Skip to main content
SpringerLink
Log in

Understanding the mechanism of polybrominated diphenyl ethers reducing the anaerobic co-digestion efficiency of excess sludge and kitchen waste

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Polybrominated diphenyl ethers (PBDEs) widely existing in the environment can pose a serious threat to the ecological safety. However, the influence of PBDEs on methane production by excess sludge (ES) and kitchen waste (KW) anaerobic co-digestion and its mechanism is not clear. To fill this gap, in this work, the co-digestion characteristics of ES and KW exposed to different levels of PBDEs at medium temperature were investigated in sequencing batch reactor, and the related mechanisms were also revealed. The results showed that PBDEs reduced methane production and the proportion of methane in the biogas. Methane yield decreased from 215.3 mL/g· volatile suspended solids (VSS) to 161.5 mL/(g·VSS), accompanied by the increase of PBDE content from 0 to 8.0 mg/Kg. Volatile fatty acid (VFA) yield was also inhibited by PBDEs; especially when PBDEs were 8.0 mg/Kg, VFA production was only 215.6 mg/g VSS, accounting for 75.7% of that in the control. Mechanism investigation revealed PBDEs significantly inhibited the processes of hydrolysis, acidogenesis, acetogenesis, and methanogenesis. Further study showed that PBDEs could inhibit the degradation and bioavailability of ES and KW, but it had a greater inhibition on the utilization of KW. Enzyme activity investigation revealed that all the key enzyme activities related to methane production were suppressed by PBDEs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  • Appels L, Baeyens J, Degrève J, Dewil R (2008) Principles and potential of the anaerobic digestion of waste-activated sludge. Prog Energ Combust 34(6):755–781

    Article  CAS  Google Scholar 

  • Chai M, Li R, Shi C, Shen X, Li R, Zan Q (2019) Contamination of polybrominated diphenyl ethers (PBDEs) in urban mangroves of Southern China. Sci Total Environ 646:390–399

    Article  CAS  Google Scholar 

  • Chen Y, Zhu R, Jiang Q, Sun T, Li M, Shi J, Chai H, Gu L, He Q (2019) Effects of green waste participation on the co-digestion of residual sludge and kitchen waste: a preliminary study. Sci Total Environ 671:838–849

    Article  CAS  Google Scholar 

  • Dong B, Xia Z, Sun J, Dai X, Chen X, Ni BJ (2019) The inhibitory impacts of nano-graphene oxide on methane production from waste activated sludge in anaerobic digestion. Sci Total Environ 646:1376–1384

    Article  CAS  Google Scholar 

  • Dorman DC, Chiu W, Hales BF, Hauser R, Johnson KJ, Mantus E, Martel S, Robinson KA, Rooney AA, Rudel R, Sathyanarayana S, Sl S, Waters KM (2018) Polybrominated diphenyl ether (PBDE) neurotoxicity: a systematic review and meta-analysis of animal evidence. J Toxicol Env Heal B 21(4):269–289

    Article  CAS  Google Scholar 

  • Ezechiáš M, Covino S, Cajthaml T (2014) Ecotoxicity and biodegradability of new brominated flame retardants: a review. Ecotox Environ Safe 110:153–167

    Article  Google Scholar 

  • Fabrellas B, Larrazabal D, Martinez MA, Eljarrat E, Barcelo D (2004) Presence of polybrominated diphenyl ethers in Spanish sewage sludges. Important Contrib Deca-BDE Organohal Compd 66:3755–3760

    Google Scholar 

  • Gao Y, Zhao J, Qin C, Yuan Q, Zhu J, Sun Y, Lu C (2021) Evaluating the effect of fluoxetine on mesophilic anaerobic dark biohydrogen fermentation of excess sludge. Bioresour Technol 125320

  • Hale RC, La Guardia MJ, Harvey EP, Gaylor MO, Mainor TM, Duff WH (2001) Persistent pollutants in land-applied sludges. Nature 412(6843):140–141

    Article  CAS  Google Scholar 

  • Huang X, Liu X, Chen F, Wang Y, Li X, Wang D, Tao Z, Xu D, Xue W, Geng M, Yang Q (2020a) Clarithromycin affect methane production from anaerobic digestion of waste activated sludge. J Clean Prod 255:120321

  • Huang C, Dong H, Zhang Z, Bian H, Yong Q (2020b) Procuring the nano-scale lignin in prehydrolyzate as ingredient to prepare cellulose nanofibril composite film with multiple functions. Cellulose 27(16):9355–9370

