New insights into different surfactants’ impacts on sludge fermentation: Focusing on the particular metabolic processes and microbial genetic traits

Highlights

• The promoting effects for VFA generation follow the order of APG>SDBS>HTAB.

• Surfactants improve the WAS solubilization/hydrolysis and acidification processes.

• The VFA promotion is associated with surfactants’ distinctive characteristics.

• Surfactants induce the enrichment of functional bacteria for VFA biosynthesis.

• The vital genes for substrates delivery, metabolism, and VFA yields are upregulated.

Abstract

Surfactants were expected to exhibit positive effects on the waste activated sludge (WAS) disposal. However, the systematic comparison of different categories of surfactants on the WAS fermentation and the functional mechanisms, especially microbial metabolic traits, have not yet been precisely explored. This study revealed the positive effects of different surfactants on the volatile fatty acid (VFA) production, which followed the order of alkyl polysaccharides (APG)>sodium dodecylbenzene sulfonate (SDBS)>hexadecyl trimethyl ammonium bromide (HTAB). Mechanistic exploration found that the presence of different surfactants improved solubilization and hydrolysis steps, and then contributed to the subsequent acidification with different efficiencies. The functional microorganisms associated with VFA generation were enriched in surfactant-conditioned reactors. Metagenomic analysis further indicated that the key genes involved in the particular process of VFA generation were over-expressed. The simultaneous bioavailable substrate improvement, functional bacterial enrichment, and metabolic activity upregulation induced by different surfactants jointly contributed to VFA promotion during WAS fermentation. This study could provide a comprehensive realization of surfactants’ impacts on the WAS fermentation process, and more importantly, it reminded the public to discern the distinct interplaying effects induced by different chemicals in regulating the WAS disposal and resource recovery.

Graphical abstract

Keywords

Waste activated sludge (WAS) / Volatile fatty acids (VFA) / Surfactant types / Functional microorganisms / Metabolic activity upregulation

References

[1] Barai M, Manna E, Sultana H, Mandal M, Guchhait K, Manna T, Patra A, Chang C H, Moitra P, Ghosh C, Larsson A C, Bhattacharya S, Panda A (2021). Micro-structural investigations on oppositely charged mixed surfactant gels with potential dermal applications: Research Square, 11(1): 15527

[2] Bolger A M, Lohse M, Usadel B (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England), 30(15): 2114–2120

[3] Cantarel B L, Coutinho P M, Rancurel C, Bernard T, Lombard V, Henrissat B (2009). The carbohydrate-active enzymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Research, 37(Database): D233–D238

[4] Cao J, Zhu Q, Zhang T, Wu Y, Zhang Q, Fu B, Fang F, Feng Q, Luo J (2021). Distribution patterns of microbial community and functional characteristics in full-scale wastewater treatment plants: Focusing on the influent types. Chemosphere, 281: 130899

[5] Chen Y, Jiang X, Xiao K, Shen N, Zeng R J, Zhou Y (2017). Enhanced volatile fatty acids (VFAs) production in a thermophilic fermenter with stepwise pH increase- Investigation on dissolved organic matter transformation and microbial community shift. Water Research, 112: 261–268

[6] Cheng X, Wang S, Huang W, Wang F, Fang S, Ge R, Zhang Q, Zhang L, Du W, Fang F, Feng Q, Cao J, Luo J (2022). Current status of hypochlorite technology on the wastewater treatment and sludge disposal: Performance, principals and prospects. Science of the Total Environment, 803: 150085

[7] De Souza Dornelles H, Motteran F, Sakamoto I K, Silva E L, Varesche M B A (2020). 4-Nonylphenol degradation changes microbial community of scale-up Anaerobic Fluidized Bed Reactor. Journal of Environmental Management, 267: 110575

[8] Duan Y, Zhou A, Yue X, Zhang Z, Gao Y, Luo Y, Zhang X (2020). Acceleration of the particulate organic matter hydrolysis by start-up stage recovery and its original microbial mechanism. Frontiers of Environmental Science & Engineering, 15(1): 12

[9] Fait M E, Garrote G L, Clapés P, Tanco S, Lorenzo J, Morcelle S R (2015). Biocatalytic synthesis, antimicrobial properties and toxicity studies of arginine derivative surfactants. Amino Acids, 47(7): 1465–1477

