Polybrominated diphenyl ether (PBDE) removal from wastewater: a perspective on advancing microbial technologies

INTRODUCTION

Flame retardants, such as polybrominated diphenyl ethers (PBDEs), are a contaminants of emerging concern (CEC) that pose many environmental challenges. Used for decades in a variety of consumer products such as furniture and electronics, PBDEs are detected in the environment despite production bans and regulatory efforts^[1]. They are found in aquatic environments at concentrations that can adversely affect the health of exposed species^[2,3]. Specifically, PBDEs disrupt endocrine systems in fish and other animals, leading to health implications^[4], including impaired thyroid function^[5] and changes in disease susceptibility^[2,3].

The chemical and physical characteristics have previously been described^[4]. Briefly, PBDEs have the base chemical formula of C₁₂H_(x)Br_(10-x)O. There are 209 possible congeners with log K_OW ranging from 4.3 to 9.9, all of which are classified as hydrophobic. Given the challenge presented by their large number, sorption coefficients for the PBDE congeners have been estimated using modeling methods^[6], while physical measurements of these coefficients have been less frequent. Sorption potential generally increases with increased bromination, with the exception of some congeners (such as BDE-154, BDE-183, and BDE-209) where bromide-bromide interactions can interfere with sorption behavior^[6].

A common pathway for PBDE movement to the environment is through treated wastewater^[7], highlighting the need for effective treatment technologies. While considerable research has focused on various methods for PBDE removal from wastewater, these are limited in their effectiveness^[8]. There remains a critical gap in exploring the potential of integrating biological degradation with sorptive techniques to enhance pollutant removal. In this perspective, an approach is proposed using bio-inoculated sorptive materials to support and improve the bacterial degradation of PBDEs from wastewater, ultimately reducing the entry of PBDEs and other co-occurring CECs^[9] into aquatic environments.

ENVIRONMENTAL IMPACTS OF PBDES

The global production of all PBDEs between 1970 and 2020 was around 1,900,000 tons^[1,10]. Considering the low rate of degradation, a significant portion of this PBDE mass remains in products or distributed in the environment. PBDEs have been detected in soil, water, sediments^[4], and wastewater^[10] throughout the world. Concentrations of PBDEs in effluent wastewater are much lower than in influent, with more than half of the PBDEs associated with suspended particles in both raw and treated wastewater^[10]. Pollution plumes in natural waters are very low and often measured in fmol per L concentrations^[11]. However, PBDEs are lipophilic and persistent^[12], which contributes to their impacts on marine and terrestrial species. As an alternative to measuring marine water plumes, pollution levels can be tracked by measuring concentration in the fatty tissues of fish, sharks, and whales^[13,14]. PBDEs are present across the food web. Fish and other marine animals bioaccumulate and biomagnify PBDEs from effluent wastewater through exposures in water, sediment, and their food. PBDEs were detected in penguin eggs as far as Antarctica^[15] and have been shown to accumulate across trophic levels of fish species^[16,17], particularly in high trophic level marine mammals, including Southern Resident Killer Whales, which can accumulate high concentrations of persistent chemicals, such as PBDEs^[18].

Despite decreasing trends in environmental concentrations, PBDEs continue to be a contaminant of concern. For example, West et al. (2017) reported that concentrations of PBDEs in Pacific herring declined between approximately 2000-2015, though levels remained above health effects thresholds, particularly in stocks from the more urbanized embayments^[17]. Similar spatial patterns have been documented for PBDE concentrations in tissues of Dungeness crab, English sole, and spiny dogfish, with significantly higher concentrations being reported in biota from highly urbanized areas compared to less urbanized areas^[19]. Receiving waters impacted by relatively high concentrations of wastewater effluent, even those outside urbanized areas, can be highly impacted by PBDEs^[20]. Monitoring juvenile Chinook salmon in the Snohomish River found high concentrations of PBDEs, at levels that could affect fish health^[2,3,7,21]. The highest concentrations were found in the fish at the lower portions of the Snohomish River, with values reaching 1,500 ng total PBDE per g lipid weight^[21]. Treated wastewater discharges were identified as the source of PBDE in the Snohomish River. A screening study was performed to characterize the influent of a wastewater treatment plant (WWTP) in the Snohomish River basin, as well as the effluent of several industrial discharges that were released directly into the WWTP conveyance system^[22]. The study identified three facilities (an industrial laundry, an aerospace facility, and a landfill) with PBDE concentrations > 100 ng/L, with the PBDE concentrations in the industrial laundry ~3,500 ng/L, which was 20× greater than detected in samples from any other facility. In addition, since PBDEs are legacy pollutants, their detection may not be associated with current applications. Thus, mitigation of the impacts on juvenile Chinook and other organisms must rely on engineered treatment technologies instead of source controls such as legislative solutions to end the use of the chemical.