    Article  CAS  Google Scholar 

  • Huang C, Zheng Y, Lin W, Shi Y, Huang G, Yong Q (2020c) Removal of fermentation inhibitors from pre-hydrolysis liquor using polystyrene divinylbenzene resin. Biotechnol Biofuels 13(1):1–14

    Article  Google Scholar 

  • Jiang Y, Yuan L, Lin Q, Ma S, Yu Y (2019) Polybrominated diphenyl ethers in the environment and human external and internal exposure in China: a review. Sci Total Environ 696:133902

  • Kuang Y, Zhao J, Gao Y, Lu C, Luo S, Sun Y, Zhang D (2020a) Enhanced hydrogen production from food waste dark fermentation by potassium ferrate pretreatment. Environ Sci Pollut Res 27:18145–18156

    Article  CAS  Google Scholar 

  • Kuang Y, Gao Y, Zhang J, Zhao J, Luo S, Zhang D, Lu C, Sun Y (2020b) Effect of initial pH on the sludge fermentation performance enhanced by aged refuse at low temperature of 10 °C. Environ Sci Pollut Res 27:31468–31476

    Article  CAS  Google Scholar 

  • Lin JG, Chang CN, Chang SC (1997) Enhancement of anaerobic digestion of waste activated sludge by alkaline solubilization. Bioresour Technol 62(3):85–90

    Article  CAS  Google Scholar 

  • Li J, Chen Y, Xiao W (2017) Polybrominated diphenyl ethers in articles: a review of its applications and legislation. Environ Sci Pollut Res 24(5):4312–4321

    Article  CAS  Google Scholar 

  • Li Y, Chen Y, Wu J (2019) Enhancement of methane production in anaerobic digestion process: a review. Appl Energ 240:120–137

    Article  CAS  Google Scholar 

  • Li M, Jiang H, Hao Y, Du K, Du H, Ma C, Tu H, He Y (2021) A systematic review on botany, processing, application, phytochemistry and pharmacological action of Radix Rehmnniae. J Ethnopharmacol 114820

  • Lin W, Yang J, Zheng Y, Huang C, Yong Q (2021) Understanding the effects of different residual lignin fractions in acid-pretreated bamboo residues on its enzymatic digestibility. Biotechnol Biofuels 14(1):1–15

    Article  Google Scholar 

  • Liang Z, Xu G, Shi J, Yu S, Lu Q, Liang D, Sun L, Wang S (2021) Sludge digestibility and functionally active microorganisms in methanogenic sludge digesters revealed by E. coli-fed digestion and microbial source tracking. Environ Res 193: 110539

  • Liu X, Du M, Yang J, Wu Y, Xu Q, Wang D, Yang Q, Yang G, Li X (2020) Sulfite serving as a pretreatment method for alkaline fermentation to enhance short-chain fatty acid production from waste activated sludge. Chem Eng J 385:123991

  • Ma J, Qiu X, Zhang J, Duan X, Zhu T (2012) State of polybrominated diphenyl ethers in China: an overview. Chemosphere 88(7):769–778

    Article  CAS  Google Scholar 

  • Mu L, Zhang L, Zhu K, Ma J, Ifran M, Li A (2020). Anaerobic co-digestion of sewage sludge, food waste and yard waste: synergistic enhancement on process stability and biogas production. Sci Total Environ 704:135429

  • Mehariya S, Patel AK, Obulisamy PK, Punniyakotti E, Wong JW (2018) Co-digestion of food waste and sewage sludge for methane production: current status and perspective. Bioresour Technol 265:519–531

    Article  CAS  Google Scholar 

  • Narihiro T, Sekiguchi Y (2011) Oligonucleotide primers, probes and molecular methods for the environmental monitoring of methanogenic archaea. Microb Biotechnol 4(5):585–602

    Article  CAS  Google Scholar 

  • Palacio-Cortés AM, de Lourdes S-S, Hara ELY, Disner RG, Rebechi D, Grassi MT, Cestari MM, Navarro-Silva MA (2017) Polybrominated diphenyl ethers (PBDEs) effects on Chironomus sancticaroli larvae after short-term exposure. Ecotox Environ Safe 139:308–315