[10] Fan Y J, Hsu Y C, Gu B C, Wu C C (2020). Voltammetric measurement of Escherichia coli concentration through p-APG hydrolysis by endogenous β-galactosidase. Microchemical Journal, 154: 104641

[11] Federation W E, Association A (2005). Standard methods for the examination of water and wastewater. Washington, DC, USA: American Public Health Association (APHA)

[12] Feng L, Chen J, Wang F, Chen Y, Luo J (2019). Acidogenic fermentation facilitates anaerobic biodegradation of polycyclic aromatic hydrocarbons in waste activated sludge. ACS Sustainable Chemistry & Engineering, 7(5): 5404–5411

[13] Hollenstein K, Dawson R J P, Locher K P (2007). Structure and mechanism of ABC transporter proteins. Current Opinion in Structural Biology, 17(4): 412–418

[14] Hyatt D, Chen G L, Locascio P F, Land M L, Larimer F W, Hauser L J (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11(1): 119

[15] Jin B, Wang S, Xing L, Li B, Peng Y (2016). Long term effect of alkali types on waste activated sludge hydrolytic acidification and microbial community at low temperature. Bioresource Technology, 200: 587–597

[16] Kotrba P, Inui M, Yukawa H (2001). Bacterial phosphotransferase system (PTS) in carbohydrate uptake and control of carbon metabolism. Journal of Bioscience and Bioengineering, 92(6): 502–517

[17] Lei Y, Wei L, Liu T, Xiao Y, Dang Y, Sun D, Holmes D E (2018). Magnetite enhances anaerobic digestion and methanogenesis of fresh leachate from a municipal solid waste incineration plant. Chemical Engineering Journal, 348: 992–999

[18] Lin X, Cai C, Lou H, Qiu X, Pang Y, Yang D (2017). Effect of cationic surfactant cetyltrimethylammonium bromide on the enzymatic hydrolysis of cellulose. Biochimica et Biophysica Acta, 24(1): 61–68

[19] Luo J, Feng L, Chen Y, Sun H, Shen Q, Li X, Chen H (2015). Alkyl polyglucose enhancing propionic acid enriched short-chain fatty acids production during anaerobic treatment of waste activated sludge and mechanisms. Water Research, 73: 332–341

[20] Luo J, Huang W, Zhang Q, Guo W, Wu Y, Feng Q, Fang F, Cao J, Su Y (2020a). Effects of different hypochlorite types on the waste activated sludge fermentation from the perspectives of volatile fatty acids production, microbial community and activity, and characteristics of fermented sludge. Bioresource Technology, 307: 123227

[21] Luo J, Huang W, Zhang Q, Wu Y, Fang F, Cao J, Su Y (2021a). Distinct effects of hypochlorite types on the reduction of antibiotic resistance genes during waste activated sludge fermentation: Insights of bacterial community, cellular activity, and genetic expression. Journal of Hazardous Materials, 403: 124010

[22] Luo J, Wang F, Cheng X, Huang W, Zhang Q, Fang F, Cao J, Wu Y (2021b). Metatranscriptomic insights of the metabolic process enhancement during food wastes fermentation driven by linear alkylbenzene sulphonates. Journal of Cleaner Production, 315: 128145

[23] Luo J, Wu L, Feng Q, Fang F, Cao J, Zhang Q, Su Y (2019a). Synergistic effects of iron and persulfate on the efficient production of volatile fatty acids from waste activated sludge: Understanding the roles of bioavailable substrates, microbial community & activities, and environmental factors. Biochemical Engineering Journal, 141: 71–79

[24] Luo J, Zhang Q, Wu L, Feng Q, Fang F, Xue Z, Li C, Cao J (2019b). Promoting the anaerobic production of short-chain fatty acids from food wastes driven by the reuse of linear alkylbenzene sulphonates-enriched laundry wastewater. Bioresource Technology, 282: 301–309

[25] Luo J H, Wu M, Yuan Z, Guo J (2017). Biological bromate reduction driven by methane in a membrane biofilm reactor. Environmental Science & Technology Letters, 4(12): 562–566

