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The viscosity behaviors of bacterial suspensions or extracellular polymeric substances and their effects on aerobic granular sludge

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Abstract

Although the viscosity behavior of bacteria and extracellular polymeric substances (EPS) in flocculent activated sludge (FAS) and aerobic granular sludge (AGS) has been investigated, no studies have explored the role of viscosity in microbial attachment in pure culture. This study investigated the viscosity behavior of bacteria and EPS. The results showed that bacteria and their EPS exhibited non-Newtonian fluid and shear-thinning behavior. The viscosity of bacteria and EPS was 1.55–3.80 cP and 1.10–2.40 cP, respectively, while the attachment of bacteria (optical density at 600 nm) was 0.1426–3.1015. Bacteria with high attachment secreted EPS with a higher viscosity (2.40 cP), whereas those with weak attachment expressed EPS with a lower viscosity (1.10 cP). Viscosity and microbial attachment or extracellular polysaccharide (PS) content were significantly positively correlated. PS content was the source of bacterial viscosity, and β-polysaccharide played a more important role in viscosity and microbial attachment than α-polysaccharide. Thus, viscosity plays a critical role in microbial attachment, and high viscosity and PS content result in high microbial attachment, which is beneficial to the granulation process of AGS.

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References

  • Adav SS, Lee DJ, Show KY, Tay JH (2008a) Aerobic granular sludge: recent advances. Biotechnol Adv 26:411–423

    Article  CAS  Google Scholar 

  • Adav SS, Lee DJ, Tay JH (2008b) Extracellular polymeric substances and structural stability of aerobic granule. Water Res 42:1644–1650

    Article  CAS  Google Scholar 

  • Alves D, Sileika T, Messersmith PB, Pereira MO (2016) Polydopamine-mediated iImmobilization of alginate lyase to prevent P. aeruginosa adhesion. Macromol Biosci 16:1301–1310

    Article  CAS  Google Scholar 

  • Araujo D, Alves VD, Campos J, Coelhoso I, Sevrin C, Grandfils C, Freitas F, Reis MA (2016) Assessment of the adhesive properties of the bacterial polysaccharide FucoPol. Int J Biol Macromol 92:383–389

    Article  CAS  Google Scholar 

  • Berk V, Fong JC, Dempsey GT, Develioglu ON, Zhuang X, Liphardt J, Yildiz FH, Chu S (2012) Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337:236–269

    Article  CAS  Google Scholar 

  • Burkus Z (2003) Determination of the molecular weight of barley β-glucan using intrinsic viscosity measurements. Carbohydr Polym 54:51–57

    Article  CAS  Google Scholar 

  • Caudan C, Filali A, Sperandio M, Girbal-Neuhauser E (2014) Multiple EPS interactions involved in the cohesion and structure of aerobic granules. Chemosphere 117:262–270

    Article  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nature reviews. Microbiology 8:623–633

  • Formosa-Dague C, Feuillie C, Beaussart A, Derclaye S, Kucharikova S, Lasa I, Van Dijck P, Dufrene YF (2016) Sticky matrix: adhesion mechanism of the Staphylococcal polysaccharide intercellular adhesin. ACS Nano 10:3443–3452

    Article  CAS  Google Scholar 

  • Gaurivaud P, Baranowski E, Pau-Roblot C, Sagne E, Citti C, Tardy F (2016) Mycoplasma agalactiae secretion of beta-(1➔6)-glucan, a rare polysaccharide in prokaryotes, is governed by high-frequency phase variation. Appl Environ Microbiol 82:3370–3383

    Article  CAS  Google Scholar 

  • Gutsche J, Remminghorst U, Rehm B (2006) Biochemical analysis of alginate biosynthesis protein AlgX from Pseudomonas aeruginosa: purification of an AlgX-MucD (AlgY) protein complex. Biochimie 88:245–251

    Article  CAS  Google Scholar 

  • Harimawan A & Ting YP. (2016) Investigation of extracellular polymeric substances (EPS) properties of P. aeruginosa and B. subtilis and their role in bacterial adhesion. Colloids Surf B Biointerfaces 146:459–467

  • Hao W, Li Y, Lv J, Chen L, Zhu J (2016) The biological effect of metal ions on the granulation of aerobic granular activated sludge. Journal of environmental sciences 44:252–259

