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. 2024 Oct 29;14(11):283. doi: 10.1007/s13205-024-04122-3

Bioremediation of metal cyanide complexes from electroplating wastewater for long-term application using Agrobacterium tumefaciens SUTS 1 and Pseudomonas monteilii SUTS 2

Nootjalee Supromin 1,2, Siraporn Potivichayanon 1,✉
PMCID: PMC11522241  PMID: 39484078

Abstract

The purpose of this study was to investigate the optimum conditions, including aerobic and anoxic conditions, for operating a long-term bioreactor system to decrease the toxicity of industrial electroplating wastewater effluents containing metal cyanide using Agrobacterium tumefaciens SUTS 1 and Pseudomonas monteilii SUTS 2. The initial results revealed that bacteria performed better under aerobic conditions than under anoxic conditions. An aerobic bioreactor system was subsequently set up in a long-term study lasting 30 days under optimum operating conditions. Both mixed-culture bacteria and indigenous bacteria promoted the high-efficiency treatment of cyanide and metals in the first 7 days of the study. When the system had high removal rates, cyanide removal was greater than that of zinc, copper, nickel, and chromium (CN− > Zn > Cu > Ni > Cr), with removal efficiencies of 96.67%, 93.93%, 74.17%, 63.43%, and 44.65%, respectively, with residual concentrations of 0.15 ± 0.01, 0.24 ± 0.005, 0.03 ± 0.002, 18.41 ± 0.06 and 14.26 ± 0.15 mg/L, respectively. The cell concentration in the bioreactor increased to approximately 107 CFU/mL over 30 days from initial cell concentrations of 6.15 × 105 CFU/mL and 1.05 × 103 CFU/mL for the mixed culture and indigenous inoculation, respectively. These results implied that the bacteria were resistant to heavy metal toxicity. The addition of an appropriate carbon source with sufficient aeration to a bioreactor resulted in increased cyanide degradation.

Keywords: Aerobic and anoxic conditions, Agrobacterium tumefaciens SUTS 1, Bioremediation, Electroplating wastewater, Long-term application, Metal cyanide complexes, Pseudomonas monteilii SUTS 2

Introduction

In recent decades, rapid industrial expansion has occurred, which has considerably contributed to the increase in environmental pollution. Mining, textiles, electroplating, metal finishing, metal hardening, jewelry gold extraction, and printed circuit board manufacturing are only some examples of industrial processes that generate large amounts of metal cyanide effluent (Kuyucak and Akcil 2013; Luque-Almagro et al. 2016; Yu et al. 2017; Gupta et al. 2018; Chen et al. 2021; Alvillo-Rivera et al. 2021, 2023; Abd-Elhalim et al. 2023; Olaya-Abril et al. 2024). In effluents, cyanide can be found in both the form of cyanide ions (CN−) and metallic cyanide complexes (Alvarado-López et al. 2023; Wei et al. 2023; Olaya-Abril et al. 2024), because metals strongly bind with cyanide to form complexes, such as Zn(CN)42−, Cd(CN)3−, Ni(CN)42−, CuCN, Cr(CN)63−, Co(CN)63−, and Fe(CN)64−, and these forms are typically very stable and toxic to most living organisms and have long-term environmental impacts (Luque-Almagro et al. 2016; Razanamahandry et al. 2016; Alvillo-Rivera et al. 2021). Therefore, the treatment of wastewater contaminated by metal cyanide complexes has been studied via biological processes, and it has been found that microorganisms can tolerate high concentrations of metal cyanide complexes and that microbes can degrade cyanide to reduce its toxicity (Bahrami et al. 2020; Xiong et al. 2020; Rishi et al. 2023). The most effective mechanism for microbial heavy metal resistance may involve the binding or sequestration of metals by metallothioneins or related proteins, which immobilize the metal and block its entry into cells, which is the main mechanism by which microbial heavy metal resistance occurs (Maier et al. 2009; Razanamahandry et al. 2019; Benhalima et al. 2020; Khan et al. 2022). However, several other laboratory-scale studies on the microbial bioremediation of cyanide and metal cyanide complexes have been conducted, but few studies have been conducted by electroplating wastewater (Maniyam et al. 2013; Benhalima et al. 2020; Rishi et al. 2023). In addition, there have been only a few investigations on the biodegradation of metal cyanide under aerobic and/or anoxic conditions (Chakraborty and Veeramani 2006; Baxter and Cummings 2006; Kim et al. 2011). Consequently, to ensure the effective treatment of metal cyanide, it is necessary to assess the potential for the elimination of pollutants from microbes grown under different redox conditions. Microorganisms can use cyanide as their only source of nitrogen and carbon for growth while also transforming it into less toxic byproducts, such as ammonia (Alvarado-López et al. 2023; Motsoeneng et al. 2023; Uribe-Ramirez et al. 2024), nitrite, and nitrate (Razanamahandry et al. 2017; Rishi et al. 2023), under aerobic, anoxic and/or anaerobic conditions (Sharma and Philip 2015; Gupta et al. 2018; Anning et al. 2021). One of the most well-known biological nitrogen removal processes is the anoxic/oxic-activated sludge process, in which Shieh and Richards (1988) demonstrated efficient cyanide removal. According to a prior study, processes involving the conversion of hydrolytic cyanide under anaerobic conditions presented less cyanide tolerance than those under aerobic conditions due to the pathways of cyanide oxidation induced by monooxygenase and dioxygenase enzymes in aerobic microorganisms and the presence of dissolved oxygen (DO), which favors oxidation reactions for the rapid degradation of cyanide (Naveen et al. 2011; Gupta et al. 2018). On the other hand, the biodegradation of cyanide compounds by Agrobacterium tumefaciens SUTS 1 and Pseudomonas monteilii SUTS 2 has been reported in a short-term study, and mixed-culture bacteria have been shown to be efficient for metal cyanide treatment (Supromin et al. 2015; Potivichayanon et al. 2017). However, cyanide levels have not met the industrial effluent standards for industrial plants in Thailand (Notification of Ministry of Industry 2017).

