Skip to main content
Log in

The identification and performance assessment of dominant bacterial species during linear alkylbenzene sulfonate (LAS)-biodegradation in a bioelectrochemical system

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

The anionic surfactant linear alkylbenzene sulfonate (LAS) is a major chemical constituent of detergent formulation. Regarding the recalcitrant nature of sulfonoaromatic compounds, discharging these substances into wastewater collection systems is a real environmental issue. A study on LAS biodegradation based on bioelectrochemical treatment and in the form of developing a single-chamber microbial fuel cell with air cathode is reported in the present work. Pretreatment study showed LAS concentration of 60 ppm resulted in the highest anaerobic LAS removal of 57%; so, this concentration was chosen to run the MFC. After the sustained anodic biofilm was formed, LAS degradation rate during 4 days in MFC was roughly 76% higher than that in the serum bottle, which indicated the role of the bioelectrochemical process in improving anaerobic LAS removal. Additionally, through 16S rRNA gene sequencing, the dominant bacterial species in the biofilm was identified as Pseudomonas zhaodongensis NEAU-ST5-21(T) with about 98.9% phylogenetic similarity and then a pathway was proposed for LAS anaerobic biodegradation. The MFC characteristics were assessed by pH monitoring as well as scanning electron microscopy and current density evolution.

Graphic abstract

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Availability of data and material

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

Code availability

Not applicable.

References

  1. Asok AK, Jisha M (2012) Biodegradation of the anionic surfactant linear alkylbenzene sulfonate (LAS) by autochthonous Pseudomonas sp. Water Air Soil Pollut 223:5039–5048

    Article  CAS  Google Scholar 

  2. Kertesz MA, Kölbener P, Stockinger H, Beil S, Cook AM (1994) Desulfonation of linear alkylbenzenesulfonate surfactants and related compounds by bacteria. Appl Environ Microbiol 60:2296–2303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fitzgerald JW (1976) Sulfate ester formation and hydrolysis: a potentially important yet often ignored aspect of the sulfur cycle of aerobic soils. Bacteriol Rev 40:698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Yang K, Zhao Y, Ji M, Li Z, Zhai S, Zhou X, Wang Q, Wang C, Liang B (2021) Challenges and opportunities for the biodegradation of chlorophenols: aerobic, anaerobic and bioelectrochemical processes. Water Res 193:116862

    Article  CAS  PubMed  Google Scholar 

  5. Bailey JE, Ollis DF (2018) Biochemical engineering fundamentals. McGraw-Hill

    Google Scholar 

  6. Delforno T, Belgini DR, Hidalgo K, Centurion VB, Lacerda-Júnior G, Duarte IC, Varesche M, Oliveira V (2020) Anaerobic reactor applied to laundry wastewater treatment: unveiling the microbial community by gene and genome-centric approaches. Int Biodeterior Biodegrad 149:104916

    Article  CAS  Google Scholar 

  7. Granatto C, Macedo T, Gerosa L, Sakamoto I, Silva E, Varesche M (2019) Scale-up evaluation of anaerobic degradation of linear alkylbenzene sulfonate from sanitary sewage in expanded granular sludge bed reactor. Int Biodeterior Biodegrad 138:23–32

    Article  CAS  Google Scholar 

  8. Eslami H, Ehrampoush MH, Ghaneian MT, Mokhtari M, Ebrahimi A (2017) Effect of organic loading rates on biodegradation of linear alkyl benzene sulfonate, oil and grease in greywater by integrated fixed-film activated sludge (IFAS). J Environ Manag 193:312–317

    Article  CAS  Google Scholar 

  9. Peressutti SR, Olivera N, Babay P, Costagliola M, Alvarez H (2008) Degradation of linear alkylbenzene sulfonate by a bacterial consortium isolated from the aquatic environment of Argentina. J Appl Microbiol 105:476–484

    Article  CAS  PubMed  Google Scholar 

  10. Costa MF, de Oliveira AM, de Oliveira Junior EN (2020) Biodegradation of linear alkylbenzene sulfonate (LAS) by Penicillium chrysogenum. Bioresour Technol Rep 9:100363

    Article  Google Scholar 

  11. Yan G, Jiang J, Wu G, Yan X (1998) Disappearance of linear alkylbenzene sulfonate from different cultures with Anabaena sp. HB 1017. Bull Environ Contam Toxicol 60:329–334

    Article  CAS  PubMed  Google Scholar 

  12. Khleifat KM, Halasah RA, Tarawneh KA, Halasah Z, Shawabkeh R, Wedyan MA (2010) Biodegradation of linear alkylbenzene sulfonate by Burkholderia sp.: effect of some growth conditions. Int J Agric Biol 12:17–25

