Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii
Graphical abstract
Introduction
Arsenic pollution is a serious environmental problem throughout the world (Meharg, 2004, Pandey, 2006). Various drinking wells of Bangladesh and a large part of East India, mainly the regions in West Bengal are contaminated with arsenic and thus causing large-scale exposure of arsenic to population directly by drinking of water and indirectly through consumption of food grown in soil and water contaminated with arsenic (Rahman et al., 2014, Chakraborti et al., 2015). The soaking of croplands by arsenic-contaminated water causes its accumulation in the soil (Abedin et al., 2002) and thus leading to arsenic uptake by plants. Soil content of arsenic may alter depending upon the severity of the contamination (Singh and Ma, 2007) and may rise to a concentration as high as 2600 mg kg− 1 in the soil of mineralized zones (Meharg et al., 1994b). Arsenic is also found in plant edible parts such as fruits, leaves and seeds and hence they become unsafe for human consumption (Rosas-Castor et al., 2014).
Arsenic interferes with the plant's metabolism resulting in disorders at several organizational levels and inhibits plant growth (Marin et al., 1993, Meharg, 1994). Once arsenic enters into plant cells, it causes damage to plant parts in several ways which include interference in aerobic phosphorylation and reduction of arsenate to arsenite inside the plant cells, targeting sulfhydryl groups of proteins (Schmoger et al., 2000). Arsenic causes interference in plant metabolism as it competes with phosphate [PO43 −]. Since PO43 − and arsenate [AsO43 −] have similar structures both are carried by the PO43 − transporters in plants (Han et al., 2016). Arsenic produces adenosine diphosphate (ADP)–As, in place of adenosine triphosphate (ATP) and energy flow is disrupted in plant cells (Meharg, 1994). This causes a reduction in plant growth and yield (Carbonell-Barrachina et al., 1995), discoloration of roots, leaf necrosis, root plasmolysis and a decrease in photosynthetic capacity of a plant (Marin et al., 1993, Meharg, 1994). Therefore arsenic gets entry into plant edible parts such as fruits, leaves, and seeds (Abedin et al., 2002). The concentration of arsenic varies based on the type of plant species (Cobb et al., 2000). It has also been known that soil arsenic interferes in uptake and accumulation of minerals into plant shoots and seeds (Paivoke and Simola, 2002, Milivojevic et al., 2006) and their nutritional composition may be influenced (Tu and Ma, 2005).
Contamination and poisoning caused by arsenic (arsenicosis) cause diseases like skin lesions, skin cancer, bladder, kidneys, and lung cancer, high blood pressure, blindness, partial paralysis and reproductive disorders (Chatterjee and De, 2015, Das and Sarkar, 2016, Álvarez-Ayuso et al., 2016, Mir et al., 2007). Pteris vittata (brake fern) is the first known hyperaccumulator of arsenic. The growth of Pteris vittata can be enhanced by the presence of arsenic as much as 46% (Xu et al., 2014). Other ferns, like P. cretica, P. umbrosa, and P. longifolia are also able to grow properly in arsenic polluted soils and accumulate a large amount of arsenic in their fronds (Ma et al., 2001, Meharg, 2003).
Although several detoxification methods such as containment, stabilization, and solidification etc. have been proposed for the remediation of onsite polluted soils, appropriate controls are needed by all of these methods and long-term monitoring to ensure the behavior of arsenic through soil column (Chang et al., 2011). Significant importance is given to arsenic-tolerant bacteria having plant growth promoting (PGP) traits and capability to arrest arsenic uptake, pollution (Das et al., 2016). The application of arsenic utilizing bacteria for bioremediation is an eco-friendly and cost-effective process if compared with other techniques (Das et al., 2016). Rhizospheric microbes interact with plants influencing their growth, increasing water uptake and mineral with the production of antimicrobial compounds to inhibit soil pathogens and produce plant growth regulators (Mishra et al., 2009).
Mung bean (Vigna radiata) is a rich source of seed proteins. Some studies reported growth of mung bean in an arsenic-contaminated environment (Singh et al., 2007). Arsenic causes the reduction in both seed germination and growth of mung bean plants causing loss of crop productivity and hence it is toxic for mung bean. There are reports showing that bacteria inoculation has abated arsenic toxicity in economically important crops like rice (Oryza sativa L.) (Das et al., 2016, Lakshmanan et al., 2015), chickpea (Cicerarietinum L.) (Srivastava and Singh, 2014), Indian mustard plant (Brassica juncea (L.) Czernetc.) (Srivastava et al., 2013) etc. However, the study related to detailed effects of microbes on the growth and crop yield of mung bean grown in the arsenic-contaminated area is largely unexcavated.
