Removal of Cadmium and Arsenic from Water through Biomineralization

doi:10.21203/rs.3.rs-2597622/v1

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Removal of Cadmium and Arsenic from Water through Biomineralization

https://doi.org/10.21203/rs.3.rs-2597622/v1

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published 07 Aug, 2023

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Due to anthropogenic activities, heavy metals such as cadmium (Cd) and arsenic (As) are one of the most toxic xenobiotics contaminating water, thus, affecting the human health and environment. The objective of the present investigation was to study the effect of ureolytic bacteria Bacillus paramycoides – MSR1 for the bioremediation of Cd, and As from contaminated water. The B. paramycoides showed high resistance to heavy metals of Cadmium and Arsenic with minimum inhibitory concentration of 12.84 µM and 48.54 µM, respectively. The urease activity and calcium carbonate (CaCO₃) precipitation was evaluated by bacteria in the presence of different concentrations of Cd and As. High removal rates for cadmium (93.13%) and arsenic (94.25%) were observed after a period of 168 hours. Microstructural analysis revealed formation of calcium carbonate in the form of calcite by the bacteria and EDS further confirmed the presence of heavy metal ions in the calcium carbonate precipitates. The results demonstate removal of Cadmium and Arsenic by microbially induced calcium carbonate precipitation to be promising technique for decontamination of water.

Arsenic

Cadmium

Calcium carbonate

Biomineralization

MIC

Heavy metal pollution primarily refers to the accumulation of heavy metals, such as lead (Pb), mercury (Hg), chromium (Cr), cadmium (Cd), nickel (Ni), Lanthanum (La), Strontium (Sr) and other biologically toxic heavy elements in the environment in quantities higher than permissible values (Abdalla et al., 2012). Contact with low concentrations of most heavy metals can lead to dangerous health consequences (Azimi et al., 2017). Over the last few decades, heavy metal production and release have increased due to various anthropogenic activities that cause severe damage to the environment (Ojuederie and Babalola, 2017). Many industries, such as electroplating, metal finishing and polishing, mining and metallurgy, electronic-circuit production, iron and steel processing, pesticide and insecticide application, and fine chemical and pharmaceutical production, discharge many toxic heavy metals into water resources that have a deleterious impact on the health of living organisms (Kubier et al., 2019 and Eccles, 1999). Arsenic and cadmium disrupt the metabolic activities of the body in different ways. Cd can accumulate because of its ability to bioaccumulate in essential body organs such as kidney, liver, heart, and brain, upsetting regular biological activities and leading to many serious ailments such as cancer, neurological illnesses, liver damage, central nervous system malfunctioning, and cardiovascular diseases (Tayang and Songachan, 2021). Several cellular toxicities have been reported to be induced by continuous exposure to excess Arsenic (> 0.05 ppm) (Dey et al., 2016). Several conservative methods for detoxifying heavy metals include oxidation/reduction, reverse osmosis, membrane filtration, electrochemical methods, and ion exchange. Physical methods include magnetic separation, electrostatic techniques, material screening, flotation, and density separation (Azimi et al., 2017). Chemical methods involve reactions between heavy metal reagents and ions, reduction-oxidation processes, and electrochemical methods. (Race, 2017). However, it has many disadvantages, such as low efficiency, high demand for chemicals, increased expenses, by-product formation of poisonous sludge, and dangerous disposal of substances. Other limitations include sample pre-treatment, labour-intensive, and feasibility (Achal et al. 2012).

