipids). The organo arsenicals are further metabolized to complete the As cycle (Dhuldhaj et al. 2013). In contrast, demethylating microorganisms carry out the conversion of methylated As species back to inorganic forms. Further, microbial activity can also methylate As(III) resulting in volatilization of As to gaseous arsines, viz. trimethylarsine gas, thereby releasing As into the atmosphere (Islam et al. 2007). Arsines are toxins which may travel in air for indefinite time period, or they may be rapidly oxidized subject to environmental conditions. Oxidation again yields inorganic As species, As(V) or As(III), or organic forms, MMAA and DMAA, which are deposited back to the soil by rain or by dry deposition, thereby completing the cycle of As.
8.5 Plant Growth Promoting Microorganisms
The plant health and soil fertility are the determinants of beneficial plant-microbe interactions in the rhizosphere which play a pivotal role in transformation, mobilization, solubilization, and subsequent uptake of essential nutrients by the plants (Dey et al. 2004). Despite the long history of interest in As-resistant plants and microbes, the attention of microbiologists toward plant-associated bacteria from heavy metal enriched habitats is more recent (Sessitsch et al. 2013). It has been well established that the soil hosts a large number of microbes, including bacteria and fungi. The microbial count of different soils is subjective to the soil conditions including temperature, pH, moisture, salinity, and presence of other chemicals, as well as by the type of vegetation of that area. There is a huge diversity of soil microbial communities which is exceptionally rich and has developed diverse As resistance and detoxification mechanisms thereby redistributing As in soil (Sheik et al. 2012). Soil microorganisms affect As mobility and availability to the plant; they produce iron chelators and siderophores, solubilize metal phosphates, and produce growth hormones (Cavalca et al. 2010). Numerous metal-resistant microbes could transform As compounds by oxidation, reduction, methylation, and demethylation (Stolz et al. 2002) and are known to promote plant growth by direct and/or indirect mechanisms (Rajkumar et al. 2012). They act as a barrier and limit the transfer of As into plant tissues, thereby improving growth of the host plant (Fitz and Wenzel 2002). These microbes may prove beneficial for the revegetation and phytostabilization of As polluted sites. Thus, the need of the hour is to enhance the efficiency of the beneficial microbes for sustainable agricultural production (Khan 2005).
8.5.1 Rhizobacteria
The beneficial, free-living bacteria that colonize roots and establish a symbiotic relationship with plants to promote growth are referred to as plant growth-promoting rhizobacteria (PGPR). The abundance of bacteria in the rhizosphere is because of the presence of nutrients including sugars, amino acids, organic acids, and other small molecules released from plant root exudates (Gupta et al. 2015). While only 1–2% of bacteria promote plant growth in the rhizosphere, even lesser is known about the heavy metal–resistant PGPR. Additionally, it is also recognized that PGPR unwilling As are widespread in nature and are phylogenetically diverse (Table 8.3). They can have the advantages of oxidizing/reducing As and promoting plant growth in As stressed soil (Das et al. 2016). Moreover, it is now an accepted fact that the bacterial inoculation significantly reduces As uptake and its accumulation in shoot and grains of many plant species. Owing to its wide action spectrum, the As-resistant PGPR could serve as a potential bioinoculant for mitigation of As in different plants, thereby contributing to sustainable crop production in As-contaminated areas (Bhattacharyya and Jha 2012).
Plant growth promoting rhizobacteria are broadly categorized into extracellular plant growth promoting rhizobacteria (ePGPR) and intracellular plant growth promoting rhizobacteria (iPGPR) (Viveros et al. 2010). These rhizobacteria effect plant growth either directly or indirectly, even in As stressed soils. The direct effect on plant growth is facilitated by the production of phytohormones (e.g., IAA), antibiotics, inorganic phosphate solubilization, increased production of iron-chelating siderophores, ammonia, and exopolysaccharides, thereby stimulating many important pathways (Fig. 8.3). However, their indirect effects can occur by antibiosis, synthesis of hydrolytic enzymes, struggle for the availability of nutrients with pathogenic bacteria in soil, or by inducing systemic resistance (ISR) against wide-ranging root pathogens in the rhizosphere. Out of the many resistance mechanisms acquired by rhizobacteria, salicylic acid-dependent SAR pathway or jasmonic acid and ethylene perception from the plant are the most evident ones (Beneduzi et al. 2012). Arsenic-resistant PGPR’s might be useful in framing new amalgamations, leading to a more efficient use for phytostabilization and improvement of cropping systems (Gupta et al. 2015).
Beneficial effects of metal-resistant and plant growth promoting bacteria
8.5.2 Arbuscular Mycorrhizal Fungi
Arbuscular mycorrhizal fungi (AMF) are ubiquitous in nature and establish important symbiotic relationships with most terrestrial plants even in heavy metal–contaminated environments (Sun et al. 2016). Moreover, plant compatibility with mycorrhizal fungi is a generalized and primordial phenomenon. Arbuscular mycorrhizas are characterized by the formation of highly branched and unique structures called arbuscules, which help plants to capture nutrients such as phosphorus, carbon, sulfur, nitrogen, and other micronutrients from soil (Gianinazzi-Pearson 1996).
However, AMF are widespread in different regions of the world; they are influenced by As concentrations and seasonal variations. A variety of species have been identified, belonging to the genus Acaulospora, Glomus, Gigaspora, Westerdykella, Trichoderma, Rhizopus, Lasiodiplodia, Paraglomus, Rhizophagus, etc. (Table 8.4). Arbuscular mycorrhizal fungi belonging to the phylum Glomeromycota form a symbiotic association with more than 80% of terrestrial plants. The predominance of these species indicates their high tolerance to excess As; nevertheless, As contamination adversely affects the diversity and function of AMF (Schneider et al. 2013a; Sun et al. 2016). Dominant plant species present in As-contaminated sites are habitually colonized by AMF, which is indicative of their central role in mitigating heavy metal stress in plants. Arbuscular mycorrhizal fungi improve the tolerance of host plants to As in contaminated soils by performing two different roles in phytoremediation: one being phytoextraction and another phytostabilization (de Melo et al. 2014; Krishnamoorthy et al. 2015).