Therefore, this work aimed to study the degradation of metal cyanide complexes by Agrobacterium tumefaciens SUTS 1 and Pseudomonas monteilii SUTS 2 under different oxygen-demand conditions, including aerobic and anoxic conditions, via electroplating wastewater (EPWW) treatment and to select optimum conditions for long-term treatment.

Materials and methods

Sources of microorganisms and electroplating wastewater

In this study, Agrobacterium tumefaciens SUTS 1 (GenBank accession number: DQ790018.1) and Pseudomonas monteilii SUTS 2 (GenBank accession number: EF600886.1) were isolated in the previous work from a cassava starch wastewater treatment plant located in Nakhon Ratchasima, Thailand (Potivichayanon and Kitleartpornpairoat 2010; Potivichayanon et al. 2017). Both isolated microorganisms were prepared for metal cyanide degradation. The potential for using the exponential growth stage based on bacterial growth curve analysis for metal cyanide treatment in a bioreactor was investigated (Supromin et al. 2015). In these experiments, the bioremediation of metal cyanide by mixed-culture bacteria (SUTS 1 and SUTS 2) was studied using real electroplating wastewater. Industrial electroplating wastewater was collected from a local manufacturing facility in Nakhon Ratchasima, Thailand. The chemical characteristics of the electroplating wastewater are shown in Table 1.

Table 1.

Chemical characteristics of the electroplating wastewater used for the long-term system tests

Parameters Values (mean ± SD) Parameters Values (mean ± SD)
1. Cyanide, (mg/L) 4.56 ± 0.08 10. Sulfate, (mg/L) 226.49 ± 0.15
2. Thiocyanate, (mg/L) 0.88 ± 0.05 11. Bicarbonate, (mg-CaCO3/L) 80.50 ± 3.54
3. Zinc, (mg/L) 3.90 ± 0.01 12. BOD, (mg/L) 71.25 ± 1.06
4. Copper, (mg/L) 0.12 ± 0.003 13. COD, (mg/L) 451.28 ± 0.00
5. Chromium, (mg/L) 25.76 ± 0.05 14. DO, (mg/L) 1.80 ± 0.14
6. Nickel, (mg/L) 50.35 ± 0.05 15. pH 6.26 ± 0.00
7. Ammonia, (mg/L) 4.83 ± 0.40 16. ORP, (mV) 28.5 ± 1.41
8. Nitrite, (mg/L) 0.12 ± 0.001 17. Indigenous microbes, (CFU/mL) 1.05 × 103
9. Nitrate, (mg/L) 1.60 ± 0.01
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Optimal conditions under aerobic and anoxic conditions

Batch experiments involving the use of aerobic and anoxic conditions in 1000-mL Erlenmeyer flasks were performed for electroplating wastewater treatment. Under aerobic conditions, diffusers are used to provide air for the oxidation of organic pollutants. The dissolved oxygen (DO) concentration was maintained at 2.0–4.0 mg/L for 24 h. For anoxic conditions, nitrogen gas was added for 10 min to quickly remove oxygen, and the DO concentration was maintained below 0.5 mg/L. The bacteria were maintained in broth culture on a 50-rpm rotary shaker at room temperature. Both treatments contained an appropriate ratio of mixed culture per electroplating wastewater of 30:70% v/v and had an optimum concentration of glucose of 500 mg/L (Supromin et al. 2015). The samples were collected at 0, 1, 3, 5, and 7 days for analysis.

Experimental design and operating conditions for the long-term system

The experimental setup consisted of an aerobic reactor with a diameter of 15.0 cm and height of 22.0 cm, a recirculation tank with a diameter of 15.0 cm and height of 25.0 cm (Fig. 1) and an identical control reactor. The experimental reactor was developed with a defined mixture (30:70% v/v) of mixed-culture bacteria (SUTS 1 and SUTS 2) per electroplating wastewater, and the control reactor contained only indigenous microbes in electroplating wastewater. A long-term study was performed, and the system was operated continuously for 30 days under optimal conditions (Table 2). The bioreactor system was maintained at room temperature, and recirculated wastewater was transferred from the recirculation tank to the aeration tank via a peristaltic pump.