    Article  Google Scholar 

  • Pan Y, Zhi Z, Zhen G, Lu X, Bakonyi P, Li YY, Zhao Y, Banu JR (2019) Synergistic effect and biodegradation kinetics of sewage sludge and food waste mesophilic anaerobic co-digestion and the underlying stimulation mechanisms. Fuel 253:40–49

    Article  CAS  Google Scholar 

  • Rayne S, Ikonomou M G (2005) Polybrominated diphenyl ethers in an advanced wastewater treatment plant. Part 1: concentrations, patterns, and influence of treatment processes. J Environ Eng Sci 4(5):353–367

  • Seberini A (2020) Economic, social and environmental world impacts of food waste on society and zero waste as a global approach to their elimination. In SHS Web of Conferences(Vol. 74, p. 03010). EDP Sciences

  • Singh J, Ordoñez I (2016) Resource recovery from post-consumer waste: important lessons for the upcoming circular economy. J Clean Prod 134:342–353

    Article  Google Scholar 

  • Stiborova H, Vrkoslavova J, Pulkrabova J, Poustka J, Hajslova J, Demnerova K (2015) Dynamics of brominated flame retardants removal in contaminated wastewater sewage sludge under anaerobic conditions. Sci Total Environ 533:439–445

    Article  CAS  Google Scholar 

  • Wang D, He D, Liu X, Xu Q, Yang Q, Li X, Liu Y, Wang Q, Ni B, Li H (2019) The underlying mechanism of calcium peroxide pretreatment enhancing methane production from anaerobic digestion of waste activated sludge. Water Res 164:114934

  • Wang D, Zeng G, Chen Y, Li X (2015) Effect of polyhydroxyalkanoates on dark fermentative hydrogen production from waste activated sludge. Water Res 73:311–322

    Article  CAS  Google Scholar 

  • Wang R, Zheng L, Xu Q, Xu L, Wang D, Li J, Lu G, Huang C, Wang Y (2021a) Unveiling the structural properties of water-soluble lignin from gramineous biomass by autohydrolysis and its functionality as a bioactivator (anti-inflammatory and antioxidative). Int J Biol Macromol 191:1087–1095

    Article  CAS  Google Scholar 

  • Wang X, Tang S, Chai S, Wang P, Qin J, Pei W, Bian H,Jiang Q, Huang C (2021b) Preparing printable bacterial cellulose based gelatin gel to promote in vivo bone regeneration. Carbohyd Polym 118342

  • Wei W, Huang QS, Sun J, Wang JY, Wu SL, Ni BJ (2019) Polyvinyl chloride microplastics affect methane production from the anaerobic digestion of waste activated sludge through leaching toxic bisphenol-A. Environ Sci Technol 53(5):2509–2517

    Article  CAS  Google Scholar 

  • Wu D, Li L, Zhao X, Peng Y, Yang P, Peng X (2019) Anaerobic digestion: a review on process monitoring. Renew Sust Energ Rev 103:1–12

    Article  CAS  Google Scholar 

  • Wu Z, He C, Han W, Song J, Li H, Zhang Y, Jing X, Wu W (2020) Exposure pathways, levels and toxicity of polybrominated diphenyl ethers in humans: a review. Environ Res :109531

  • Xu Q, Huang Q S, Wei W, Sun J, Dai X, Ni B J (2020a) Improving the treatment of waste activated sludge using calcium peroxide. Water Res 116440

  • Xu Q, Zeng Y, Tang W, Peng W, Xia T, Li Z, Teng F, Li W, Guo J (2020b) Multi-task joint learning model for segmenting and classifying tongue images using a deep neural network. Ieee J Biomed Health 24(9):2481–2489

    Article  Google Scholar 

  • Xu G, Zhao X, Zhao S, Chen C, Rogers MJ, Ramaswamy R, He J (2021a) Insights into the occurrence, fate, and impacts of halogenated flame retardants in municipal wastewater treatment plants. Environ Sci Technol 55(8):4205–4226

    Article  CAS  Google Scholar 

  • Xu G, Zhao X, Zhao S, He J (2021b) Acceleration of polychlorinated biphenyls remediation in soil via sewage sludge amendment. J Hazard Mater 420: 126630

  • Xu Q, Guo Q, Wang C X, Zhang S, Wen C B, Sun T, Peng W, Chen J, Li W H (2021c). Network differentiation: a computational method of pathogenesis diagnosis in traditional Chinese medicine based on systems science. Artif Intell Med 118: 102134