8.6 Plant Growth Promoting Microorganisms in Extenuating Arsenic Toxicity
8.6.1 Precipitation, Binding, or Chelation of Arsenic in the Rhizosphere
The biochemical and molecular mechanisms of plant-microbe interactions in As stressed soils can change metal bioavailability in soil through various mechanisms such as acidification, precipitation, chelation, complexation, and redox reactions. The microbial activities are known to enhance the mobility of metals by forming metal/mineral complexes, intracellular binding, electron transfer by enzymes in the rhizosphere (redox reactions), etc. The microbes present in the As-contaminated soils have evolved resistance strategies to tolerate considerably high concentrations of metals. The extensive research on the metal-resistant PGPM have shown many possibilities to improve plant growth by alleviating metal toxicity, and improving restoration by mobilization/transformation of metals in soil (Rajkumar et al. 2012; Tak et al. 2013; Ma et al. 2016).
8.6.2 Root Colonization
Rhizobacteria provide nutrients to the plant by habituating the soil surrounding the roots of the beneficiary plant. In turn, the plant creates and maintains root nodules for rhizobacteria, thereby providing a proper place and conditions for the bacteria to be alive and active. This colonization makes the soil, surrounding the plant, more rich in terms of nutrients. The effectiveness of PGPR has often been attributed to their ability to colonize plant roots. Bacterial colonization into plant roots is a series of a process involving various steps. It defines the ability of the bacteria to survive and multiply in the region surrounding the roots in response to the plant exudates, to attach with the root surface, and to colonize developing a root system. There could be multifactorial phenomenon contributing the process of colonization, viz. chemotaxis to root exudates, cell motility, production of pili or fimbriae, quorum sensing, etc. (Ma et al. 2016).
In case of AMF, the process of colonization takes place in a way different to that in bacteria. The plant-microbe interaction starts with the signal exchange and recognition between host plants and AMF before they come into physical contact. Signal recognition has been proposed to help in cellular adaptation in fungi required for the functional compatibility between the plant and fungal cells. This finely tuned recognition processes help in establishing molecular coordination between the two. The recognition signal from the host plant helps in inducing hyphal branching followed by the formation of appressoria at the root surface during the early hours of contact. Metabolites exuded by plant roots specifically enhance spore germination and fungal growth which helps the fungus to invade the root. Fungal development is limited to the outer root tissues, while hyphae quickly enter the inner cortical cells of host plant where they differentiate into the highly ramified arbuscules (Gianinazzi-Pearson 1996).
This proves that the successful colonization forms an important part of the plant-microbe relationship. It not only helps in the exchange of nutrients but also limits the uptake of harmful chemicals and heavy metals like As to the plant tissues and prevents the rate and extent of pathogen colonization in roots, thereby helping the plants to grow and propagate at high concentrations of As (Jog et al. 2014; Mallick et al. 2014).
8.6.3 Facilitating Resource Acquisition
8.6.3.1 Nitrogen Fixation
Nitrogen is an imperative nutrient to all life forms; however, gaseous nitrogen remains unavailable to the plants due to the high energy required to break the triple bonds present between the two atoms. Rhizobacteria, through nitrogen fixation, are able to convert gaseous nitrogen to ammonia, and making it available to the host plant (Ullah and Bano 2015). This is one of the most mutualistic relationships between a microbe and the plant taking place in soil, where the host plant provides the bacteria with amino acids for the production of ammonia. The enzyme involved in the process of nitrogen fixation is called nitrogenase, while the oxygen is provided by a protein called leghemoglobin, which is produced within the nodules (Vejan et al. 2016). A wide range of PGPR is present in nature and belongs to the genera: Rhizobium, Sinorhizobium, Mesorhizobium, Bradyrhizobium, and Frankia (Masson-Boivin et al. 2009). Although the presence of As adversely affects the process of biological nitrogen fixation, the As-resistant microbes have all managed to cope up with such extreme conditions, hence providing the plants with the requited nitrogen even in the presence of As.
8.6.3.2 Phosphate Solubilization
Plant growth promoting rhizobacteria solubilize insoluble phosphorus in the soil and increase the accessibility of unavailable nutrients to plants. Phosphorus, a key element required for the nutrition of plants, is abundantly present in soil, but its insoluble nature makes it inaccessible to plants. The two soluble forms of phosphate, i.e., monobasic (H2PO4 −) and diabasic (HPO4 −) ions, are readily absorbed by the plants. Rhizobacteria may employ one of the following mechanisms to facilitate the conversion of insoluble forms of phosphorus to soluble forms: release of compounds, for example, organic acid anions to dissolve minerals; production of extracellular enzymes like phosphatases for phosphate solubilization; release of phosphate during substrate degradation, etc. (Kumar et al. 2010). Phosphate solubilizing rhizobacteria are included in the genera Rhodococcus, Bacillus, Serratia, Erwinia, Flavobacterium, Arthrobacter, Pseudomonas, Beijerinckia, Burkholderia, Microbacterium, Rhizobium, and Enterobacter, and are extensively studied to improve plant growth and yield responses. Further, the application of phosphate solubilizing bacteria has also been reported to show many beneficial effects when employed with other metal-resistant rhizospheric microbes for the increased productivity and stability of plants in contaminated soils (Tian et al. 2014).