Fig. 1.

Fig. 1

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Schematic of the aerobic bioreactor system consisting of 1. wastewater flask; 2. peristaltic pump; 3. aerobic tank; 4. recirculation tank; 5. effluent tank; and 6. recirculation tube

Table 2.

Operating conditions of an aerobic system for metal cyanide bioremediation

Conditions Values
Hydraulic retention time (HRT) 24 h
Wastewater flow rate (Q) 3.0 L/day
Recirculation rate 1.5 L/day
Aeration duration 24 h
Ratio of mixed-culture bacteria (SUTS 1 and SUTS 2): EPWW 30:70% v/v
Glucose (carbon source) 500 mg/L
Potential of hydrogen ion (pH) Approximately 6.0–7.0
Dissolved oxygen (DO) More than 1.0 mg/L
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Metal element accumulation in bacterial cells

The samples were analyzed by scanning electron microscopy (SEM) and energy dispersive X-ray analysis (EDX) to identify and quantify the metal species present on the cell surfaces of bacteria (Ezz et al. 2023). In this work, SEM and EDX were performed via a JSM-700 (Carl Zeiss, Germany) microscope to identify the elements present in samples at approximate depths of 50–300 nm, with detection limits of 0.1–100 wt% (Lucideon 2017). The bioreactors were sampled on day 15 and day 30. The bacterial sample was prepared by fixing the samples to preserve their structure. The samples were relatively thin (< 2 mm) and small (only a few mm). The fixed and dried bacteria were sputter coated with a thin layer of gold (Kaláb et al. 2018).

Analytical methods

All the experiments were analyzed in triplicate. The concentrations of cyanide (CN−), thiocyanate (SCN−), copper (Cu), zinc (Zn), nickel (Ni), chromium (Cr), and byproducts after degradation in the form of bicarbonate (HCO3−), sulfate (SO42−), ammonia nitrogen (NH3–N), and nitrite (NO2−–N) were determined following standard protocols for the analysis of water and wastewater (APHA, AWWA, WPCF, 2017) and nitrate (NO3−–N) (APHA, AWWA, WPCF, 1998). The reduction of sugar was analyzed via the dinitrosalicylic acid (DNS) method (Chaplin and Kennedy 1994). The following sensors were used: dissolved oxygen (DO) (HACH Sension 6 Portable, USA), oxidation‒reduction potential (ORP) (YSI Professional Plus, USA), and pH (Jenway 3510, UK). Mixed-culture bacterial growth was analyzed via the colony counting technique (APHA, AWWA, WPCF, 2017). The chemicals were of analytical grade and were obtained from Merck (Darmstadt, Germany), Sigma‒Aldrich (St. Louis, USA) or Ajax (Auckland, New Zealand).

The removal efficiency, RE (%), was calculated via the following equation:

RE%=Ci-CfCi×100, 1

where Ci is the influent concentration (mg/L), and Cf is the effluent concentration of the treated compounds (mg/L).

Statistical analysis

The experimental data were estimated and are presented as the mean with standard deviation (SD). The t test was used for statistical analysis in Microsoft Excel 2019, where the significance level at the 95% confidence level was p < 0.05.

Results and discussion

Optimal parameters for metal cyanide degradation under aerobic and anoxic conditions