PAST APPROACHES TO PBDE TREATMENT

There has been a large body of work evaluating the treatment, fate, and transport of PBDEs (reviewed in^[8,23]). Three treatment approaches have shown effectiveness in lab-based studies for removing PBDE from water, including sorptive removal, biological transformation, and photocatalytic transformation [Table 1]. Each approach has limitations, and there is currently a lack of technologies that have been adopted within the wastewater treatment industry.

Sorption is the primary removal mechanism in traditional wastewater treatment^[24]. PBDEs are hydrophobic compounds and thus have an affinity to sorb to organic particulate matter. During wastewater treatment, PBDEs are moved from the water to the activated sludge^[25]. Less-brominated BDEs (BDE-3 and BDE-15) partition to common adsorbents (black tea and coconut palm leaf powders) with short retention times^[26]. Engineered modifications to secondary treatment processes can alter sorption efficiency, including chemical modifiers to improve adsorption or cation additions to decrease adsorption^[27], though this approach has not been tested for PBDEs. Sorptive removal of PBDEs has additionally been demonstrated as a tertiary (i.e., polishing) step for municipal wastewater treatment^[28], documenting the efficacy of absorbents across the range of PBDE congeners under environmentally realistic conditions. While modeling^[6] provides a starting point for sorptive-removal designs, the experimental data on sorption coefficients for all 209 congeners with comparisons among differing sorptive materials and wastewater conditions are missing. Filling this gap will require worldwide data sharing building on current efforts^[24,26,28] to ensure that information is garnered from case studies and bench studies representing broad ranges of wastewater conditions. As an additional challenge, sorption only moves the PBDEs, and the sorbent must be either regenerated or, more often, disposed of in a landfill. Since landfill leachate is among the industrial sources of PBDEs to municipal wastewater treatment facilities, sorption alone is not a sustainable solution.

Complete bacterial degradation of PBDEs can occur, but the process does not occur in a single step. Aerobic biodegradation of PBDEs has been documented using bacteria within the Bacillus^[24] and Rhodococcus sp. (with genome evaluation)^[23], and by aerobic mixed cultures enriched in Arcobacter sp.^[29]. However, aerobic PBDE biodegradation can be congener-specific^[30], and highly brominated PBDEs are resistant to oxidation. During aerobic wastewater treatment, the removal of highly brominated PBDE (i.e., BDE-209) is via absorption and not by microbial degradation^[31]. Anaerobic bacteria are capable of debrominating PBDEs^[32]. Several cultured anaerobic bacteria have been identified with intrinsic PBDE-debromination capabilities, such as Dehalococcoides sp.^[33,34]. Other work has found PBDE debrominators present in wastewater sludge^[35,36]. Shifts in microbial community structures have been documented in association with improved BDE-209 degradation during anaerobic wastewater treatment^[37], and facultative anaerobes can also contribute to BDE-209 degradation, though these are often identified to be uncultured species^[36]. However, the anaerobic step on its own is insufficient, because highly brominated compounds - such as BDE-209 - are converted to partially brominated compounds - such as BDE-90 and -47, which are not completely degraded and may be more toxic than the parent compound. To achieve complete destruction of the PBDEs, an oxidative step is required, during which aerobic bacteria break the carbon-carbon bonds in the diphenyl ether core of less-brominated PBDE, resulting in final destruction^[38]. Genetic studies have been conducted with an aim toward identifying the genes associated with aerobic^[38] and anaerobic^[39] PBDE biodegradation, which allow current researchers to test hypotheses about whether PBDE-degrading genes are active in a treatment system.