8.6.3.3 Siderophore Production
The plant’s nutritional requirements of iron are satisfied by specific microorganisms which have evolved precise pathways that employ low molecular weight iron chelators termed siderophores. Siderophores are small peptidic molecules secreted to solubilize iron from their surrounding environments, forming a complex called ferric-siderophore that can move by diffusion (Glick 2012). Siderophores can chelate ferric ion with high affinity, allowing its solubilization and extraction from most mineral or organic complexes. In soil, siderophore production activity plays a central role in determining the ability of different microorganisms to improve plant development (Arora et al. 2013). Microbial siderophores enhance iron uptake by plants that are able to recognize the bacterial ferric-siderophore complex. The highly competitive conditions in the root environment help the plants to selectively use iron for their growth. Siderophore-forming microbes also selectively inhibit the growth of other soil-borne fungal and bacterial pathogens through the release of iron-chelating substances (Dwivedi and Johri 2003). Siderophore-producing bacteria have been extensively studied belonging to the genera Bradyrhizobium, Pseudomonas, Rhizobium, Serratia, and Streptomyces (Sujatha and Ammani 2013). Siderophore-producing metal-resistant microbes are also identified which serve a dual role in soil; they are actively engaged in providing nutrients and helping the plants to survive in heavy metal–contaminated soil (Wani and Khan 2013).
8.6.4 Modulating Phytohormones
A wide range of microorganisms has been found in the rhizosphere which is capable of producing plant growth regulating substances. Plant growth promoting microorganisms produce phytohormones such as auxin(s), cytokinin(s), gibberellin(s), and ethylene, which affect cell proliferation with a subsequent increase in nutrient and water uptake.
8.6.4.1 Cytokinin
Several PGPMs of the genera Azotobacter, Rhizobium, Rhodospirillum, Pseudomonas, Bacillus, and Paenibacillus are known which can produce cytokinins (Glick 2012). However, a detailed understanding of the role of bacterial-synthesized hormones is still unclear; it is believed to provide exogenous and purified hormones to growing plants.
8.6.4.2 Gibberellin
Gibberellin is another hormone actively engaged in regulating plant growth and influencing various developmental processes including stem elongation, germination, dormancy breaking, flowering, sex expression, enzyme induction, and leaf and fruit senescence. Many bacterial species have been identified contributing to the production of this hormone in the soil, thereby promoting plant growth (Glick 2012).
8.6.4.3 Auxin
Although several naturally occurring plant growth regulators, indole-3-acetic acid (IAA) is by far the most common as well as the most studied auxin and much of the scientific concern, exerting a positive effect on root growth. It is evident that up to 80% of root colonizing rhizobacteria can synthesize IAA to stimulate cell proliferation and enhance the uptake of minerals and nutrients from the soil (Gupta et al. 2015). Indole-3-acetic acid not only affects plant cell division, extension, and differentiation but also provides resistance to stressful conditions. An array of metabolically active PGPRs like Pseudomonas, Rhizobium, Bradyrhizobium, Agrobacterium, Enterobacter, and Klebsiella are known to promote root growth in various plant species (Shilev 2013).
8.6.4.4 Ethylene
Ethylene is a key phytohormone having a wide range of biological activities. It affects plant growth and development by promoting root initiation, fruit ripening, seed germination, leaf abscission, and synthesis of other plant hormones, while inhibiting root elongation and wilting (Glick et al. 2007). The enzyme ACC is a prerequisite for ethylene production which is reported to improve dry weight, grain yield, straw production, and nitrogen content in different plant species (Glick 2012; Gupta et al. 2015). Currently, bacterial strains exhibiting ACC deaminase activity have been identified in a wide range of genera such as Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Serratia, and Rhizobium (Kang et al. 2010).
8.6.5 Reducing Oxidative Stress/ Improving Antioxidant Potential
Arsenic induces toxicity in plants that has been linked to the production of reactive oxygen species (ROS), thereby inducing lipid peroxidation and damage to nucleic acids and proteins (Aksakal and Esim 2015; Chandrakar et al. 2016; Chandrakar et al. 2017). Production of ROS in plants is regulated by antioxidative enzymes which remove free radicals thereby protecting the cells from oxidative damage. In the presence of metal-resistant PGPM, the oxidative stress decreases to a considerable level, owing to the reduced uptake of As, thereby balancing the levels of antioxidative enzymes required in the cell (Mishra et al. 2013; Talukdar and Talukdar 2013).
8.6.6 Induced Systemic Resistance
Plant growth promoting microorganisms are capable of controlling diseases that are caused by inhabiting pathogenic bacteria and fungi. The disease is suppressed through Induced Systemic Resistance (ISR) against a broad spectrum of plant pathogens and the production of antibacterial/antifungal metabolites. The production of antibiotics is considered to be one of the most powerful and studied biocontrol mechanisms of PGPR against phytopathogens. The microbial metabolites produced in the rhizosphere help in the reduction of diseases of fungal, bacterial, and/or viral origin, and in some instances even damage caused by insects and nematodes (Choudhary et al. 2007). Beneficial microbes also induce signaling pathways within the plant to stimulate the production of hormones involved in plants defense responses against a variety of pathogens (Haas et al. 2002). A number of bacterial components like lipopolysaccharides (LPS), siderophores, cyclic lipopeptides, and some volatiles are known to encourage ISR, which have now been commercialized to increase the resistance of host plant (Ongena et al. 2004; Ryu et al. 2004). This has led to the genetic modification of many bacterial strains to develop as a bioinoculant to improve plant growth and disease resistance of agricultural crops.
8.6.7 Reducing Arsenic Absorption and Translocation
Metal-resistant PGPR and AMF, particularly those isolated from metalliferous sites, are capable of boosting plant growth by reducing As absorption, changing available As through alteration of soil pH, and by affecting As translocation (Rajkumar et al. 2012). Moreover, As accumulation in plant tissues is more likely to be associated with the availability of As in the soil. The presence of microbial population is known to significantly decrease the uptake and accumulation of As in plant tissues even in the As rich soil, may be due to the microbial uptake of a metalloid. It is well established that the presence of the beneficial bacteria/fungi not only colonizes the roots of the plants but also decreases the uptake of As in tissues, thereby helping the plants to grow and propagate at high concentrations of As (Wani and Khan 2013; Mallick et al. 2014; Selamat et al. 2014).