Mixed-culture growth analyses of SUTS 1 and SUTS 2 in wastewater during the treatment of cyanide complexes of Zn(CN)2, CuCN, and Cd(CN)2 have been reported (Supromin et al. 2015; Potivichayanon et al. 2017). As a result, cells were taken from the mixed culture during the maximum growth phase for the degradation of cyanide and metal cyanide in the present study, because the metal cyanide degradation rate is related to cell growth (Maniyam et al. 2013; Supromin et al. 2015). The present study examined the optimum aerobic and anoxic conditions for the degradation of metal cyanide by a mixed culture. The results showed that bacteria can grow under aerobic conditions, but the initial cell count in the first 24 h was slightly reduced, because bacteria require time to acclimate to wastewater pollution. After that, the microbial growth increased to approximately 108 CFU/mL. Mixed-culture bacteria are a facultative bacterial group that can grow with or without molecular oxygen (Holt et al. 1994). Over 7 days, the DO and ORP were 3.06–4.31 mg/L and 93.2–128.8 mV, respectively. The cyanide, copper, and zinc removal efficiencies were approximately 95.05%, 87.87%, and 40.95%, respectively. However, the residual concentrations of cyanide, copper, and zinc were 0.14, 0.03, and 0.63 mg/L, respectively, on day 7. In the control set, the cell count of indigenous microbes over 7 days ranged from 104–105 CFU/mL, with efficiencies of approximately 88.66%, 64.56%, and 28.08% for cyanide, copper, and zinc, respectively. The residual concentrations of cyanide, copper, and zinc were approximately 0.32, 0.10, and 0.77 mg/L, respectively (Table 3). This interesting result demonstrated that the experimental conditions with mixed-culture bacteria resulted in greater cyanide degradation efficiency than the control conditions did, resulting in the complete degradation of thiocyanate in the first 24 h, whereas the control conditions resulted in an increase in the thiocyanate concentration relative to the initial concentration. This may be because the bacteria in the mixed culture could more efficiently use thiocyanate as a source of nitrogen or sulfur than indigenous microbes. In addition, previous studies revealed that Pseudomonas sp. has an enzyme system for the degradation of sulfur compounds (Guo et al. 2013) and that thiocyanate is converted to ammonia and carbon dioxide (Dzombak et al. 2006), indicating that these compounds can be easily utilized by microbes. Dzombak et al. (2006) reported that Pseudomonas sp. is the dominant species for cyanide treatment, specifically cyanogenic bacteria. These cyanogenic bacteria can eliminate cyanide toxicity by synthesizing organic cyanide compounds within cells through cyanide-metabolizing pathways (Gupta et al. 2018; Luque-Almagro et al. 2018; Razanamahandry et al. 2019). Several species of the genus Pseudomonas have been investigated for cyanide and/or metal cyanide removal (Luque-Almagro et al. 2016; Alvillo-Rivera et al. 2021; Rishi et al. 2023). However, the accumulation of thiocyanate and cyanide in the system may affect microbial cell growth, and the time required for degradation could increase (Kim et al. 2011). This study demonstrated that the presence of cyanide in the system did not affect thiocyanate degradation and that thiocyanate was completely degraded.

Table 3.

Comparison of metal cyanide removal on day 7 under aerobic and anoxic conditions in this study

Conditions Residual cyanide (mg/L) % RE of cyanidea Copper (mg/L) % RE of coppera Zinc (mg/L) % RE of zinca
Aerobic (control) 0.32 ± 0.01 88.66 0.10 ± 0.001 64.56 0.77 ± 0.001 28.08
Aerobic 0.14 ± 0.00 95.05 0.03 ± 0.001 87.87 0.63 ± 0.001 40.95
Anoxic (control) 0.39 ± 0.00 86.28 0.10 ± 0.003 63.62 0.76 ± 0.002 28.38
Anoxic 0.29 ± 0.00 89.75 0.05 ± 0.002 80.36 0.58 ± 0.001 45.55
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The values are shown as the mean ± SD

RE removal efficiency (%)

aWhere the significance level is p < 0.05

In contrast, for metal cyanide degradation under anoxic conditions, the DO content and ORP throughout the 7 days of the study were approximately 0.20–0.29 mg/L and -28.41–33.9 mV, respectively. Under these conditions, the cell density was approximately 106–107 CFU/mL, and the efficient removal of metal cyanide occurred in the first 24 h, which was similar to the performance under aerobic conditions. The removal efficiency increased over time. On day 7 of the studies, residual cyanide was found at approximately 0.29 mg/L, with a degradation efficiency of 89.75%. However, when copper and zinc were decreased to 0.05 and 0.58 mg/L from the initial concentration, the removal efficiencies were approximately 80.36% and 45.55%, respectively, and thiocyanate was completely degraded in the first 24 h. For the control set under anoxic conditions, the cell density in the system was approximately 104–105 CFU/mL, which was less than that in the experimental set under the same conditions. As a result, on day 7, the cyanide, copper, and zinc removal efficiencies were approximately 86.28%, 63.62%, and 28.38%, respectively, and thiocyanate was somewhat degraded (data not shown). The residual cyanide in the anoxic system effluent did not meet the standard criteria (Notification of Ministry of Industry 2017), but this was able to provide higher efficiency for metal cyanide degradation than the control.

In this study, under aerobic and anoxic conditions, the aerobic conditions were more effective at removing metal cyanide than were the anoxic conditions over 7 days (statistically significant at p < 0.05) (Fig. 2). This may have occurred as a result of aerobic bacteria undergoing oxidative reactions produced by monooxygenase and dioxygenase enzymes for rapid cyanide breakdown in the presence of sufficient amounts of dissolved oxygen in the system (Naveen et al. 2011).

Fig. 2.

Fig. 2

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Comparison of the relationships between the cell count and other metals cyanide removal under aerobic and anoxic conditions

Kandasamy et al. (2015) and Huddy et al. (2015) illustrated the successful application of an aerobic system to remove cyanide from wastewater and that the degradation of cyanide increased when the aeration rate increased (Chapatwala et al. 1998). The effectiveness of heavy metal removal and the capacity to grow under aerobic conditions over a broad range of metal concentrations in synthetic wastewater have been interestingly observed in bacteria (Raja et al. 2006). In terms of reactor performance, an aerobic bioreactor removes more cyanide than either anaerobic or anoxic reactors (Sharma and Philip 2015). Similar to the results of other studies, cyanide degradation in anoxic reactors was significantly lower than that in anaerobic and aerobic reactors (Chakraborty and Veeramani 2006). This can be explained by bacteria carrying out the conversion of hydrolytic cyanide in an anaerobic system being less tolerant to cyanide than bacteria in aerobic systems are (Naveen et al. 2011). Therefore, the appropriate conditions for metal cyanide degradation are aerobic.