It is more challenging to remove toxic metals from water than other pollutants that can be removed using chemical and biological wastewater treatment (Knox et al., 2000). Therefore, appropriate techniques must be developed to remove heavy metals from polluted wastewater. Microorganisms can break down and detoxify xenobiotics and then degrade them into comparatively less toxic compounds or immobilize them by utilizing their transformation or biomineralization abilities (Ayangbenro and Babalola, 2017; Cheng et al., 2016). In extremely unfriendly environments, such as media polluted with heavy metals, microorganisms are appropriate for detoxifying heavy metals (Maity et al., 2019; Qian and Zhan, 2016). Microorganisms transform heavy metals by changing their physicochemical characteristics (Liu et al., 2021). Biomineralization is a technique through which organisms synthesize inorganic substances through their metabolism (Niedermeier et al., 2018). Various researchers have demonstrated microbially induced calcium carbonate precipitation (MICP) to be an effective method for eliminating heavy metal pollution (e.g., Mitchell and Ferris, 2005; Achal et al., 2011, 2012, 2013; Kang et al., 2014; Kumari et al., 2014; He et al., 2019; Kim et al., 2021) because calcium carbonate is a suitable host matrix for many heavy metals (Callagon et al., 2014). Microbially induced calcium carbonate precipitation (MICCP) is a type of induced biomineralization involving extracellular carbonate production by bacteria, most commonly through the ureolytic pathway. Bacteria play a significant role in MICCP by serving as nucleation sites for carbonate crystals (Lin et al., 2018). Carbonate is released by bacteria that forms bond with cations to create minerals during MICCP (Almajed et al., 2021). Microbes, such as Bacillus licheniformis, can precipitate high concentrations of metal ions, such as calcium and magnesium, in a highly alkaline environment (Zhao et al. 2019). Ureolytic bacteria synthesize the urease enzyme, which breaks urea in aqueous conditions to carbonate ions, increasing the pH and resulting in carbonate formation. Mineralization of heavy metal ions is caused by the reaction of a heavy metal-cell complex, after which the ultimate conversion to metal carbonate precipitate takes place (Hussein et al., 2019). Prokaryotic microorganisms take part in oxidation-reduction reactions and alter the valency of heavy metals, thus altering their activity, which impacts their mobility or toxicity (Gavrilescu, 2004). Cadmium and Arsenic are more toxic in ionic form than the metal carbonate form as the latter is relatively more insoluble and inert due to decreased bioavailability (Chen et al., 2021b). The insoluble precipitate is formed when cadmium and arsenic ions in the contaminated water or soil system react with the chemical species formed during the precipitation. Heavy metal ions get surrounded by carbonate in the mineral structures through coprecipitation are generally more stable and less toxic over time (Achal et al., 2013). Bioremediation of heavy metals by ureolytic microorganisms is an effective method for eliminating metals from the environment through precipitation or coprecipitation in carbonate minerals regardless of the toxicity of metal, redox potential, or valency (Li and Gadd, 2017). Many researchers have reported studies on calcium carbonate derived bioremediation of metals such as Pb, Ni, Cd, Cr, La, and through the use of ureolytic microbes (Zhu et al., 2016a; Dhami et al., 2017; Horiike et al., 2017; Li and Gadd, 2017; Qian et al., 2017; Zhao et al., 2017)

Recently, microbial-induced calcium carbonate precipitation (MICCP) has received significant attention on the bioremediation of heavy metals. Therefore, the present study uses the MICCP technique for bioremediation of heavy metal (cadium and Arsenic) in contaminated water using ureolytic bacteria. The alkaliphilic bacteria Bacillus paramycoides was assessed for urease enzyme activity and calcium carbonate precipitation. The biomineralization potential of B. paramycoides for removing Cd and As was evaluated through atomic absorption spectroscopy (AAS). The biomineralized product was verified through field emission scanning electron microscopy (FESEM).

Microorganism

The halophilic bacteria, Bacillus paramycoides- MSR1 was used in the current study. The bacterial strain was isolated from the water sediments of Sambhar Lake near Jaipur, Rajasthan, India and was selected based on its ureolytic activity. The bacteria was identified as B. paramycoides based on its 16S rRNA sequence analysis. The 16S rRNA sequence obtained from B. paramycoides was submitted to GenBank of NCBI under the accession number OQ186756. The bacterial culture was grown in nutrient broth media (Hi Media, India), shaking at 120 rpm at 37°C.