8.6.8 Enhancing Plant Growth and Biomass
Certain bacterial strains synthesize a wide spectrum of multifunctional exopolysaccharide (EPS) in response to the heavy metals. Exopolysaccharide is a mode of protecting bacteria from desiccation, environmental stress, and plant defense responses in plant-microbe interactions (Limoli et al. 2015). This class of polysaccharide also helps plants to flourish in As stressed soil in many different ways. Production of EPS is known to assist in biofilm formation, attachment to plant surface, root colonization, holding free phosphorus in soils, cation binding including Na+, circulating essential nutrients to the plant for proper growth and development, and protecting it from the attack of foreign pathogens (Vu et al. 2009; Gupta et al. 2015). This indicates the importance of PGPR producing EPS in promoting plant growth and biomass production by establishing beneficial interactions, satisfying environmental stress. and providing defense response during the infection process.
8.6.9 Improving Plant Establishment in Contaminated Soils
The association of As-resistant PGPMs with the roots opens new ways in securing the host plant not only against As but also from the deleterious effects of other cross contaminating heavy metals. The metal-resistant systems in bacteria/fungi enable them to limit the availability of metals to plants by producing and transporting inorganic phosphate and other growth-promoting substances from the soil. Further, the efflux of As from the host plant is absorbed by the microbes residing in the roots, thereby ensures reabsorption of As decreasing the overall metal concentration of the soil. The AMF may also act as a filter to maintain low plant As levels while maintaining an adequate supply of phosphorus to the host (Liu et al. 2005; Chen et al. 2007; Xia et al. 2007; Xu et al. 2008).
8.7 Microbial Technologies for the Alleviation of Arsenic Effects in Plants
8.7.1 Enzyme Technology
Among biological agents, enzymes have a great potential to effectively transform and detoxify environmental pollutants (Rao et al. 2010). Biocatalysts may serve as an alternate method for As remediation, and recently, there has been increasing interest in their potential applications. Enzymes could provide a more specific and clean way of dealing with the toxic metalloid, As (Dhankher et al. 2002; Bahar et al. 2012). Many microorganisms are known to produce enzymes involved in As detoxification, which could be successfully extracted and used for the remediation purposes. Enzymes in their immobilized forms are drawing significant attention for potential applications in As removal due to the reducing operational expenses and the increased process utilization of the enzymes (Talat et al. 2009). Typically, immobilized enzymes have greater thermal and operational stability at various pH values, ionic strengths and are more resistant to denaturation than the soluble native form of the enzyme (Bayramoglu et al. 2013). Similarly, immobilized biocatalyst displays the property of recycling and offer continued activity and stability for being reused many times (Eş et al. 2015).
However, the use of nanoparticle as supporting material for immobilized enzymes of microbial origin is drawing great attention to other materials. It provides many advantages such as the higher surface area that allows greater enzyme loading, higher stability and lower mass transfer resistance (Ho et al. 2008; Ansari and Husain 2012). The selectivity and increased activity of the immobilized enzymes could be utilized on a large scale for the improved As removal from soil and treatment process.
8.7.2 Genetic Engineering
The severity of the As contamination had raised an alarming situation demanding immediate attention and novel methods of remediation. The method of genetic engineering could be a potential strategy to overcome the drawbacks of this toxic metalloid. Many studies have been undertaken for the improvement of As methylation and detoxification abilities of the microbes by successful expression of the target gene (Qin et al. 2006; Yuan et al. 2008; Chen et al. 2014; Huang et al. 2015). These recombinant bacteria had 10-fold increase in response and resistance toward As and showed the successful transformation of inorganic As into less toxic organoarsenicals when compared to wild-type strains (Liu et al. 2011). This demonstrates the potential application of genetically engineered microorganisms as an efficient strategy for As bioremediation from contaminated soil (Liu et al. 2011), thereby reducing its translocation and accumulation in food stuff (Chen et al. 2013).
8.8 Conclusions and Prospects
The uniqueness of microorganisms and their often unpredictable nature and biosynthetic competences have made them promising candidates for solving As stress in different plant species. The conscientious use of indigenous microorganisms with the advanced technologies and modern techniques would attract economic, social, and environmental benefits which would provide an efficient way to protect the ecosystem. Microbial populations are known to affect As mobility and availability to the plant and therefore have potential to enhance phytoremediation processes. The advances in exploring and utilizing the significance of As-resistant rhizobacteria and AMF would be the simplest phenomenon to protect crops from As, as they may prevent the transport of As from root to shoot, thereby decreasing its uptake by plants. There is an urgent need to improve our understanding of the mechanisms involved in the transfer and mobilization of As by PGPRs and AMF, and to conduct research on the selection of microbial isolates from the rhizosphere of plants growing on As-contaminated soils for specific restoration programs.