Metal cyanide treatment in an aerobic bioreactor system for long-term applications

The optimal aerobic conditions were applied to a long-term study of the biological treatment of electroplating wastewater for 30 days. The removal of cyanide has been reported in several groups of aerobic activated sludge systems (Richards et al. 2002). According to Pandey et al. (1987), biological processes in activated sludge plants may degrade up to 200 mg/L cyanide. The chemical characteristics of the electroplating wastewater used in this study are shown in Table 1. The average DO, pH, and ORP values throughout the experiment were approximately 3.48 mg/L, 5.77, and 126.6 mV, respectively. The results demonstrated that within the first 24 h, the number of microorganisms in the system increased, and the maximum cell count was approximately 108 CFU/mL from day 8 to day 11. The number of cells increased by approximately 107 cells over 30 days in the bioreactor. Considering the relationship between the number of cells and the system capabilities for cyanide treatment, rapid degradation of cyanide occurred within the first 24 h, which is consistent with the increased number of microorganisms present during the same time. In addition, glucose was decreased to 80 mg/L and completely used by microorganisms within 5 days, glucose is one of the carbon sources supporting microbial growth during degradation (Mirizadeh et al. 2014). As a result, the increase in microorganisms in the system resulted in the maximum removal of cyanide on days 3–5 of the experiment, and the cyanide concentration decreased to 0.15–0.18 mg/L from the initial cyanide concentration of 4.56 mg/L. The maximum cyanide removal efficiency was observed on day 3; when cyanide was rapidly degraded, the degradation efficiency reached 96.67%, and the complete degradation of more than 99.99% thiocyanate was reached within 5 days. It was observed to degrade to approximately 0.20–0.50 mg/L on days 11–30 of the experiment. It has been reported that cyanide removal in aerobic systems could occur via volatilization to the atmosphere in the form of hydrogen cyanide (HCN) at pH < 2 from wastewater (Dzombak et al. 2006; Razanamahandry et al. 2016). However, Gessner et al. (2005) reported that the degradation of cyanide occurs predominantly by biological mechanisms, which depend on appropriate conditions in the wastewater treatment system, such as dissolved oxygen, pH, temperature, nutrients, and wastewater treatment processes (Ibrahim et al. 2015; Alvillo-Rivera et al. 2021; Yao-ting et al. 2023; Rangel‑Gonzalez et al. 2024). This result indicated that in the aerobic system, cyanide treatment met the standard criterion and was not above 0.2 mg/L (Notification of Ministry of Industry 2017), and the system degraded more than 2 times more cyanide than did the control reactor (statistically significant at p < 0.05) (Fig. 3).

Fig. 3.

Fig. 3

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Comparison of cyanide degradation in the experimental (aerobic) and control systems over 30 days

Furthermore, the results revealed that the levels of the byproducts ammonia, nitrite, nitrate, sulfate, and bicarbonate tended to decrease. Although ammonia accumulates during cyanide degradation, it does not interfere with the growth of microbes or the elimination efficiency of the treatment system. Similar observations were made by earlier researchers (Dzombak et al. 2006; Kandasamy et al. 2015). The values of ammonia were approximately 1.96–4.55 mg/L, and the concentrations of nitrite, nitrate, sulfate, and bicarbonate over 30 days were approximately 0.061–0.204 mg/L, 0.25–1.45 mg/L, 136–388 mg/L, and 37.50–107.50 mg-CaCO3/L, respectively (Figs. 4, 5). It is possible that microbes use these byproducts for cell growth, causing microorganism cell counts to increase to approximately 108 CFU/mL on days 9–11. A mixed culture (A. tumefaciens SUTS 1 and P. monteilii SUTS 2) has been shown to utilize ammonia as a nitrogen source more effectively than indigenous microbes from wastewater treatment for electroplating, because Pseudomonas sp. can degrade cyanide and transform it into ammonia under aerobic and/or anaerobic conditions (Supromin et al. 2015), similar to the ability of A. tumefaciens SUTS 1, and other microorganisms can decompose cyanide into ammonia and nitrate as byproducts and utilize them as nitrogen or carbon sources (Razanamahandry et al. 2019; Alvillo-Rivera et al. 2021), which are rapidly used by microbes (Wang et al. 1996). Other studies have reported that several kinds of microorganisms use the ammonia produced from thiocyanate degradation as a source of nitrogen for growth (Acheampong et al. 2010; Alvillo-Rivera et al. 2021). Furthermore, Holt et al. (1994) noted that nitrate and ammonia salts could be the sole nitrogen sources used by Agrobacterium sp. or microbes that can oxidize ammonia and transform it into nitrite and nitrate or that microbes could be involved in converting these byproducts into CO2 and N2 (Akcil 2003), but the enzymatic mechanisms involved have not yet been fully elucidated. Several distinct enzymatic mechanisms can result in the production of ammonia from cyanide degradation (Bouari et al. 2013; Anning et al. 2021). These findings provide an understanding of aerobic decomposition over 30 days. A removal efficiency of up to 80% was achieved for the cyanide treatment, and the BOD and COD percentage removals were approximately 50–60% and 20–30%, respectively.