    CAS  Google Scholar 

  13. Scott MJ, Jones MN (2000) The biodegradation of surfactants in the environment. Biochim Biophys Acta 1508:235–251

    Article  CAS  PubMed  Google Scholar 

  14. Zubay GL (1998) Biochemistry. Wm. C. Brown Publishers, Dubuque

    Google Scholar 

  15. Mungray AK, Kumar P (2009) Fate of linear alkylbenzene sulfonates in the environment: a review. Int Biodeterior Biodegrad 63:981–987

    Article  CAS  Google Scholar 

  16. Lara-Martín PA, Gómez-Parra A, Sanz JL, González-Mazo E (2010) Anaerobic degradation pathway of linear alkylbenzene sulfonates (LAS) in sulfate-reducing marine sediments. Environ Sci Technol 44:1670–1676

    Article  PubMed  CAS  Google Scholar 

  17. Sathe SM, Bhowmick GD, Dubey BK, Ghangrekar MM (2020) Surfactant removal from wastewater using photo-cathode microbial fuel cell and laterite-based hybrid treatment system. Bioprocess Biosyst Eng 43:2075–2084

    Article  CAS  PubMed  Google Scholar 

  18. Wenzel J, Fuentes L, Cabezas A, Etchebehere C (2017) Microbial fuel cell coupled to biohydrogen reactor: a feasible technology to increase energy yield from cheese whey. Bioprocess Biosyst Eng 40:807–819

    Article  CAS  PubMed  Google Scholar 

  19. Serra P, Espírito-Santo A (2021) Sourcing power with microbial fuel cells: a timeline. J Power Sources 482:228921

    Article  CAS  Google Scholar 

  20. Watanabe K (2008) Recent developments in microbial fuel cell technologies for sustainable bioenergy. J Biosci Bioeng 106:528–536

    Article  CAS  PubMed  Google Scholar 

  21. Baranitharan E, Khan MR, Prasad DMR, Teo WFA, Tan GYA, Jose R (2015) Effect of biofilm formation on the performance of microbial fuel cell for the treatment of palm oil mill effluent. Bioprocess Biosyst Eng 38:15–24

    Article  CAS  PubMed  Google Scholar 

  22. Di Lorenzo M, Curtis TP, Head IM, Scott K (2009) A single-chamber microbial fuel cell as a biosensor for wastewaters. Water Res 43:3145–3154

    Article  PubMed  CAS  Google Scholar 

  23. Mohanakrishna G, Abu-Reesh IM, Kondaveeti S, Al-Raoush RI, He Z (2018) Enhanced treatment of petroleum refinery wastewater by short-term applied voltage in single chamber microbial fuel cell. Bioresour Technol 253:16–21

    Article  CAS  PubMed  Google Scholar 

  24. Sciarria TP, Tenca A, D’Epifanio A, Mecheri B, Merlino G, Barbato M, Borin S, Licoccia S, Garavaglia V, Adani F (2013) Using olive mill wastewater to improve performance in producing electricity from domestic wastewater by using single-chamber microbial fuel cell. Bioresour Technol 147:246–253

    Article  CAS  PubMed  Google Scholar 

  25. Wen Q, Kong F, Zheng H, Cao D, Ren Y, Yin J (2011) Electricity generation from synthetic penicillin wastewater in an air-cathode single chamber microbial fuel cell. Chem Eng J 168:572–576

    Article  CAS  Google Scholar 

  26. Noori MT, Mukherjee C, Ghangrekar M (2017) Enhancing performance of microbial fuel cell by using graphene supported V2O5-nanorod catalytic cathode. Electrochim Acta 228:513–521

    Article  CAS  Google Scholar 

  27. Ortiz-Martínez V, Salar-García M, Touati K, Hernández-Fernández F, De los Ríos A, Belhoucine F, Berrabbah AA (2016) Assessment of spinel-type mixed valence Cu/Co and Ni/Co-based oxides for power production in single-chamber microbial fuel cells. Energy 113:1241–1249

    Article  CAS  Google Scholar 

  28. Mohamed HO, Obaid M, Sayed ET, Liu Y, Lee J, Park M, Barakat NAM, Kim HY (2017) Electricity generation from real industrial wastewater using a single-chamber air cathode microbial fuel cell with an activated carbon anode. Bioprocess Biosyst Eng 40:1151–1161

    Article  CAS  PubMed  Google Scholar 

  29. Cao Y, Hu Y, Sun J, Hou B (2010) Explore various co-substrates for simultaneous electricity generation and Congo red degradation in air-cathode single-chamber microbial fuel cell. Bioelectrochemistry 79:71–76

