Assisted phytoremediation of chromium spiked soils by Sesbania Sesban in association with Bacillus xiamenensis PM14: A biochemical analysis

Highlights

• First time reported the heavy metal tolerance and assisted phytoremediation by B. xiamenensis.

• Potential of S. sesban against contaminated soils was investigated from Pakistan.

• Increased metal tolerance of Sesbania in association with B. xiamenensis is reported first time.

• Inoculated plants have positive effects on growth and metals accumulation by S. sesban.

Abstract

Due to anthropogenic activities, chromium (Cr) contamination is ubiquitous with deleterious effects on plant and soil microbiota. Present study was designed to address beneficial effects of Bacillus xiamenensis PM14 on Sesbania sesban. Its physiological and biochemical attributes along with enhanced antioxidant enzyme activities under different levels of Cr toxicity (50, 100 and 200 mg kg⁻¹) were evaluated. After harvesting at 50 days of sowing, plant growth attributes (root and shoot length, fresh and dry weight), physiological parameters (chlorophyll a, b and carotenoid content), antioxidant activities (superoxide dismutase, peroxidase and catalase), malondialdehyde content, electrolyte leakage, proline, relative water content and total Cr uptake in S. sesban were recorded. Experiment was statistically managed as complete randomized design (CRD). Results revealed that Cr stress reduced plant growth, relative water content at all levels of Cr contamination. However, inoculation of B. xiamenensis PM14 positively influence all parameters of S. sesban both under normal and stressed conditions. Inoculation of B. xiamenensis PM14 promoted plant growth (root length 17.08%, shoot length 28.36%) physiological attributes (chlorophyll a 55.26%, chlorophyll b 59.13%), antioxidant activities (superoxide dismutase 30.09%, peroxidase 6.96% and catalase 0.89%), relative water content 25.79%, enhanced total Cr uptake 47.33% and reduced proline 12.33%, malondialdehyde content 27.53% and electrolyte leakage 2.73% in S. sesban at 200 mg kg⁻¹ Cr stress as compared to uninoculated plants grown under the same level of Cr. Our findings revealed first report of B. xiamenensis as phytoremediator and its inoculation on Sesbania plant. It also exposed dual effects of B. xiamenensis to ameliorate Cr stress along with improved plant growth and induced heavy metal stress tolerance in spiked soils.

Introduction

Anthropogenic activities in industrial, urban and agricultural sectors triggered environmental pollution in 20th century (Gavrilescu et al., 2015). In the modern industrial age, avoiding toxic effects of chemicals and metals in environment is unendurable. Excessive deposit of heavy metals in agricultural soil results in soil contamination and elevates heavy metal uptake in crop plants affecting quality and safety of food (Amna et al., 2015a, Amna et al., 2015b; Rafique et al., 2019). In contrary with most organic pollutants, metal contaminants are non-biodegradable and can easily enter into the living system (Ali et al., 2016; Ali et al., 2017). Non-biodegradable nature of heavy metals, long term biological half-life and their ability to accumulate in living system made it more toxic even at low concentration (Amjad et al., 2018). Industrial activities such as tannery, electroplating, paints, cooling towers and timber treatment release Chromium (Cr) containing wastes (Gill et al., 2016). Its 22nd ranked element and second most abundant metal entering in agro-system via anthropogenic activities (Amna et al., 2015a, Amna et al., 2015b; Choppala et al., 2018; Gupta et al., 2018). In Pakistan, the range of Cr contents in ground water was noticed <0.001–9.8 mg/L (mean value 2.12 mg/L) and in surface water 0.16–0.29 mg/L. During soil sample analysis 100–150 mg kg⁻¹ of Cr was present with few exceptions of 42–756 ppm in Pazang site while 92–850 mg kg⁻¹ was reported in a contaminated site of Lahore city (Waseem et al., 2014). There is no substantial evidence of Cr role in plant growth and metabolism that's why its transport system in plants is yet not elucidated. However, it moves to plant via passive transport from roots to above ground plant parts (Gill et al., 2015a; Gill et al., 2017). Chromium toxicity results in the stunted growth of plants due to alterations in morphological, physiological, photosynthetic and defense related mechanisms in various plant species. It also disturbs plant physiology by production of reactive oxygen species (ROS), alterations in mineral uptake and water imbalances in the cells. Under high toxicity levels top wilting of plants, stunted growth, damaged/burned roots and impaired photosynthesis eventually leads to plant death (B2). Soil composition, metabolic activities and diversity of microbiome are also seriously threatened by high concentration of Cr in soil (Oves et al., 2013). Prolonged lag phase during microbial growth under toxic conditions, inhibited process of respiration and photosynthesis lead to decreased microbial growth. Moreover, alteration in cytoskeleton results in less motility of bacteria. Extensive range of chemical and biological technologies has been established for removal of heavy metals. Phytoremediation is one of the tool to remediate polluted soil, sediments, sludges and water bodies (Rezania et al., 2016). In comparison to conventional strategies, green technology is considered a good alternative as it is inexpensive, eco-friendly and non-destructive to soil (Gheju and Balcu, 2017). This technology acts via extraction, translocation and accumulation of contaminates in aerial and sub aerial parts of plant (Farid et al., 2018). Plants being sessile naturally have some capabilities to cope the environmental stresses. However, when these plants subject to high concentrations of toxins they face the problem of phytotoxicity because the damage may increase than their internal defense capabilities (Bukhari et al., 2016). Under such conditions PGPR played an important role in the rhizosphere. Distinct type of bacterial interaction is noticed with Cr i.e its extracellular precipitation detoxifies it into less toxic insoluble metallic complexes.

Therefore, now a days, bioaugmentation of microbes emerged as another efficient strategy. Interconnection between plants and rhizospheric microbes play a vital role in enhancement of phytoremediation efficacy via a mechanism called “bio-assisted phytoremediation” (Shameer and Prasad, 2018). Heavy metal resistant plant growth promoting rhizobacteria (PGPR) have ability to alleviate the heavy metal stress by plant growth improvement, production of antioxidant enzymes to scavenge ROS, increased nutrient uptake, reduced stress ethylene by ACC deaminase that encourage development of longer roots and shoots (Islam et al., 2014a; Islam et al., 2014b).

Sesbania sesban is an important medicinal plant distributed in several tropical countries of the world (Gomase, 2012). Its ability to tolerate metal toxicity is due to N fixing bacteria which cause nodule formation and its survival is reported in contaminated soils (Chan et al., 2003). Current study was basically designed to first time report the potential of B. xiamenensis for its heavy metal tolerance and role in assisted phytoextraction of Cr contaminated soils in association with Sesbania plant. Moreover, to relate the differential effects of bacteria on morpho-physiological and biochemical attributes of inoculated plants under various concentrations of Cr stress.