Fig. 4.

Fig. 4

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Byproducts formed from cyanide degradation over 30 days in the aerobic system

Fig. 5.

Fig. 5

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Byproducts formed of sulfate and bicarbonate from cyanide degradation over 30 days in the aerobic system

Heavy metals in the form of Cu, Zn, Ni, and Cr were removed in the aerobic system. The Ni and Cr contamination levels in the electroplating effluent were very high (Table 1). Copper was rapidly eliminated during the first 24 h, and the removal efficiency stabilized at approximately 50–70%. Copper was removed to the range of 0.03–0.05 mg/L, and later, from days 25 to 30, the removal efficiency decreased. An equilibrium may be reached in the uptake of the metals on the cell surface, followed by an efflux mechanism caused by bacterial efflux pumps. This mechanism, in most bacteria isolated from areas with metal pollution, has been shown to function as a resistance system (Rosas-Ramírez et al. 2023). When zinc was removed, the removal did not stabilize. The removal efficiency over 30 days was approximately 30–90%. The zinc concentration decreased to the range of 1.0–2.0 mg/L. Microorganisms have mechanisms for resistance to metallic compounds and detoxification in response to the presence of metals in the environment. Common defense systems or systems specific to each metal might exist. Some metals, such as zinc and copper, are essential trace elements. They may play a considerable role in the formation of complexes (such as zinc fingers in DNA) and as constituents of cell enzymes (Domingues et al. 2020; Irawati et al. 2021). Bacterial cells can take up zinc through a fast, nonspecific absorption mechanism, and zinc is typically found in greater concentrations than other heavy metals are but is less hazardous (Domingues et al. 2020). In addition, Pseudomonas sp. is tolerant to copper ion accumulation in the periplasm and the internal and outer walls of cells (Cooksey 1994; Abd-Elhalim et al. 2019). These mechanisms may be active under optimal conditions, such as those related to nutrients, microorganism cell counts, initial cyanide concentration, oxygen availability, retention time, pH, and temperature (Moradkhani et al. 2018; Alvillo-Rivera et al. 2021). A comparison of the removal efficiencies of nickel and chromium revealed that nickel could be removed, and after the first 24 h, the maximum efficiency was approximately 63.43%. The residual nickel concentration was 18.41 mg/L. In addition, in the first 5 days, the removal efficiency was approximately 60%. The Ni residuals were within the range of 18.41–20.04 mg/L, and the system nickel removal performance decreased to 20–40%. According to an earlier study, free nickel released from compounds reacts rapidly with sulfide to produce a nickel sulfide precipitate during cyanide degradation (Quan et al. 2004). Consequently, cyanide decomposition and nickel precipitation demonstrate the bioremediation of cyanide in these systems. However, Bacillus subtilis N10 had the highest uptake rate, at 60.1% Ni2+, within 2 h of contact, according to research by EI-Sersy and EI-Sharouny (2007). Raja et al. (2006) and Alhammadi et al. (2024) also reported that nickel was eliminated quickly. In addition, this study revealed that high concentrations of nickel, up to approximately 50 mg/L, could be used for treatment. This did not interfere with the growth of microbes in the bioreactor system during the 30-day operating period. Furthermore, microorganisms can import nickel into cells via ATP-binding cassette transporters that transport nickel into the inner membrane of cells (Mulrooney and Hausinger 2003). In contrast, Poulson et al. (1997) reported that nickel concentrations greater than 20 mg/L considerably affected the growth of microorganisms. Nevertheless, the presence of metal cyanide in wastewater can affect the treatment of nitrate. Sirianuntapiboon and Chumlaong (2013) reported that the efficiency of nitrogen treatment in the form of ammonia and nitrate decreased when the concentrations of Ni2+ and Pb2+ were high. A similar observation was made in an earlier study (Zou et al. 2013). However, their study demonstrated that influent wastewater heavy metals did not affect nitrite or nitrate treatment efficiency. A decreasing trend was observed for these substances throughout the treatment. For Cr, removal occurred quite consistently over the last 5 days, from 24.68 to 25.80 mg/L to approximately 14.26–14.68 mg/L (Fig. 6). Thereafter, the removal efficiency decreased, with the residual chromium content ranging from approximately 16.5521.61 mg/L (removal efficiency of approximately 20–30%). The chromium in the control system was removed after the first 24 h, which was slower than that in the experimental system. Although the system can remove chromium, microbes are affected by heavy metal toxicity. This was determined on the basis of the constant number of cells throughout the treatment, which was similar to the findings of a previous study (Pal et al. 2004; Raja et al. 2006). Microbes have mechanisms to reduce the toxicity of chromium, such as the use of oxidase enzymes and reductase enzymes to change Cr6+ to Cr3+, the less toxic form (Joutey et al. 2014, 2015), and promote its uptake into cells (Brown et al. 2006). In addition, chromium removal by microorganisms occurs under aerobic, anoxic, and anaerobic conditions (Ramirez-Diaz et al. 2008). According to earlier research, aerobic conditions increased the rates of the reduction of Cr6+ to Cr3+ more than anaerobic conditions did (Ishibashi et al. 1990). Hence, the aeration system promoted faster removal of chromium, along with other factors. Nickel and chromium still exceeded the wastewater discharge criteria for factories situated in industrial compounds in Thailand. It would be suggested that the use of immobilized cells might be one of the bioremediation processes for the enhancement of those metals removal (EI-Sersy and EI-Sharouny 2007; Guadalima and Monteros 2018; Mehrotra et al. 2021; Schommer et al. 2023). The use of immobilized cells might be a bioremediation process for enhancing the removal of these metals (Mehrotra et al. 2021; Schommer et al. 2023). However, the addition of the SUTS 1 and SUTS 2 microbial groups increased the system’s removal efficiency. The bacteria were able to grow and withstand several types of heavy metal toxicity better than those in the control system (Fig. 3). Most research has focused on the treatment of cyanide compounds and heavy metals and on cyanide and/or metal cyanide complex treatment in synthetic wastewater (Khamar et al. 2015; Singh and Balomajumder 2016; Alvarado-López et al. 2023; Zmirli et al. 2023), and the treatment of metal cyanide in real wastewater has been studied but not often. This work demonstrated the high degradation and/or removal efficiency of metal cyanide in the first 7 days of treatment. For the days on which the system had high removal rates, the cyanide removal rates were greater than those of zinc, copper, nickel, and chromium (CN− > Zn > Cu > Ni > Cr), reaching 96.67%, 93.93%, 74.17%, 63.43%, and 44.65%, respectively. However, the water still contained residual amounts of 0.15, 0.24, 0.03, 18.41, and 14.26 mg/L of the metals. Furthermore, in the long-term treatment system, heavy metal contamination of the wastewater did not affect the treatment of cyanide by microbes, demonstrating that the degradation efficiency of cyanide over 30 days was approximately 80–90%.This finding was similar to the results of a study by Maniyam et al. (2013), who reported that heavy metals did not affect cyanide treatment by microbes.