References
Aksakal O, Esim N (2015) Evaluation of arsenic trioxide genotoxicity in wheat seedlings using oxidative system and RAPD assays. Environ. Sci Pollut Res 22:7120–7128
Álvarez-Ayuso E, Abad-Valle P, Murciego A, Villar-Alonso P (2015) Arsenic distribution in soils and rye plants of a cropland located in an abandoned mining area. Sci Total Environ 542:238–246
Ansari SA, Husain Q (2012) Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol Adv 30:512–523
Ao L, Zeng XC, Nie Y, Mu Y, Zhou L, Luo X (2014) Flavobacterium arsenatis sp. nov., a novel arsenic-resistant bacterium from high-arsenic sediment. Int J Syst Evol Microbiol 64:3369–3374
Arora NK, Tewari S, Singh R (2013) Multifaceted plant-associated microbes and their mechanisms diminish the concept of direct and indirect PGPRs. In: Arora NK (ed) Plant microbe Symbiosis: fundamentals and advances. Springer, New Delhi, pp 411–449
Bahar MM, Megharaj M, Naidu R (2012) Arsenic bioremediation potential of a new arsenite-oxidizing bacterium Stenotrophomonas sp. MM-7 isolated from soil. Biodegradation 23:803–812
Banerjee S, Datta S, Chattyopadhyay D, Sarkar P (2011) Arsenic accumulating and transforming bacteria isolated from contaminated soil for potential use in bioremediation. J Environ Sci Health A Tox Hazard Subst Environ Eng 46:1736–1747
Banerjee S, Majumdar J, Samal AC, Bhattachariya P, Santra SC (2013) Biotransformation and bioaccumulation of arsenic by Brevibacillus brevis isolated from arsenic contaminated region of West Bengal. J Environ Sci Toxicol Food Technol 3:1–10
Batool K, Tuz Zahra F, Rehman Y (2017) Arsenic-redox transformation and plant growth promotion by purple nonsulfur bacteria Rhodopseudomonas palustris CS2 and Rhodopseudomonas faecalis SS5. Biomed Res Int 2017:6250327. https://doi.org/10.1155/2017/6250327
Bayramoglu G, Altintas B, Arica MY (2013) Immobilization of glucoamylase onto polyaniline-grafted magnetic hydrogel via adsorption and adsorption/cross-linking. Appl Microbiol Biotechnol 97:1149–1159
Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051
Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271
Bhargavi SD, Savitha J (2014) Arsenate resistant Penicillium coffeae: a potential fungus for soil bioremediation. Bull Environ Contam Toxicol 92:369–373
Bhat S, Luo X, Xu Z, Liu L, Zhang R (2011) Bacillus sp. CDB3 isolated from cattle dip sites possesses two ars gene clusters. J Environ Sci 23:95–101
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Ca’novas D, Vooijs R, Schat H, de Lorenzo V (2004) The role of thiol species in the Hypertolerance of Aspergillus sp. P37 to Arsenic. J Biol Chem 279:51234–51240
Cai L, Rensing C, Li X, Wang G (2009) Novel gene clusters involved in arsenite oxidation and resistance in two arsenite oxidizers: Achromobacter sp. SY8 and Pseudomonas sp. TS44. Appl Microbiol Biotechnol 83:715–725
Cavalca L, Zanchi R, Corsini A, Colombo M, Romagnoli C, Canzi E, Andreoni V (2010) Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. Syst Appl Microbiol 33:154–164
Cavalca L, Corsini A, Bachate SP, Andreoni V (2013) Rhizosphere colonization and arsenic translocation in sunflower (Helianthus annuus L.) by arsenate reducing Alcaligenes sp. strain Dhal-L. World J Microbiol Biotechnol 29:1931–1940
Cernanský S, Kolencík M, Sevc J, Urík M, Hiller E (2009) Fungal volatilization of trivalent and pentavalent arsenic under laboratory conditions. Bioresour Technol 100:1037–1040
Chandrakar V, Naithani SC, Keshavkant S (2016) Arsenic-induced metabolic disturbances and their mitigation mechanisms in crop plants: a review. Biologia 71:367–377
Chandrakar V, Yadu B, Meena RK, Dubey A, Keshavkant S (2017) Arsenic-induced genotoxic responses and their amelioration by diphenylene iodonium, 24-epibrassinolide and proline in Glycine max L. Plant Physiol Biochem 112:74–86
Chen B, Xiao X, Zhu YG, Smith FA, Xie ZM, Smith SE (2007) The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Sci Total Environ 379:226–234
Chen J, Qin J, Zhu YG, de Lorenzo V, Rosen BP (2013) Engineering the soil bacterium Pseudomonas putida for arsenic methylation. Appl Environ Microbiol 79:4493–4495
Chen J, Sun GX, Wang XX, Vd L, Rosen BP, Zhu YG (2014) Volatilization of arsenic from polluted soil by Pseudomonas putida engineered for expression of the arsM Arsenic(III) S-adenosine methyltransferase gene. Environ Sci Technol 48:10337–10344
Choe S-I, Gravelat FN, Abdallah QA, Lee MJ, Gibbs BF, Sheppard DC (2012) Role of Aspergillus niger acrA in arsenic resistance and its use as the basis for an arsenic biosensor. Appl Environ Microbiol 78:3855–3863
Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47:289–297
Cuebas M, Villafane A, McBride M, Yee N, Bini E (2011) Arsenate reduction and expression of multiple chromosomal ars operons in Geobacillus kaustophilus A1. Microbiology 157:2004–2011
Das S, Jean JS, Chou M (2015) Arsenite-oxidizing bacteria exhibiting plant growth promoting traits isolated from the rhizosphere of Oryza sativa L.: implications for mitigation of arsenic contamination in paddies. J Hazard Mater 302:10–18
Das S, Jean JS, Chou ML, Rathod J, Liu CC (2016) Arsenite-oxidizing bacteria exhibiting plant growth promoting traits isolated from the rhizosphere of Oryza sativa L.: implications for mitigation of arsenic contamination in paddies. J Hazard Mater 302:10–18
Deepika KV, Raghuram M, Kariali E, Bramhachari PV (2016) Biological responses of symbiotic Rhizobium radiobacter strain VBCK1062 to the arsenic contaminated rhizosphere soils of mung bean. Ecotoxicol Environ Saf 134:1–10
Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394
Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145
Dhuldhaj UP, Yadav IC, Singh S, Sharma NK (2013) Microbial interactions in the arsenic cycle: adoptive strategies and applications in environmental management. Rev Environ Contam Toxicol 224:1–38