  • Hong E, Yeneneh AM, Sen TK, Ang HM, Kayaalp A (2017) The relationship between physico-chemical and rheological characteristics of digested sludge, biosolid, centrate and the effects on dewatering performance (a case study). J Water Process Eng 19:193–204

    Article  Google Scholar 

  • Jiang HL, Tay JH, Maszenan AM, Tay ST (2006) Enhanced phenol biodegradation and aerobic granulation by two coaggregating bacterial strains. Environ Sci Technol 40:6137–6142

    Article  CAS  Google Scholar 

  • Jiao B, Shi A, Liu H, Sheng X, Liu L, Hu H, Adhikari B, Wang Q. (2018) Effect of electrostatically charged and neutral polysaccharides on the rheological characteristics of peanut protein isolate after high-pressure homogenization. Food Hydrocolloids 77:329–335

  • Kolodkin-Gal I, Cao S, Chai L, Bottcher T, Kolter R, Clardy J, Losick R (2012) A self-produced trigger for biofilm disassembly that targets exopolysaccharide. Cell 149:684–692

    Article  CAS  Google Scholar 

  • Li AJ, Hou BL, Li MX (2015) Cell adhesion, ammonia removal and granulation of autotrophic nitrifying sludge facilitated by N-acyl-homoserine lactones. Bioresour Technol 196:550–558

    Article  CAS  Google Scholar 

  • Li N, Wei D, Wang S, Hu L, Xu W, Du B, Wei Q (2017) Comparative study of the role of extracellular polymeric substances in biosorption of Ni(II) onto aerobic/anaerobic granular sludge. J Colloid Interface Sci 490:754–761

    Article  CAS  Google Scholar 

  • Liao CT, Du SC, Lo HH, Hsiao YM (2014) The galU gene of Xanthomonas campestris pv. campestris is involved in bacterial attachment, cell motility, polysaccharide synthesis, virulence, and tolerance to various stresses. Arch Microbiol 196:729–738

    Article  CAS  Google Scholar 

  • Limoli DH, Jones CJ, Wozniak DJ (2015) Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr 3:1–30

    Article  Google Scholar 

  • Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014a) The microbial attachment potential and quorum sensing measurement of aerobic granular activated sludge and flocculent activated sludge. Bioresour Technol 151:291–296

    Article  CAS  Google Scholar 

  • Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014b) The effect of quorum sensing and extracellular proteins on the microbial attachment of aerobic granular activated sludge. Bioresour Technol 152:53–58

    Article  CAS  Google Scholar 

  • Ma YJ, Xia CW, Yang HY, Zeng RJ (2014) A rheological approach to analyze aerobic granular sludge. Water Res 50:171–178

    Article  CAS  Google Scholar 

  • Markis F, Baudez J-C, Parthasarathy R, Slatter P, Eshtiaghi N (2016) The apparent viscosity and yield stress of mixtures of primary and secondary sludge: impact of volume fraction of secondary sludge and total solids concentration. Chem Eng J 288:577–587

    Article  CAS  Google Scholar 

  • Mohapatra DP, Brar SK, Tyagi RD, Picard P, Surampalli RY (2012) Ferro-sonication and partial ozonation pre-treatment and biotransformation of wastewater sludge for degradation of bisphenol a: rheology studies. Chem Eng Sci 81:20–27

    Article  CAS  Google Scholar 

  • Mori M, Seyssiecq I, Roche N (2006) Rheological measurements of sewage sludge for various solids concentrations and geometry. Process Biochem 41:1656–1662

    Article  CAS  Google Scholar 

  • Pevere A, Guibaud G, Goin E, van Hullebusch E, Lens P (2009) Effects of physico-chemical factors on the viscosity evolution of anaerobic granular sludge. Biochem Eng J 43:231–238

    Article  CAS  Google Scholar 

  • Rodriguez FA, Martinez-Toledo MV, Gonzalez-Lopez J, Hontoria E, Poyatos JM (2010) Performance of bench-scale membrane bioreactor under real work conditions using pure oxygen: viscosity and oxygen transfer analysis. Bioprocess Biosyst Eng 33:885–892