ENHANCING MICROBIAL TREATMENT TECHNOLOGIES THROUGH COMBINATION WITH SORPTION

Neither sorptive removal nor biological degradation, when used alone, is an effective approach for PBDE removal in wastewater treatment systems^[8]. Spent sorptive materials must be disposed of or recharged, and bacterial degradation can be too slow compared to the treatment times in wastewater systems. A solution for increasing the residence time for the bacteria in wastewater could be achieved by combining sorption with biological degradation. This combined approach has been documented in anaerobic granular sludge reactors for some trace-level organic pollutants where sorption to the biological granules was shown to be part of the removal mechanism^[40], though this combination has yet to be tested for the treatment of PBDEs. As an additional example, a biofilm fluidized-bed reactor can improve biodegradation by retaining slow-growing bacteria within the reactor without the need for decreasing hydraulic retention times. Combined sorption and biological degradation has been demonstrated for recalcitrant organic pollutants such as phenol^[41] and in sequencing batch mode for biodegradation of the recalcitrant aromatic pollutants 2,4-dinitrotoluene and 2,6-dinitrotoluene^[42]. As an additional benefit, fluidized-bed reactors also function well for conventional wastewater contaminants while requiring less energy than other biosystems^[43].

For a fluidized bed, the appropriate solid material support is important. Granular activated carbon (GAC) and zero-valent iron are both commonly used in wastewater treatment, but have an energy and material sourcing footprint that reduces the sustainability of these materials. Biochar is an eco-friendly granular support material that is documented for its ability to create an environment for microbes that contains cation exchange capacity, sorption capacity, and high porosity^[44-46]. In addition, biochar can be made from a range of organic waste materials such as wood chips, algae, biosolids, crop residues, and other organic solid waste^[47-50], making it a sustainable and locally sourceable resource for treatment processes. It has been reported as an excellent material for biofilm development^[51] and is amenable to bioinoculation for application in wastewater treatment^[52]. In addition, microbial interactions within the micropores in biochar facilitate stabilized anaerobic microbial processes^[53], which is important for the breakdown of PBDE molecules into less brominated compounds.

We submit that two fluidized-bed reactors in series could solve the challenges of removal of PBDEs (and potentially other CECs) from wastewater. Using anaerobic-aerobic systems with biochar to treat municipal and industrial wastewater has been shown to achieve microbial degradation of other contaminants^[54,55], and here we propose this as a potential solution for PBDE biodegradation. The first reactor would be anaerobic to allow PBDEs to debrominate. The anaerobic step requires an abundance of an electron donor^[56], which would be supplied by the untreated municipal wastewater. The second reactor would be aerobic to allow biological cleavage of the carbon-carbon bonds in the diphenyl ether core of the residual PBDEs. Inoculated biochar added to each reactor would improve the treatment by encouraging rapid sorptive removal that would extend contact times for biological conversion. Pilot scale testing is needed to document the efficacy of immobilized bacterial cultures on sorptive materials using real-world wastewater to ensure an understanding of how the complex and variable matrix affects PBDE biological removal.

CONCLUSION

The scientific community has faced the challenge of treatment for trace-level organic pollutants for more than two decades^[57-60]. It is time to move from documentation of the fundamentals toward demonstration of technologies that can be applied at real-world wastewater treatment facilities, while also considering the resource limitations faced by smaller communities. Inoculated biochar in anaerobic and aerobic reactors is a way forward through the innovative application of established knowledge that can create economically, socially, and environmentally sustainable solutions. Case study documentation of these efforts will be critical in establishing the influence of wastewater and biochar variability on the efficacy of this treatment approach.