Drewniak L, Dziewit L, Ciezkowska M, Gawor J, Gromadka R, Sklodowska A (2013) Structural and functional genomics of plasmid pSinA of Sinorhizobium sp. M14 encoding genes for the arsenite oxidation and arsenic resistance. J Biotechnol 164:479–488
Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: biosynthesis and regulation. Curr Sci 12:1693–1703
Eş I, Vieira JD, Amaral AC (2015) Principles, techniques, and applications of biocatalyst immobilization for industrial application. Appl Microbiol Biotechnol 99:2065–2082
Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil rhizosphere plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278
Garelick H, Jones H, Dybowska A, Valsami-Jones E (2008) Arsenic pollution sources. Rev Environ Contam Toxicol 197:17–60
Ghosh S, Sar P (2013) Identification and characterization of metabolic properties of bacterial populations recovered from arsenic contaminated ground water of North East India (Assam). Water Res 47:6992–7005
Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci 96:5001–5006
Ghosh P, Rathinasabapathi B, Ma LQ (2011) Arsenic-resistant bacteria solubilized arsenic in the growth media and increased growth of arsenic hyperaccumulator Pteris vittata L. Bioresour Technol 102:8756–8761
Ghosh P, Rathinasabapathi B, Ma LQ (2015) Phosphorus solubilization and plant growth enhancement by arsenic-resistant bacteria. Chemosphere 134:1–6
Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the Symbiosis. Plant Cell 8:1871–1883
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401. https://doi.org/10.6064/2012/963401
Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242
Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting Rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102
Haas D, Keel C, Reimann C (2002) Signal transduction in plant beneficial rhizobacteria with biocontrol properties. Antonie van Leeuw 81:385–395
Heinrich A (2007) Biosorption and biovolatilization of arsenic by heat-resistant fungi. Environ Sci Pollut Res Int 14:31–35. (5 pp)
Ho KM, Mao X, Gu L, Li P (2008) Facile route to enzyme immobilization: core-shell nanoenzyme particles consisting of well-defined poly(methyl methacrylate) cores and cellulose shells. Langmuir 24:11036–11042
Huang K, Chen C, Shen Q, Rosen BP, Zhao FJ (2015) Genetically engineering Bacillus subtilis with a heat-resistant arsenite methyltransferase for bioremediation of arsenic-contaminated organic waste. Appl Environ Microbiol 81:6718–6724
Hudson-Edwards KA, Santini JM (2013) Arsenic-microbe-mineral interactions in mining-affected environments. Fortschr Mineral 3:337–351
Islam SM, Fukushi K, Yamamoto K, Saha GC (2007) Estimation of biologic gasification potential of arsenic from contaminated natural soil by enumeration of arsenic methylating bacteria. Arch Environ Contam Toxicol 52:332–338
Jankong P, Visoottiviseth P (2008) Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere 72:1092–1097
Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160:778–788
Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183
Kao AC, Chu YJ, Hsu FL, Liao VH (2013) Removal of arsenic from groundwater by using a native isolated arsenite-oxidizing bacterium. J Contam Hydrol 155:1–8
Karn SK, Pan X, Jenkinson IR (2017) Bio-transformation and stabilization of arsenic (As) in contaminated soil using arsenic oxidizing bacteria and FeCl3 amendment. 3 Biotech 7:50. https://doi.org/10.1007/s13205-017-0681-1
Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364
Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One 10:e0128784. https://doi.org/10.1371/journal.pone.0128784
Kruger MC, Bertin PN, Heipieper HJ, Arsène-Ploetze F (2013) Bacterial metabolism of environmental arsenic mechanisms and biotechnological applications. Appl Microbiol Biotechnol 97:3827–3841
Kumar A, Bhargava P, Rai LC (2010) Isolation and molecular characterization of phosphate solubilizing Enterobacter and Exiguobacterium species from paddy fields of eastern Uttar Pradesh, India. Afr J Microbiol Res 4:820–829
Kuramata M, Sakakibara F, Kataoka R, Abe T, Asano M, Baba K, Takagi K, Ishikawa S (2015) Arsenic biotransformation by Streptomyces sp. isolated from rice rhizosphere. Environ Microbiol 17:1897–1909
Lakshmanan V, Shantharaj D, Li G, Seyfferth AL, Janine Sherrier D, Bais HP (2015) A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta 242:1037–1050
Lampis S, Santi C, Ciurli A, Andreolli M, Vallini G (2015) Promotion of arsenic phytoextraction efficiency in the fern Pteris vittata by the inoculation of As-resistant bacteria: a soil bioremediation perspective. Front Plant Sci 6:80. https://doi.org/10.3389/fpls.2015.00080
Li B, Lin J, Mi S, Lin J (2010) Arsenic resistance operon structure in Leptospirillum ferriphilum and proteomic response to arsenic stress. Bioresour Technol 101:9811–9814
Li P, Wang Y, Dai X, Zhang R, Jiang Z, Jiang D, Wang S, Jiang H, Wang Y, Dong H (2015) Microbial community in high arsenic shallow groundwater aquifers in Hetao Basin of Inner Mongolia, China. PLoS One 10:e0125844. https://doi.org/10.1371/journal.pone.0125844
Liao VH, Chu YJ, Su YC, Hsiao SY, Wei CC, Liu CW, Liao CM, Shen WC, Chang FJ (2011) Arsenite oxidizing and arsenate reducing bacteria associated with arsenic rich groundwater in Taiwan. J Contam Hydrol 123:20–29
Lièvremont D, Bertin PN, Lett MC (2009) Arsenic in contaminated waters: biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91:1229–1237
Limoli DH, Jones CJ, Wozniak DJ (2015) Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr 3:10. https://doi.org/10.1128/microbiolspec.MB-0011-2014
Liu Y, Zhu YG, Chen BD, Christie P, Li XL (2005) Yield and arsenate uptake of arbuscular mycorrhizal tomato colonized by Glomus mosseae BEG167 in As spiked soil under glasshouse conditions. Environ Int 31:867–873