    Article  CAS  Google Scholar 

  • Rodríguez FA, Reboleiro-Rivas P, Osorio F, Martínez-Toledo MV, Hontoria E, Poyatos JM (2012) Influence of mixed liquid suspended solids and hydraulic retention time on oxygen transfer efficiency and viscosity in a submerged membrane bioreactor using pure oxygen to supply aerobic conditions. Biochem Eng J 60:135–141

    Article  Google Scholar 

  • Seviour T, Lynette KL, Maite P, Yuan Z (2010) Structural determination of a key exopolysaccharide in mixed culture aerobic sludge granules using NMR spectroscopy. Environ Sci Technol 44:8964–8970

    Article  CAS  Google Scholar 

  • Seviour T, Yuan Z, van Loosdrecht MC, Lin Y (2012) Aerobic sludge granulation: a tale of two polysaccharides? Water Res 46:4803–4813

    Article  CAS  Google Scholar 

  • Shene C, Canquil N, Bravo S, Rubilar M (2008) Production of the exopolysaccharides by Streptococcus thermophilus: effect of growth conditions on fermentation kinetics and intrinsic viscosity. Int J Food Microbiol 124:279–284

    Article  CAS  Google Scholar 

  • Sweity A, Ying W, Ali-Shtayeh MS, Yang F, Bick A, Oron G, Herzberg M (2011) Relation between EPS adherence, viscoelastic properties, and MBR operation: biofouling study with QCM-D. Water Res 45:6430–6440

    Article  CAS  Google Scholar 

  • Tahtat D, Boutrig HH, Khodja AN, Benamer S, Hammache Y, Mahlous M (2019) The synergistic effect of gamma irradiation and alkaline soaking at low temperature on the pre-deacetylation of alpha-chitin: optimization by design of experiment. Carbohydr Polym 215:39–46

    Article  CAS  Google Scholar 

  • Wan C, Lee DJ, Yang X, Wang Y, Wang X, Liu X (2015) Calcium precipitate induced aerobic granulation. Bioresour Technol 176:32–37

    Article  CAS  Google Scholar 

  • Wang H, Wilksch JJ, Chen L, Tan JW, Strugnell RA, Gee ML (2017) Influence of fimbriae on bacterial adhesion and viscoelasticity and vorrelations of the two properties with biofilm formation. Langmuir 33:100–106

    Article  CAS  Google Scholar 

  • Wei D, Li M, Wang X, Han F, Li L, Guo J, Ai L, Fang L, Liu L, Du B, Wei Q (2016) Extracellular polymeric substances for Zn (II) binding during its sorption process onto aerobic granular sludge. J Hazard Mater 301:407–415

    Article  CAS  Google Scholar 

  • Yang SF, Li XY, Yu HQ (2008) Formation and characterisation of fungal and bacterial granules under different feeding alkalinity and pH conditions. Process Biochem 43:8–14

    Article  Google Scholar 

  • Yuan D, Wang Y, Qian X (2017) Variations of internal structure and moisture distribution in activated sludge with stratified extracellular polymeric substances extraction. Int Biodeterior Biodegradation 116:1–9

    Article  CAS  Google Scholar 

  • Zhu L, Zhou J, Lv M, Yu H, Zhao H, Xu X (2015) Specific component comparison of extracellular polymeric substances (EPS) in flocs and granular sludge using EEM and SDS-PAGE. Chemosphere 121:26–32

    Article  CAS  Google Scholar 

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Funding

This research project was financed by the National Natural Science Foundation of China (No. 51578069) and Beijing Municipal Science and Technology Commission Project (Z171100000717012).

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Correspondence to Jianrong Zhu.

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Responsible editor: Gerald Thouand

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Highlights

• Bacterial suspensions and EPS are non-Newtonian fluids with shear-thinning behavior.

• Viscosity, particularly EPS viscosity, plays a more critical role in the microbial attachment.

• β-Polysaccharide plays a more important role in the viscosity and microbial attachment than α-polysaccharide.

• PS content is more influential than PN content in viscosity and microbial attachment.

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Yang, X., Xu, T., Cao, P. et al. The viscosity behaviors of bacterial suspensions or extracellular polymeric substances and their effects on aerobic granular sludge. Environ Sci Pollut Res 26, 30087–30097 (2019). https://doi.org/10.1007/s11356-019-06012-1

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  • DOI: https://doi.org/10.1007/s11356-019-06012-1

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