  • Yuan Q, Sui M, Qin C, Zhang H, Sun Y, Luo S, Zhao J (2022) Migration, transformation and removal of macrolide antibiotics in the environment: a review. Environ Sci Pollut Res 1–10

  • Zhao J, Jing Y, Zhang J, Sun Y, Wang Y, Wang H, Bi X (2019) Aged refuse enhances anaerobic fermentation of food waste to produce short-chain fatty acids. Bioresour Technol 289:121547

  • Zhao J, Xin M, Zhang J, Sun Y, Luo S, Wang H, Wang Y, Bi X (2020) Diclofenac inhibited the biological phosphorus removal: performance and mechanism. Chemosphere 243: 125380

  • Zhao J, Zhang J, Zhang D, Hu Z, Sun Y (2021a) Effect of emerging pollutant fluoxetine on the excess sludge anaerobic digestion. Sci Total Environ 752:141932

  • Zhao J, Yuan Q, Sun Y, Zhang J, Zhang D, Bian R (2021b) Effect of fluoxetine on enhanced biological phosphorus removal using a sequencing batch reactor. Bioresour Technol 320: 124396

  • Zhao S, Rogers M J, Cao L, Ding C, He J (2021c) Identification of reductive dehalogenases that mediate complete debromination of penta- and tetra-brominated diphenyl ethers in Dehalococcoides. Appl Environ Microb AEM-00602

  • Zhang J, Zhao J, Sun Y, Xin M, Zhang D, Bian R (2021) Mechanisms of emerging pollutant Dechlorane Plus on the production of short-chain fatty acids from sludge anaerobic fermentation. Environ Sci Pollut Res 28:34902–34912

    Article  CAS  Google Scholar 

  • Zheng L, Lu G, Pei W, Yan W, Li Y, Zhang L, Huang C, Jiang Q (2021a) Understanding the relationship between the structural properties of lignin and their biological activities. Int J Biol Macromol 190:291–300

    Article  CAS  Google Scholar 

  • Zheng Y, Yu Y, Lin W, Jin Y, Yong Q, Huang C (2021b). Enhancing the enzymatic digestibility of bamboo residues by biphasic phenoxyethanol-acid pretreatment. Bioresour Technol 325: 124691

  • Zheng L, Yu P, Zhang Y, Wang P, Yan W, Guo B, Huang C, Jiang Q (2021c) Evaluating the bio-application of biomacromolecule of lignin-carbohydrate complexes (LCC) from wheat straw in bone metabolism via ROS scavenging. Int J Biol Macromol 176:13–25

    Article  CAS  Google Scholar 

  • Zhou Q, Ge CH, Ahmad HA, Ni SQ, Liu X, Bu C, Wang F, Gao B (2018) Production of more toxic hexa-brominated diphenyl ether from rapid biotransformation of decabromodiphenyl ether in anaerobic granular sludge. Int Biodeter Biodegr 134:7–15

    Article  CAS  Google Scholar 

Download references

Funding

This research was financially supported by the project of the National Natural Science Foundation of China (NSFC) (51908305), the Open Fund of Innovation Institute for Sustainable Maritime Architecture Research and Technology (iSMART), Qingdao University of Technology (No. 2020–042), China Postdoctoral Science Foundation (2019M660162), Shandong Postdoctoral Innovation Project (202001017), and Shanghai Engineering Research Center of Biotransformation of Organic Solid Waste (SERC2020C05).

Author information

Authors and Affiliations

  1. School of Environmental and Municipal Engineering, Qingdao University of Technology, Qingdao, 266033, People’s Republic of China

    Jianwei Zhao, Chengzhi Qin, Meiping Sui, Siyi Luo & Huanyun Zhang

  2. Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

    Jiangwei Zhu

Authors
  1. Jianwei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chengzhi Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meiping Sui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siyi Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huanyun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiangwei Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J-Zhao investigated the experiment; CQ reviewed and revised the manuscript; MS analyzed the experimental data; SL directed the experimental design; HZ reviewed the manuscript; J-Zhu reviewed the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jianwei Zhao or Siyi Luo.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Ta Yeong Wu

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, J., Qin, C., Sui, M. et al. Understanding the mechanism of polybrominated diphenyl ethers reducing the anaerobic co-digestion efficiency of excess sludge and kitchen waste. Environ Sci Pollut Res 29, 41357–41367 (2022). https://doi.org/10.1007/s11356-022-18795-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-18795-x

Keywords

Search

Navigation