[26] Luo J Y, Huang W X, Guo W, Ge R, Zhang Q, Fang F, Feng Q, Cao J S, Wu Y (2020b). Novel strategy to stimulate the food wastes anaerobic fermentation performance by eggshell wastes conditioning and the underlying mechanisms. Chemical Engineering Journal, 398: 125560

[27] Ma H, Lin Y, Jin Y, Gao M, Li H, Wang Q, Ge S, Cai L, Huang Z, Van Le Q, Xia C (2021). Effect of ultrasonic pretreatment on chain elongation of saccharified residue from food waste by anaerobic fermentation. Environmental Pollution, 268(Part B): 115936

[28] Ma Y, Liu Y (2019). Turning food waste to energy and resources towards a great environmental and economic sustainability: An innovative integrated biological approach. Biotechnology Advances, 37(7): 107414

[29] Martin Vincent N, Wei Y, Zhang J, Yu D, Tong J (2018). Characterization and dynamic shift of microbial communities during start-up, overloading and steady-state in an anaerobic membrane bioreactor. International Journal of Environmental Research and Public Health, 15(7): 1399

[30] Nyström B, Kjøniksen A L, Beheshti N, Maleki A, Zhu K, Knudsen K D, Pamies R, Hernández Cifre J G, García de la Torre J (2010). Characterization of polyelectrolyte features in polysaccharide systems and mucin. Advances in Colloid and Interface Science, 158(1–2): 108–118

[31] Pan Y, Liu X, Zhang W, Liu Z, Zeng G, Shao B, Liang Q, He Q, Yuan X, Huang D, Chen M (2020). Advances in photocatalysis based on fullerene C₆₀ and its derivatives: Properties, mechanism, synthesis, and applications. Applied Catalysis B: Environmental, 265: 118579

[32] Pang H, He J, Ma Y, Pan X, Zheng Y, Yu H, Yan Z, Nan J (2021). Enhancing volatile fatty acids production from waste activated sludge by a novel cation-exchange resin assistant strategy. Journal of Cleaner Production, 278: 123236

[33] Peng Z, Liu X, Zhang W, Zeng Z, Liu Z, Zhang C, Liu Y, Shao B, Liang Q, Tang W, Yuan X (2020). Advances in the application, toxicity and degradation of carbon nanomaterials in environment: A review. Environment International, 134: 105298

[34] Ramprakash B, Muthukumar K (2018). Influence of sulfuric acid concentration on biohydrogen production from rice mill wastewater using pure and coculture of Enterobacter aerogenes and Citrobacter freundii. International Journal of Hydrogen Energy, 43(19): 9254–9258

[35] Regueira A, Lema J M, Carballa M, Mauricio-Iglesias M (2020). Metabolic modeling for predicting VFA production from protein-rich substrates by mixed-culture fermentation. Biotechnology and Bioengineering, 117(1): 73–84

[36] Romanowski M, Zhu X, Kim K, Hruby V J, O’brien D F (2002). Interaction of enkephalin peptides with anionic model membranes. Biochimica et Biophysica Acta (BBA) -. Biomembranes, 1558(1): 45–53

[37] Shapovalova A A, Khijniak T V, Tourova T P, Muyzer G, Sorokin D Y (2008). Heterotrophic denitrification at extremely high salt and pH by haloalkaliphilic Gammaproteobacteria from hypersaline soda lakes. Extremophiles, 12(5): 619–625

[38] Shi Y, Chen Z, Cao Y, Fan J, Clark J H, Luo G, Zhang S (2021). Migration and transformation mechanism of phosphorus in waste activated sludge during anaerobic fermentation and hydrothermal conversion. Journal of Hazardous Materials, 403: 123649

[39] Wang F, Luo J, Fang S, Huang W, Zhang Y, Zhang L, Cheng X, Du W, Fang F, Cao J, Wu Y (2022). Mechanisms of allicin exposure for the sludge fermentation enhancement: Focusing on the fermentation processes and microbial metabolic traits. Journal of Environmental Sciences, 115: 253–264

[40] Wang L, Yang C, Thangavel S, Guo Z, Chen C, Wang A, Liu W (2020). Enhanced hydrogen production in microbial electrolysis through strategies of carbon recovery from alkaline/thermal treated sludge. Frontiers of Environmental Science & Engineering, 15(4): 56