Fig. 6.

Fig. 6

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Heavy metal removal efficiency over 30 days in the aerobic system

The characterization of metal accumulation on bacterial cells in the aerobic system

In addition, many biosorption studies on heavy metal elimination from aqueous solutions have been carried out. Almost all of these methods are intended to optimize biosorption parameters to achieve the greatest elimination efficiency, and biosorption mechanisms have been investigated in other studies (Ramya and Thatheyus 2018; Girdhar et al. 2022; Alhammadi et al. 2024). According to Zouboulis et al. (2004), the biosorption process allows some microbial biomass to retain large amounts of metal ions. Scanning electron microscopy (SEM) and energy dispersive X-ray (EDX) analysis were used to obtain insights into the mechanism and chemical components resulting in heavy metal sequestration by bacteria. The order of the accumulation of elements was carbon, nitrogen, copper, zinc, nickel, and chromium on day 15 and day 30 at random positions on the bacterial cell walls. The bacterial cells were sampled on day 15 at 6 random positions (Table 4). This analysis demonstrated that each position on the sample contained different elements. Metal adsorption onto the cell walls of bacteria was also confirmed by EDX analysis. The SEM and EDX images are presented in Fig. 7. The main elements found on the cell surfaces of bacteria were carbon, nitrogen, and oxygen, on average, at approximately 55.07%, 11.88%, and 27.71% by weight, and copper, zinc, nickel, and chromium, on average, were approximately 0.81%, 1.53%, 0.87% and 2.12% by weight, respectively. On day 30, the same elements were found on the cell surface as they were on day 15, but chromium was not found. The accumulated elements on the cell walls included carbon, nitrogen, oxygen, copper, zinc, and nickel, which were present at approximately 56.90%, 12.09%, 27.99%, 0.25%, 0.94%, and 1.83% by weight, respectively. This may be because functional groups on the surface of microorganisms rapidly take up chromium in the initial phase before reaching equilibrium, which helps biosorbents bind metal ions through equilibrium reactions (Rangsayatorn et al. 2002; Chojnacka et al. 2005). Subsequently, efflux occurs via bacterial efflux pumps (Abdelbary et al. 2019; Bazzi et al. 2020). Similar to the results of the treatment, a high removal efficiency for chromium was observed in the first 5 days, after which the efficiency decreased. Similar results were obtained in the bioreactor treatment, which achieved the rapid removal of metals within the first 7 days, after which metal uptake decreased (Alboghobeish et al. 2014). Therefore, the reason may be that on day 30, there was no chromium on the cell surfaces of the microbes. Kim et al. (2007) used SEM and EDX studies to verify that biosorption mechanisms vary depending on the types of metals passing through the cell surfaces of the bacteria that were isolated and that the Bacillus spp. strain CPB4 had a high absorption capacity for metals present in both pure and combined heavy metal solutions (Pb > Cd > Cu > Ni > Co > Mn > Cr > Zn). Thus, all of these approaches generally demonstrate that bacteria either prevent metal ions from entering cells or actively pump metal ions out of cells (Abdelbary et al. 2019; Girdhar et al. 2022). Microorganisms have developed strategies for resistance to metals and metal toxicity, including the efflux of metal ions and the use of detoxifying enzymes in response to the presence of metal contaminants in the environment (Bruins et al. 2000). P-type ATPase efflux and RND-driven transporter mechanisms are the two major pathways of efflux (I) and (II), respectively (Scherer and Nies 2009). At an elementary level, the nutritional requirements for bacterial growth must be satisfied. This study shows glucose as a carbon source that supported bacterial growth and increased the degradation similar to Mirizadeh et al. (2014). Furthermore, the major constituents, i.e., carbon, oxygen, and nitrogen, are approximately 50%, 20%, and 14% by weight in cells, respectively. Trace elements such as manganese, zinc, molybdenum, copper, and cobalt, which are needed by certain cells, were found in smaller amounts of 0.3% by weight (Cowan 2015). The results of this work demonstrate that the microorganisms in the system can remove metals, accumulate heavy metals on cell walls and tolerate heavy metal toxicity even at high concentrations of nickel (approximately 48.78–50.35 mg/L) and chromium (24.68–25.80 mg/L). The concentrations of copper and zinc were in the ranges of 0.10–0.13 and 3.71–3.96 mg/L, respectively, and bacteria could grow continuously, as demonstrated over 30 days.