Growth Assay

Influence of various concentrations of Cd and As were tested on the growth of B. paramycoides. The stock solutions of 2 mM for cadmium and Arsenic were prepared by dissolving cadmium chloride (CdCl₂) and sodium arsenate heptahydrate (Na₂HAsO₄·7H₂O) in Milli-Q water. B. paramycoides was grown in 250 ml Erlenmeyer flasks containing different concentrations of Cd (0, 10, 20, 30, 40, 50 and 60 µM) and As (0, 20, 40, 60, 80 and 100µM). The flasks were incubated at 37° C for 24 hours under shaking conditions (120 rpm). The optical density at 600 nm was recorded after 24 hours using spectrophotometer (UV-1800 Shimadzu spectrophotometer). The minimum inhibitory concentration of the Cd and As were evaluated by progressively increasing the concentration of metal salts in nutrient broth until the complete inhibition of the bacterial growth.The IC50 Value for cadmium and Arsenic was calculated by plotting the OD600 values obtained for log of varying concentrations in GraphPad prism (version 9.3.0) software.

Urease Activity

Bacterial culture was analysed for its urease activity by measuring the breakdown of urea and the production of ammonia. The protocol for urease enzyme activity measurement was optimised by Natarajan, 1995. The bacterial culture grown in presence of different concetrations of Cd and As as mentioned above for seven days were used to assess the urease activity. One ml of bacterial culture from flasks was extracted in separate autoclaved eppendorf tubes and centrifuged at 8000 rpm for 5 minutes. Culture filtrate (250 µl) was taken in clean and dried test tubes and added 1 ml of 0.1 M potassium phosphate buffer (pH 8.0) and 2.5 mL of 0.1 M freshly prepared urea solution and incubated at 37°C for 5 minutes One ml of phenol nitroprusside solution and 1 ml alkaline hypochlorite solution was then added and incubated for 25 minutes at 37°C. The optical density was recorded at 626 nm a using UV-Vis spectrophotometer. The optical density readings were recorded at interval of 24 hours for a period of 7 days.

Calcium Carbonate Precipitation

The bacterial culture was inoculated in nutrient broth and incubated at 37°C overnight under shaking conditions. In 90 ml nutrient broth urea (2%) and calcium chloride (25 mM) were added along with varying Cd (0, 10, 20, 30, 40, 50 and 60 µM) and As (0, 20, 40, 60, 80 and 100 µM). One ml overnight culture was added to each flask and incubated for 7 days at 37° C under shaking conditions. The quantification of calcium carbonate precipitated was determined using EDTA titration method and the weight of calcium carbonate crystals was recorded as described by Dhami et al, 2013b.

Removal of Cadmium and Arsenic

After the completion of 7 days of calcium carbonate precipitation experiment the flasks were removed from incubation. The calcium carbonate precipitates were collected in a cellulose membrane filter (Pore size- 0.45 micrometer) using membrane filter apparatus by connecting it to the vacuum pump and the filtrate was quantified for the heavy metals using Atomic Absorption Spectroscopy. The precipitated powder was collected in the filter paper which was dried using different concentration of ethanol and then left at room temperature for 6 hours. After complete drying, the calcium carbonate powder was weighed.

Microstructural analysis

The bio-precipitates were analysed by field emission scanning electron microscopy (FESEM) to study the topographical information and energy dispersive spectroscopy (EDS) to study the elemental characterization. The samples were coated with a thin layer of gold to increase the conductivity of the sample. Generally, the thickness of coating lies between 20 nm to 30 nm. The imaging was carried out by Carl Zeiss Sigma 500 Field emission microscope and eds was carried by Bruker, QUANTAX 200.

Statistical Analysis

All the experiments were performed in triplicates. The data were analyzed by analysis of variance and significant differences among the means were compared by Tukey's test at p < 0.05. All the analyses were performed using GraphPad Prism 5 software.