Liu S, Zhang F, Chen J, Sun G (2011) Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions. J Environ Sci 23:1544–1550
Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918. https://doi.org/10.3389/fpls.2016.00918
Majumder A, Ghosh S, Saha N, Kole SC, Sarkar S (2013) Arsenic accumulating bacteria isolated from soil for possible application in bioremediation. J Environ Biol 34:841–846
Mallick I, Hossain ST, Sinha S, Mukherjee SK (2014) Brevibacillus sp. KUMAs2, a bacterial isolate for possible bioremediation of arsenic in rhizosphere. Ecotoxicol Environ Saf 107:236–244
Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466
Mateos LM, Ordóñez E, Letek M, Gil JA (2006) Corynebacterium glutamicum as a model bacterium for the bioremediation of arsenic. Int Microbiol 9:207–215
de Melo RW, Schneider J, de Souza CE, Sousa SC, Guimarães GL, de Souza MF (2014) Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int J Phytoremediation 16:840–858
Mishra S, Srivastava S, Dwivedi S, Tripathi RD (2013) Investigation of biochemical responses of Bacopa monnieri L. upon exposure to arsenate. Environ Toxicol 28:419–430
Moreno-Jiménez E, Esteban E, Peñalosa JM (2012) The fate of arsenic in soil-plant systems. Rev Environ Contam Toxicol 215:1–37
Mukhopadhyay R, Shi J, Rosen BP (2000) Purification and characterization of ACR2p, the Saccharomyces cerevisiae arsenate reductase. J Biol Chem 275:21149–21157
Nagvenkar GS, Ramaiah N (2010) Arsenite tolerance and biotransformation potential in estuarine bacteria. Ecotoxicology 19:604–613
Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipooxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant-Microbe Interact 17:1009–1018
Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49
Páez-Espino D, Tamames J, de Lorenzo V, Cánovas D (2009) Microbial responses to environmental arsenic. Biometals 22:117–130
Pandey N, Bhatt R (2015) Arsenic resistance and accumulation by two bacteria isolated from a natural arsenic contaminated site. J Basic Microbiol 55:1275–1286
Pandey N, Bhatt R (2016) Arsenic removal and biotransformation potential of Exiguobacterium isolated from an arsenic- rich soil of Chhattisgarh, India. Clean (Weinh) 44:211–218
Paul D, Poddar S, Sar P (2014) Characterization of arsenite-oxidizing bacteria isolated from arsenic contaminated groundwater of West Bengal. J Environ Sci Health A Tox Hazard Subst Environ Eng 49:1481–1492
Paul D, Kazy SK, Gupta AK, Pal T, Sar P (2015) Diversity, metabolic properties and arsenic mobilization potential of indigenous bacteria in arsenic contaminated groundwater of West Bengal, India. PLoS One 10:e0118735. https://doi.org/10.1371/journal.pone.0118735
Pepi M, Volterrani M, Renzi M, Marvasi M, Gasperini S, Franchi E, Focardi SE (2007) Arsenic resistant bacteria isolated from contaminated sediments of the Orbetello Lagoon, Italy, and their characterization. J Appl Microbiol 103:2299–2308
Qamar N, Rehman Y, Hasnain S (2017) Arsenic-resistant and plant growth-promoting Firmicutes and γ-Proteobacteria species from industrially polluted irrigation water and corresponding cropland. J Appl Microbiol 123:748–758
Qin J, Rosen BP, Zhang Y, Wang G, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci 103:2075–2080
Rahman MA, Hassler C (2014) Is arsenic biotransformation a detoxification mechanism for microorganisms? Aquat Toxicol 146:212–219
Rahman A, Nahar N, Nawani NN, Jass J, Desale P, Kapadnis BP, Hossain K, Saha AK, Ghosh S, Olsson B, Mandal A (2014) Isolation and characterization of a Lysinibacillus strain B1-CDA showing potential for bioremediation of arsenics from contaminated water. J Environ Sci Health A Tox Hazard Subst Environ Eng 49:1349–1360
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant associated microbes in heavy metal phytoremediation. Biotech Adv 30:1562–1574
Rao MA, Scelza R, Scotti R, Gianfreda L (2010) Role of enzymes in the remediation of polluted environments. J Soil Sci Plant Nutr 10:333–353
Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Rosen BR, Liu ZJ (2009) Transport pathways for arsenic and selenium: a minireview. Environ Int 35:512–515
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026
Sarkar A, Kazy SK, Sar P (2013) Characterization of arsenic resistant bacteria from arsenic rich groundwater of West Bengal, India. Ecotoxicology 22:363–376
Schneider J, Stürmer SL, Guilherme LR, de Souza Moreira FM, Soares CR (2013a) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115
Schneider J, Labory CR, Rangel WM, Alves E, Guilherme LR (2013b) Anatomy and ultrastructure alterations of Leucaena leucocephala (Lam.) inoculated with mycorrhizal fungi in response to arsenic-contaminated soil. J Hazard Mater 262:1245–1258
Schneider J, Bundschuh J, Rangel WM, Guilherme LR (2017) Potential of different AM fungi (native from As-contaminated and uncontaminated soils) for supporting Leucaena leucocephala growth in As-contaminated soil. Environ Pollut 224:125–135
Selamat SN, Abdullah SR, Idris M (2014) Phytoremediation of lead (Pb) and arsenic (As) by Melastoma malabathricum L. from contaminated soil in separate exposure. Int J Phytoremediation 16:694–703
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Shagol CC, Krishnamoorthy R, Kim K, Sundaram S, Sa T (2014) Arsenic-tolerant plant-growth-promoting bacteria isolated from arsenic-polluted soils in South Korea. Environ Sci Pollut Res Int 21:9356–9365
Shakya S, Pradhan B, Smith L, Shrestha J, Tuladhar S (2012) Isolation and characterization of aerobic culturable arsenic resistant bacteria from surface water and groundwater of Rautahat District, Nepal. J Environ Manag 95:250–255
Sharma S, Anand G, Singh N, Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Front. Plant Sci 8:906. https://doi.org/10.3389/fpls.2017.00906