    Article  CAS  PubMed  Google Scholar 

  30. Wen Q, Kong F, Zheng H, Yin J, Cao D, Ren Y, Wang G (2011) Simultaneous processes of electricity generation and ceftriaxone sodium degradation in an air-cathode single chamber microbial fuel cell. J Power Sources 196:2567–2572

    Article  CAS  Google Scholar 

  31. Marassi RJ, Queiroz LG, Silva DCVR, dos Santos FS, Silva GC, de Paiva TCB (2020) Long-term performance and acute toxicity assessment of scaled-up air–cathode microbial fuel cell fed by dairy wastewater. Bioprocess Biosyst Eng 43:1561–1571

    Article  CAS  PubMed  Google Scholar 

  32. An B-M, Seo S-j, Hidayat S, Park J-Y (2020) Treatment of ethanolamine and electricity generation using a scaled-up single-chamber microbial fuel cell. J Ind Eng Chem 81:1–6

    Article  CAS  Google Scholar 

  33. Cheng S, Liu H, Logan BE (2006) Increased performance of single-chamber microbial fuel cells using an improved cathode structure. Electrochem Commun 8:489–494

    Article  CAS  Google Scholar 

  34. Logan BE (2008) Microbial fuel cells. John Wiley & Sons

    Google Scholar 

  35. Jurado E, Fernández-Serrano M, Nunez-Olea J, Luzon G, Lechuga M (2006) Simplified spectrophotometric method using methylene blue for determining anionic surfactants: applications to the study of primary biodegradation in aerobic screening tests. Chemosphere 65:278–285

    Article  CAS  PubMed  Google Scholar 

  36. APH Association, AWW Association, WPC Federation, WE Federation (1912) Standard methods for the examination of water and wastewater. American Public Health Association

    Google Scholar 

  37. Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  38. Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Madden T (2013) The BLAST sequence analysis tool. The NCBI handbook [internet], 2nd edn. National Center for Biotechnology Information, USA

    Google Scholar 

  40. Zhang L, Pan Y, Wang K, Zhang X, Zhang C, Zhang S, Fu X, Jiang J (2015) Pseudomonas zhaodongensis sp. nov., isolated from saline and alkaline soils. Int J Syst Evol Microbiol 65:1022–1030

    Article  CAS  PubMed  Google Scholar 

  41. Massaoudi Y, Anissi J, Lefter R, Lobiuc A, Sendide K, Ciobica A, Hassouni ME (2020) Protective effects of two halophilic crude extracts from Pseudomonas zhaodongensis and Bacillus stratosphericus against memory deficits and anxiety-and depression-like behaviors in methionine-induced schizophrenia in mice focusing on oxidative stress status. Evid Based Complement Altern Med 2020:8852418

  42. Abdel-Mageed WM, Lehri B, Jarmusch SA, Miranda K, Al-Wahaibi LH, Stewart HA, Jamieson AJ, Jaspars M, Karlyshev AV (2020) Whole genome sequencing of four bacterial strains from South Shetland Trench revealing biosynthetic and environmental adaptation gene clusters. Mar Genom 54:100782

    Article  Google Scholar 

  43. Qiao Y-J, Qiao Y, Zou L, Wu X-S, Liu J-H (2017) Biofilm promoted current generation of Pseudomonas aeruginosa microbial fuel cell via improving the interfacial redox reaction of phenazines. Bioelectrochemistry 117:34–39

    Article  CAS  PubMed  Google Scholar 

  44. Ilamathi R, Sheela AM, Gandhi NN (2019) Comparative evaluation of Pseudomonas species in single chamber microbial fuel cell with manganese coated cathode for reactive azo dye removal. Int Biodeterior Biodegrad 144:104744

    Article  CAS  Google Scholar 

  45. Thulasinathan B, Nainamohamed S, Samuel JOE, Soorangkattan S, Muthuramalingam J, Kulanthaisamy M, Balasubramani R, Nguyen DD, Chang SW, Bolan N (2019) Comparative study on Cronobacter sakazakii and Pseudomonas otitidis isolated from septic tank wastewater in microbial fuel cell for bioelectricity generation. Fuel 248:47–55

    Article  CAS  Google Scholar 

  46. Juliano M, Yanuaria C, Caparanga A, Tayo L (2020) Low level electricity production and COD removal in wastewater using a dual chamber microbial fuel cell with pseudomonas fluorescens as biocatalyst. In: IOP conference series: earth and environmental science, IOP Publishing, p 012011