Table 4.

Accumulation of heavy metals on the cell walls of microorganisms on days 15 and 30 at random locations on the cell walls

Days Positions Weight%, (total 100%)
Carbon (C) Nitrogen (N) Oxygen (O2) Copper (Cu) Zinc (Zn) Nickel (Ni) Chromium (Cr)
15 1 46.48 20.19 29.60 ND 1.55 2.18 ND
2 53.12 19.80 24.16 ND 1.35 1.57 ND
3 45.47 16.81 22.99 ND 0.56 1.45 12.72
4 62.75 ND 31.47 2.65 3.13 ND ND
5 69.24 ND 27.05 2.23 1.48 ND ND
6 53.38 14.50 31.01 ND 1.11 ND ND
Average 55.07 11.88 27.71 0.81 1.53 0.87 2.12
30 1 64.37 ND 28.38 ND ND 7.25 ND
2 55.59 16.26 24.39 ND 1.47 2.28 ND
3 61.54 ND 34.29 ND 4.17 ND ND
4 48.76 22.01 29.23 ND ND ND ND
5 58.10 14.61 25.86 ND ND 1.43 ND
6 53.06 19.67 25.77 1.51 ND ND ND
Average 56.90 12.09 27.99 0.25 0.94 1.83 ND
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ND not detected

Fig. 7.

Fig. 7

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Scanning electron microscopy analysis of a sample on days 15 (A) and 30 (B). Energy dispersive X-ray analysis of the elemental composition of heavy metals on the cell surface on days 15 (C) and 30 (D)

Conclusion

These results offer a comprehensive overview of the bioremediation of metal cyanide complexes from electroplating effluent by aerobic bioreactor treatment. In the long-term reactor, the system was able to treat cyanide and heavy metals with high efficiency during the first 7 days, and the efficiency of cyanide treatment through the 30-day operation was not affected by the presence of several heavy metals in the system. In addition to almost complete cyanide degradation, the treatment system's efficiency reached 80–90%, and the maximum removal efficiency values of zinc, copper, nickel, and chromium were approximately 93.93%, 74.17%, 63.43%, and 44.65%, respectively. This confirmed that the mixed microbial culture could accumulate several metal elements on the cell surface over the long term and was able to resist toxicity from heavy metals. Microbial growth was stable at approximately 107 CFU/mL. Therefore, an aerobic treatment system could provide a promising alternative for treating metal cyanide-containing wastewater by achieving high-efficiency bioremediation of cyanide and its decomposition into less toxic compounds, such as ammonia, nitrite, and nitrate. This can be achieved when enough aeration and carbon are supplied to ensure good biological treatment performance for metal cyanide remediation, and the process is environmentally friendly.

Acknowledgements

This research was supported and funded by Suranaree University of Technology, Nakhon Ratchasima, Thailand. We thank Prof. Dr. Prayad Pokethitiyook for the scientific suggestions regarding this manuscript.

Data availability

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

Declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

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