[41] Wood D E, Salzberg S L (2014). Kraken: Ultrafast metagenomic sequence classification using exact alignment. Genome Biology, 15(3): R46

[42] Wu L, Yang Y, Guo W, Huang W, Peng Z, Zhang Z, Zou M, Luo J (2020). Deterioration of biological pollutants removal induced by linear alkylbenzene sulphonates in sequencing batch reactors: Insight of sludge characteristics, microbial community and metabolic activity. Bioresource Technology, 315: 123843

[43] Wu Y, Wu J, Shen Q, Zheng X, Chen Y (2021). Anaerobic fermentation metabolism of Moorella thermoacetica inhibited by copper nanoparticles: Comprehensive analyses of transcriptional response and enzyme activity. Water Research, 197: 117081

[44] Xu Q, Huang Q S, Wei W, Sun J, Dai X, Ni B J (2020). Improving the treatment of waste activated sludge using calcium peroxide. Water Research, 187: 116440

[45] Xu R Z, Fang S, Zhang L, Huang W, Shao Q, Fang F, Feng Q, Cao J, Luo J (2021). Distribution patterns of functional microbial community in anaerobic digesters under different operational circumstances: A review. Bioresource Technology, 341: 125823

[46] Yang C X, Zhao S, Guo Z C, Liu W Z, Wang L, Yu S P, Liu B L, Cong X (2020). Alkaline aided thermophiles pretreatment of waste activated sludge to increase short chain fatty acids production: Microbial community evolution by alkaline on hydrolysis and fermentation. Environmental Research, 186: 109503

[47] Ye T, Li X, Zhang T, Su Y, Zhang W, Li J, Gan Y, Zhang A, Liu Y, Xue G (2018). Copper(II) addition to accelerate lactic acid production from co-fermentation of food waste and waste activated sludge: Understanding of the corresponding metabolisms, microbial community and predictive functional profiling. Waste Management (New York, N.Y.), 76: 414–422

[48] Yin C, Li Y, Zhang T, Liu J, Yuan Y, Huang M (2020). Effects of exposure to anionic surfactants (SDBS and SDS) on nitrogen removal of aerobic denitrifier. Water Environment Research, 92(12): 2129–2139

[49] Yuan C, Wang B, Peng Y, Li X, Zhang Q (2021). Simultaneous enhanced biological phosphorus removal and semi-nitritation (EBPR-SN) followed by anammox process treating municipal wastewater at seasonal temperatures: From summer to winter. Science of the Total Environment, 757: 144048

[50] Zeppilli M, Chouchane H, Scardigno L, Mahjoubi M, Gacitua M, Askri R, Cherif A, Majone M (2020). Bioelectrochemical vs hydrogenophilic approach for CO₂ reduction into methane and acetate. Chemical Engineering Journal, 396: 125243

[51] Zhang Q, Cao J, Wu Y, Zhao J, Guo W, Huang W, Feng Q, Fang F, Aleem M, Luo J (2020). Shifts of microbial community and metabolic function during food wastes and waste activated sludge co-fermentation in semi-continuous-flow reactors: Effects of fermentation substrate and zero-valent iron. Bioresource Technology, 313: 123686

[52] Zhao J, Liu Y, Ni B, Wang Q, Wang D, Yang Q, Sun Y, Zeng G, Li X (2016). Combined effect of free nitrous acid pretreatment and sodium dodecylbenzene sulfonate on short-chain fatty acid production from waste activated sludge. Scientific Reports, 6(1): 21622

[53] Zhao Y, Fang Y, Jin Y, Huang J, Ma X, He K, He Z, Wang F, Zhao H (2015). Microbial community and removal of nitrogen via the addition of a carrier in a pilot-scale duckweed-based wastewater treatment system. Bioresource Technology, 179: 549–558

Acknowledgements

The work is financially supported by the National Natural Science Foundation of China (Grant No. 52070069), Fundamental Research Funds for the Central Universities (China) (No. B200202099), Jiangsu Province Natural Science Foundation (China) (BK20211207), Shanghai Post-doctoral Excellence Program (China) (No. 2020419), China Postdoctoral Science Foundation (No. 2021M692423) and the State Key Laboratory of Pollution Control and Resource Reuse Foundation (China) (No. PCRRF20005).

RIGHTS & PERMISSIONS

2022 Higher Education Press