Growth Assay

The growth of B. paramycoides significantly reduced with increase in concentration of both Cd and As (Fig. 1). In Fig. 1a and b, the normalized absorbance has been plotted against the increasing cadmium concentrations as a function of logarithm. The IC₅₀ value for Cd was found to be 12.84 µM. Inhibitory concentration 50 (IC₅₀) was determined as the concentration of heavy metal required to inhibit the growth of 50% bacterial population. As the concentration of cadmium was increased in media, a decrease in the growth of Bacillus paramycoides was observed which is in concurrence with the observations made by Kang et al., (2014)

The IC₅₀ value for Arsenic was 48.54 µM. On comparing, it was observed that as the concentration of arsenic was increased, the bacterial growth decreased correspondingly and similar observations were reported by Achal et al., (2012). The possible reason for the decline in bacterial growth in the presence of Arsenic could be the binding of arsentite ion with the membrane which could lead to the expansion of the membrane which consequently increases the number of attachment sites thus hindering the transport of materials required for cellular growth (Liu et al., 2004). It was noted by Fang et al. (2021) that the Cd^+ 2 possesses much more toxic potential than other ions of heavy metals and the impact of anions on bacteria is not significant. The lower IC₅₀ value suggests higher potency of the heavy metal to inhibit the bacterial growth and population (Situmorang et. al., 2020). Similarly, a higher IC₅₀ value signifies that the bacteria can tolerate a higher concentration of the heavy metal before showing a significant decline in the growth due to interference of heavy metal with the metabolism.

Urease Activity

The urease activity significantly decreased with increasing concentration of Cd and As at different time intervals (Fig. 2). In Cd, the highest urease enzyme activity was reported at 96 hours, while in As, the most increased urease enzyme activity was observed at 120 hours. The maximum urease enzyme (722 U/ml) was observed in control without any metal. The urease enzyme activity at cadmium (Cd) concentrations of 10 µM, 20 µM, 30 µM, and 40 µM was noted to be 616 U/ml, 602 U/ml, 562 U/ml and 525 U/ml (Fig. 2). A sharp decrease in the urease enzyme activity, i.e., 278 U/ml was noted upon reaching the cadmium concentration of 50 µM followed by 60 µM, i.e., 172 U/ml. The variation of urease enzyme activity with increasing concentrations of arsenic through a period of 7 days has been reported (Fig. 2b). After 24 hours of inoculation, the urease activity is almost negligible and increases fivefold within the next 24 hours. The urease enzyme activity at arsenic concentrations 0 µM, 20 µM, 40 µM, 60 µM, 80 µM & 100 µM was 855 U/ml, 847 U/ml, 836 U/ml, 824 U/ml, 797 U/ml, 734 U/ml, respectively. The statistical analysis inferred that time intervals and different concentrations of Cd and As significantly affected the urease activity by the bacterial strain (Table 1). Urease producing bacteria breakdown urea which leads to the formation of carbonate ions which react with heavy metal ions to form precipitates of heavy metal-carbonate (Jalilvand et al., 2020). Many studies show the directly proportional relation between the increase in heavy metal concentration and urease enzyme activity and bacterial growth (Cheng et al., 2017; Fan et al., 2020). Similar results were corroborated by Wei et al. (2022) and Qiao et al. (2021). The effectiveneness of urease facilitated Calcium-Cadmium carbonate precipitation in bioremediation of cadmium by Salmonella mucilaginosa and Enterobacter cloacae was observed by Bhattacharya et al. (2018).

Table − 1. The factorial Analysis of Variation (ANOVA) results indicating the effects of urease activity at different time periods (24–168 hours) in nutrient broth media with different concentrations of cadmium and arsenic. The P values < 0.001 indicates the values are highly significant. Two way ANOVA revealed significant variation between two factors i.e. metal concentration and time. The interactions are highly significant (Tabel 1).

Table 1

Two way ANOVA between metal concetrations and time intervals and their interaction
Variables		Metal concentration	Time (hours)	Conc. × Time
Cadmium	df	7, 112	6, 112	42, 112
Cadmium		P < 0.0001	P < 0.0001	P < 0.0001
Arsenic	df	5, 84	6, 84	30, 84
Arsenic		P < 0.0001	P < 0.0001	P < 0.0001