  47. Duarte I, Oliveira L, Mayor M, Okada D, Varesche M (2010) Degradation of detergent (linear alkylbenzene sulfonate) in an anaerobic stirred sequencing-batch reactor containing granular biomass. Int Biodeterior Biodegrad 64:129–134

    Article  CAS  Google Scholar 

  48. Delforno T, Moura A, Okada D, Sakamoto I, Varesche M (2015) Microbial diversity and the implications of sulfide levels in an anaerobic reactor used to remove an anionic surfactant from laundry wastewater. Bioresour Technol 192:37–45

    Article  CAS  PubMed  Google Scholar 

  49. Velázquez-Martí B, Meneses-Quelal OW, Gaibor-Chavez J, Niño-Ruiz Z (2018) Review of mathematical models for the anaerobic digestion process. Anaerobic digestion. IntechOpen

    Google Scholar 

  50. Zhang H, Li M, Li J, Wang G, Liu Y (2017) Purification and properties of a novel quizalofop-p-ethyl-hydrolyzing esterase involved in quizalofop-p-ethyl degradation by Pseudomonas sp. J-2. Microb Cell Fact 16:1–10

    Article  CAS  Google Scholar 

  51. Askari A, Vahabzadeh F, Mardanpour MM (2021) Quantitative determination of linear alkylbenzene sulfonate (LAS) concentration and simultaneous power generation in a microbial fuel cell-based biosensor. J Clean Prod 294:126349

    Article  CAS  Google Scholar 

  52. Luo H, Liu G, Zhang R, Jin S (2009) Phenol degradation in microbial fuel cells. Chem Eng J 147:259–264

    Article  CAS  Google Scholar 

  53. Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485

    Article  CAS  PubMed  Google Scholar 

  54. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Park HS, Kim BH, Kim HS, Kim HJ, Kim GT, Kim M, Chang IS, Park YK, Chang HI (2001) A novel electrochemically active and Fe (III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe 7:297–306

    Article  CAS  Google Scholar 

  56. Chaudhuri SK, Lovley DR (2003) Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat Biotechnol 21:1229–1232

    Article  CAS  PubMed  Google Scholar 

  57. Liu H, Logan BE (2004) Electricity generation using an air-cathode single chamber microbial fuel cell in the presence and absence of a proton exchange membrane. Environ Sci Technol 38:4040–4046

    Article  CAS  PubMed  Google Scholar 

  58. Gil G-C, Chang I-S, Kim BH, Kim M, Jang J-K, Park HS, Kim HJ (2003) Operational parameters affecting the performance of a mediator-less microbial fuel cell. Biosens Bioelectron 18:327–334

    Article  CAS  PubMed  Google Scholar 

  59. Naraghi ZG, Yaghmaei S, Mardanpour MM, Hasany M (2015) Produced water treatment with simultaneous bioenergy production using novel bioelectrochemical systems. Electrochim Acta 180:535–544

    Article  CAS  Google Scholar 

  60. Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381

    Article  CAS  PubMed  Google Scholar 

  61. Choi S, Chae J (2013) Optimal biofilm formation and power generation in a micro-sized microbial fuel cell (MFC). Sens Actuators A 195:206–212

    Article  CAS  Google Scholar 

  62. Jiang D, Li B, Jia W, Lei Y (2010) Effect of inoculum types on bacterial adhesion and power production in microbial fuel cells. Appl Biochem Biotechnol 160:182–196

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

No funds, grants, or other support was received.

Author information

Authors and Affiliations

Authors

Contributions

The corresponding author is responsible for ensuring that the descriptions are accurate and agreed by all authors. The roles of all authors are listed, using the relevant above categories as follow (it should be noted that authors have contributed in multiple roles): AA: formal analysis, investigation, and writing—original draft; FV: supervision, conceptualization, and writing—review and editing; MMM: supervision, conceptualization, and writing—review and editing.

Corresponding author

Correspondence to Farzaneh Vahabzadeh.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors. The authors have complied with Springer’s ethical requirements. The article has not been published previously (except in the form of an abstract or as part of a published lecture or academic thesis), and it is not under consideration for publication elsewhere. The publication is approved by all authors and tacitly or explicitly by the responsible authorities where the work was carried out. If the manuscript accepted, it will not be published elsewhere in the same form, in English or in any other language, without the written consent of the Publisher.

Additional information

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 30 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Askari, A., Vahabzadeh, F. & Mardanpour, M.M. The identification and performance assessment of dominant bacterial species during linear alkylbenzene sulfonate (LAS)-biodegradation in a bioelectrochemical system. Bioprocess Biosyst Eng 44, 2579–2590 (2021). https://doi.org/10.1007/s00449-021-02629-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-021-02629-0

Keywords

Navigation