Sharples JM, Meharg AA, Chambers SM, Cairney JWG (2000) Mechanism of arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. Plant Physiol 124:1327–1334
Sheik CS, Mitchell TW, Rizvi FZ, Rehman Y, Faisal M, Hasnain S, McInerney MJ, Krumholz LR (2012) Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS One 7:e40059. https://doi.org/10.1371/journal.pone.0040059
Shilev S (2013) Soil rhizobacteria regulating the uptake of nutrients and undesirable elements by plants. In: Arora NK (ed) Plant microbe symbiosis: fundamentals and advances. Springer, New Delhi, pp 147–167
Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608
Singh M, Srivastava PK, Verma PC, Kharwar RN, Singh N, Tripathi RD (2015) Soil fungi for mycoremediation of arsenic pollution in agriculture soils. J Appl Microbiol 119:1278–1290
Singh N, Marwa N, Mishra SK, Mishra J, Verma PC, Rathaur S, Singh N (2016) Brevundimonas diminuta mediated alleviation of arsenic toxicity and plant growth promotion in Oryza sativa L. Ecotoxicol Environ Saf 125:25–34
Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442
Srivastava PK, Shenoy BD, Gupta M, Vaish A, Mannan S, Singh N, Tewari SK, Tripathi RD (2012) Stimulatory effects of arsenic-tolerant soil fungi on plant growth promotion and soil properties. Microbes Environ 27:477–482
Srivastava S, Verma PC, Chaudhry V, Singh N, Abhilash PC, Kumar KV, Sharma N, Singh N (2013) Influence of inoculation of arsenic-resistant Staphylococcus arlettae on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J Hazard Mater 262:1039–1047
Stolz JF, Basu P, Oremland RS (2002) Microbial transformation of elements: the case of arsenic and selenium. Int Microbiol 5:201–207
Su S, Zeng X, Bai L, Li L, Duan R (2011) Arsenic biotransformation by arsenic-resistant fungi Trichoderma asperellum SM-12F1, Penicillium janthinellum SM-12F4, and Fusarium oxysporum CZ-8F1. Sci Total Environ 409:5057–5062
Sujatha N, Ammani K (2013) Siderophore production by the isolates of fluorescent Pseudomonads. Int J Cur Res Rev 5:1–7
Sun Y, Zhang X, Wu Z, Hu Y, Wu S, Chen B (2016) The molecular diversity of arbuscular mycorrhizal fungi in the arsenic mining impacted sites in Hunan Province of China. J Environ Sci 39:110–118
Tak HI, Ahmad F, Babalola OO (2013) Advances in the application of plant growth-promoting rhizobacteria in phytoremediation of heavy metals. Rev Environ Contam Toxicol 223:33–52
Talat M, Prakash O, Hasan SH (2009) Enzymatic detection of As(III) in aqueous solution using alginate immobilized pumpkin urease: optimization of process variables by response surface methodology. Bioresour Technol 100:4462–4467
Talukdar T, Talukdar D (2013) Response of antioxidative enzymes to arsenic induced phytotoxicity in leaves of a medicinal daisy, Wedelia chinensis Merrill. J Nat Sci Biol Med 4:383–388
Tian J, Peng XW, Li X, Sun YJ, Feng HM, Jiang ZP (2014) Isolation and characterization of two bacteria with heavy metal resistance and phosphate solubilizing capability. Huan Jing Ke Xue 35:2334–2340
Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotechnol 20:659–667
Ullah S, Bano A (2015) Isolation of plant-growth-promoting rhizobacteria from rhizospheric soil of halophytes and their impact on maize (Zea mays L.) under induced soil salinity. Can J Microbiol 61:307–313
Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 21:573. https://doi.org/10.3390/molecules21050573
Vishnoi N, Singh DP (2014) Biotransformation of arsenic by bacterial strains mediated by oxido-reductase enzyme system. Cell Mol Biol 60:7–14
Viveros OM, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554
Wang G, Huang Y, Li J (2011) Bacteria live on arsenic analysis of microbial arsenic metabolism- a review. Acta Microbiol Sin 51:154–160
Wang Z, Luo Z, Yan C (2013) Accumulation, transformation, and release of inorganic arsenic by the freshwater cyanobacterium Microcystis aeruginosa. Environ Sci Pollut Res Int 20:7286–7295
Wang PP, Bao P, Sun GX (2015) Identification and catalytic residues of the arsenite methyltransferase from a sulfate-reducing bacterium, Clostridium sp BXM. FEMS Microbiol Lett 362:1–8
Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124
Wysocki R, Bobrowicz P, Ulaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem 272:30061–30066
Xia YS, Chen BD, Christie P, Smith FA, Wang YS, Li XL (2007) Arsenic uptake by arbuscular mycorrhizal maize (Zea mays L.) grown in an arsenic-contaminated soil with added phosphorus. J Environ Sci 19:1245–1251
Xu P, Christie P, Liu Y, Zhang J, Li X (2008) The arbuscular mycorrhizal fungus Glomus mosseae can enhance arsenic tolerance in Medicago truncatula by increasing plant phosphorus status and restricting arsenate uptake. Environ Pollut 156:215–220
Yuan C, Lu X, Qin J, Rosen BP, Le XC (2008) Volatile arsenic species released from Escherichia coli expressing the AsIII S-adenosylmethionine methyltransferase gene. Environ Sci Technol 42:3201–3206
Zhang Z, Yin N, Cai X, Wang Z, Cui Y (2016) Arsenic redox transformation by Pseudomonas sp. HN2 isolated from arsenic contaminated soil in Hunan, China. J Environ Sci 47:165–173
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794
Acknowledgments
Authors are grateful to Science and Engineering Research Board, New Delhi; Department of Science and Technology, New Delhi; and Chhattisgarh Council of Science and Technology, Raipur, for providing financial assistance/research project to Neha Pandey, Vibhuti Chandrakar, and S. Keshavkant, respectively.
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Pandey, N., Chandrakar, V., Keshavkant, S. (2018). Mitigating Arsenic Toxicity in Plants: Role of Microbiota. In: Hasanuzzaman, M., Nahar, K., Fujita, M. (eds) Mechanisms of Arsenic Toxicity and Tolerance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-1292-2_8
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