Calcium carbonate precipitation

Calcium carbonate precipitation was observed for a period of seven days from the time of inoculation in nutrient broth in presence of urea and calcium chloride. The quantification of calcium carbonate precipitation was done after an interval of 24 hours using the EDTA titration method. As seen in Fig. 3(a), after 24 hours, significantly less calcium carbonate was precipitated, increasing successively with every 24-hour interval. The increase in calcium carbonate precipitation was observed until the 168th hour, which was recorded to be the highest for every cadmium concentration. Upon completion of 7 days of inoculation, the maximum amount of calcium carbonate precipitated was measured for 0 µM to be 204 mg/100 ml, followed by 189 mg/100 ml (10 µM), 174 mg/100 ml (20 µM), 159 mg/ 100 ml (30 µM), 134 mg/100 ml, (40 µM). Almost a threefold drop was observed in the precipitation of calcium carbonate at cadmium concentration above 50 µM (50 mg/100 ml) followed by 45 mg/ 100 ml in 60 µM concentration of cadmium. As the concentration of heavy metals in the solution was increased, the precipitation of calcium carbonate decreased because heavy metal ions act as an inhibitor to the normal cellular functions of bacteria. Similar observations were reported by Li et al. (2014). At 96 hours and 120 hours, a significant increase in the precipitation of calcium carbonate can be seen, which can also be attributed to the fact that the urease enzyme activity was found to be at its peak at the same number of hours post-inoculation.

In case of As, it was observed that calcium carbonate precipitation showed an increasing trend during the 168- hours of incubation. The maximum calcium carbonate precipitation was observed in As concentration of 0 µM (208 mg/100 ml) followed by 20 µM (198 mg/ 100 ml), 40 µM (183 mg/100 ml), 60 µM (178 mg/100 ml), 80 µM (163 mg/100 ml) and lastly, 100 µM (141 mg/100 ml). The statistical analysis inferred that time intervals and different concentrations of Cd and As significantly affected the calcium carbonate precipitation by the bacterial strain (Table 2). There was an increase in calcium carbonate precipitation with a rise in time intervals of incubation. This might be because bacteria inoculated in the medium could utilize the urease enzyme to precipitate the calcium carbonate even in the presence of different concentrations of the As. During the urease enzyme activity, the medium showed higher urease activity until 120 hours of incubation.

Table 2

The factorial ANOVA results indicating the effects of calcium carbonate precipitation at different time periods (24–168 hours) in nutrient broth media with different concentrations of cadmium and arsenic. The P values < 0.001 indicates the values are highly significant. Two way ANOVA revealed significant variation between metal concentration vs time. Interactions are highly significant
Variables		Metal concentration	Time (hours)	Conc. × Time
Cadmium	df	7, 112	6, 112	42, 112
Cadmium		P < 0.0001	P < 0.0001	P < 0.0001
Arsenic	df	5, 84	6, 84	30, 84
Arsenic		P < 0.0001	P < 0.0001	P < 0.0001

Change in pH

Due to the ureolytic action of enzyme urease, urea is hydrolyzed and as a consequence, ammonium and hydroxyl ions are generated, leading to a rise in pH of the medium. This phenomenon leads to binding Ca²⁺ ions to the heavy metal in the solution. The trend observed in the change of pH over time showed a slight reduction in the pH upon the addition of urea and calcium chloride for the first 5 hours, considering the addition of urea and calcium carbonate to be done at 0 hours. This pH reduction can be explained by considering the dissociation of the ions in water upon addition. The pH showed an increasing trend till 96 hours, after which a plateau is observed. Achal et al. (2012) reported the increase in the pH due to the presence of ammonium ions and the evolution of carbon dioxide during the ureolysis. Due to alkaline conditions, the rate of metal oxidation is amplified while the solubilization of metal is prevented (Ayangbenro et al. 2018). Figure 4 shows variation in pH for different Cd concentrations for the introductory period (0–10 hours) and the secondary period (24–168 hours). The pH variation in control sample was more abrupt than the cadmium concentrations from 10 µM to 60 µM. The pH changed from 7 to 8.5 from day 0 to day 7. An extreme change in pH was observed in the first 24 hours, which then increased until the experiment's completion from pH 7 to approximately 9.5. Similar results were observed in the medium inoculated with different As concentrations (0–100 µM). Figure 5 shows the change in pH over a diverse range of As concentrations for 0 to 10 hours and, subsequently, 24 to 168 hours. The pH falls upon adding the calcium chloride, which might be due to the absorption of hydroxide ions, leaving free protons in the medium (Sidhu et al., 2022). However, in the second phase of the experiment, the pH of the medium starts increasing because of bacterial metabolic activity. Statistically the results were observed to be significant at a 5% level of significance.