In the current study, the isolated soil bacterium Acinetobacter lwoffii (RJB-2) (Banerjee et al., 2011) exhibit minimum inhibitory concentrations (MIC) of 125 mM (i.e. 9365.25 mg L− 1/9365.25 mg kg− 1) of arsenate [As(V)] and 50 mM (3746.1 mg L− 1/3746.1 mg kg− 1) of arsenite [As(III)]. Arsenic detoxification mechanisms in bacterial cells are responsible for these (Kitja et al., 2009, Srivastava et al., 2012). The mechanisms that have evolved in bacteria for resisting or detoxifying metals can be classified as sequestration, exclusion, efflux, bioaccumulation, enzymatic action and reduction (Silver and Phung, 1996, Srivastava et al., 2012). Microbial arsenic detoxification mechanisms include As(V) uptake in the form of phosphate by phosphate transporters, As(III) uptake in the form of arsenite by aquaglyceroporins (Banerjee et al., 2016, Satyapal et al., 2016). There is an important role of the “Ars” operon in arsenic detoxification in bacterial cells (Srivastava et al., 2012). The product of the arsC gene in “Ars” operon i.e. a cytoplasmic arsenate reductase, catalyzes the reduction of As(V) to As(III). Some bacteria can perform oxidation and methylation of As(III) by arsenite oxidase and methyltransferase respectively. They can also extrude or sequester As(III). In this way, the arsenic-tolerant rhizospheric microbes present in soil can remediate arsenic toxin and simultaneously stop plant arsenic uptake.
The aim of the present study was to determine the effects of inoculation of arsenic resistant bacterial strain Acinetobacter lwoffii (RJB-2) on the growth promotion and yield of mung bean plants (Vigna radiata) under arsenic stressed condition and to investigate the extent of arsenic uptake and its distribution in various plant parts.
Section snippets
Isolation and characterization of bacterial strain from arsenic contaminated soil
The bacterium RJB-2 (Acinetobacter lwoffii) was isolated from the soil samples collected from the arsenic contaminated region of village Chakdah, North 24 Parganas, West Bengal, India (Banerjee et al., 2011). RJB-2 was screened for arsenic resistance assay. 16 s rRNA sequencing of RJB-2 (Acinetobacter lwoffii) was already performed by Banerjee et al., 2011. The strain possesses minimum inhibitory concentrations of 125 mM (i.e. 9365.25 mg L− 1/9365.25 mg kg− 1) of arsenate [As(V)] and 50 mM (3746.1 mg L− 1
Morphological characteristics and numbers of plants per pot of mung bean plants
Significant decrements in morphological aspects, as well as numbers of plants per pot of mung bean plants, had been observed when grown in arsenic-contaminated [22.5 mg kg− 1of Na2HAsO4·7H2O i.e. 5.4 mg kg− 1 of As(V)] soil (CCAs) (Figs. 2a, b, 3). The root length, shoot length (Fig. 2a), plant fresh weight, dry stem weight and plant biomass in presence of arsenic [22.5 mg kg− 1 of Na2HAsO4·7H2O] were compared with those obtained from CBAs (Fig. 3). When the bacterial strain RJB-2 was treated in the
Conclusions
The results of the present study clearly indicated that the inoculated bacterium RJB-2 (Acinetobacter lwoffii) was highly efficient in protecting the crop plant (Vigna radiata) against the toxic effects of arsenic. Moreover, the isolated bacterium was highly arsenic tolerant and produced plant growth promoting substances like IAA, exopolysaccharide (EPS), and siderophores and also showed phosphate solubilization activity in the absence and even in the presence of high concentration of As(V) [up
Acknowledgements
The authors are thankful to DBT IPLS (Department of Biochemistry, Ballygunge Science College)-University of Calcutta, Kolkata, West Bengal, India for providing Confocal microscopic facilities. The authors are also thankful to Mr. Prothyush Sengupta, Centre for Research in Nanoscience and Nanotechnology, Calcutta University, Kolkata, India and Mr. Krishnendu Paramanik, CIT, Howrah, West Bengal, India for performing SEM imaging studies and for helping in conductivity measurement studies
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