Removal of cadmium and Arsenic

Microstructural analysis

Scanning electron microscopy was performed to study the morphology of the precipitated calcium carbonate crystal. The crystal structure was studied using FESEM and EDS to determine the percentage of calcium carbonate and heavy metal content in the precipitate to ensure that the heavy metal ions have been trapped within the calcium carbonate crystal lattice. Calcium carbonates behave as an effective adsorbent and have also demonstrated its ability to engulf divalent heavy metals cations (Achal et al., 2011; Callagon et al., 2014; Kim et al., 2021). Calcium carbonates have been used as heavy metal scavengers since long (e.g., Dang et al., 2017; Liu and Lian, 2019a, b; He et al., 2019). The FESEM images obtained for the heavy metal-calcium carbonate bio- precipitates are shown in Fig. 7. The structure of calcium carbonate crystals with the morphology resembling the calcite polymorph of calcium carbonate was observed and labelled as CC in Fig. 7. The EDS graphs along with the elemental composition of heavy metal calcium carbonate bio-precipitates is shown in Fig. 8. EDS analysis specified that the precipitated compound was Ca²⁺, oxygen, and carbon of CaCO₃. The bacteria represent the nucleating sites for calcite-precipitation which is the main crystalline product involved in the bioremediation process. Calcite in the form of CaCO₃ as verified by EDS analysis.

In the present investigation growth of ureolytic bacteria B. paramycoides strain was determined for the minimum inhibitory concentration 50 (IC50) in water contaminated with different metal (cadmium and arsenic) conconcentrations. The bacteria was observed to exhibit urease activity and calcium carbonate precipitation in the presence of different metal stress. The IC50 value for cadmium was 12.84 µM while it was 48.54 µM for arsenic. The highest urease activity was reported at 96 hours in cadmium while in arsenic the highest urease activity was ob rved till the 120 hours incubation at 37°C. The Cd and As removal from the water was evaluated using the atomic absorption spectroscopy. The heavy metal removal percentage of cadmium was 93.13% while it was 94.25% for arsenic. No heavy metal removal was observed in water without bacterial inoculum. The FESEM and EDX results also showed the formation of heavy metal-calcium carbonate complex which means the immobilization of the heavy metals was achieved successfully through microbially induced calcium carbonate precipitation.

Acknowledgments

The authors are thankful to the Department of Biotechnology, Ministry of Science and Technology, Govt. of India, for providing the research grant under BT/PR27190/BCE/8/1428/2017.

Authors contribution

All authors have contributed to the study. Manjot kaur carried out the experiment and wrote the main manuscript text Navneet Sidhu conceptualized the methodlogy and carried out the statistical analysis M. Sudhakara Reddy conceptualized the methodlogy, supervised, reviewed and edited the manuscript.

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Conflict of interest The authors have no conflicts of interest to declare. All co-authors have seen and agree with the contents of the manuscript and there is no financial interest to report. We certify that the submission is original work and is not under review at any other publication.

Funding

This study was financially supported by the Department of Biotechnology, Governmento f India, Ministry of Science & Technology under the research grant No. BT/PR27190/BCE/8/1428/2017.

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No competing interests reported.

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published 07 Aug, 2023

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Editorial decision: Major revision
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Removal of Cadmium and Arsenic from Water through Biomineralization

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Microorganism

Growth Assay

Urease Activity

Calcium Carbonate Precipitation

Removal of Cadmium and Arsenic

Microstructural analysis

Statistical Analysis

Results And Discussion

Growth Assay

Urease Activity

Calcium carbonate precipitation

Change in pH

Removal of cadmium and Arsenic

Microstructural analysis

Conclusions

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1