Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of the production of alginate-like exopolysaccharides (ALE) and tryptophan in aerobic granular sludge systems

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

Abstract

The engineering and microbiological aspects involved in the production of alginate-like exopolysaccharides (ALE) and tryptophan (TRY) in aerobic granular sludge systems were evaluated. The inclusion of short anoxic phase (A/O/A cycle–anaerobic, oxic, and anoxic phase) and the control of sludge retention time (SRT ≈ 10 days) proved to be an important strategy to increase the content of these bioproducts in granules. The substrate concentration also has a relevant impact on the production of ALE and TRY. The results of the microbiological analysis showed that slow-growing heterotrophic microbial groups (i.e., PAOs and GAOs) might be associated with the production of ALE, and the EPS-producing fermentative bacteria might be associated with the TRY production. The preliminary economic evaluation indicated the potential of ALE recovery in AGS systems in decreasing the OPEX (operational expenditure) of the treatment, especially for larger sewage treatment plants or industrial wastewaters with a high organic load.

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

Similar content being viewed by others

References

  1. de Bruin LMM, de Kreuk MK, van der Roest HFR, Uijterlinde C, van Loosdrecht MCM (2004) Aerobic granular sludge technology: an alternative to activated sludge? Water Sci Technol. https://doi.org/10.2166/wst.2004.0790

    Article  PubMed  Google Scholar 

  2. Rollemberg SLS, Barros ARM, Firmino PIM, dos Santos AB (2018) Aerobic granular sludge: cultivation parameters and removal mechanisms. Bioresour Technol. https://doi.org/10.1016/j.biortech.2018.08.130

    Article  Google Scholar 

  3. van Haandel AC, van der Lubbe JGM (2012) Handbook biological waste water treatment: design and optimization of activated sludge systems, 2nd edn. IWA Publishing, London

    Google Scholar 

  4. Rollemberg SLS, de Barros AN, Lira VNSA, Firmino PIM, dos Santos AB (2019) Comparison of the dynamics, biokinetics and microbial diversity between activated sludge flocs and aerobic granular sludge. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.122106

    Article  PubMed  Google Scholar 

  5. van Haandel AC, Lettinga G (1994) Anaerobic sewage treatment. John Wiley and Sons, London

    Google Scholar 

  6. Guo H, van Lier JB, de Kreuk M (2020) Digestibility of waste aerobic granular sludge from a full-scale municipal wastewater treatment system. Water Res. https://doi.org/10.1016/j.watres.2020.115617

    Article  PubMed  Google Scholar 

  7. Gobi K, Vadivelu VM (2015) Polyhydroxyalkanoate recovery and effect of in situ extracellular polymeric substances removal from aerobic granules. Bioresour Technol. https://doi.org/10.1016/j.biortech.2015.04.023

    Article  PubMed  Google Scholar 

  8. Vjayan T, Vadivelu VM (2017) Effect of famine-phase reduced aeration on polyhydroxyalkanoate accumulation in aerobic granules. Bioresour Technol. https://doi.org/10.1016/j.biortech.2017.09.038

    Article  PubMed  Google Scholar 

  9. Lin YM, Nierop KGJ, Girbal-Neuhauser E, Adriaanse M, van Loosdrecht MCM (2015) Sustainable polysaccharide-based biomaterial recovered from waste aerobic granular sludge as a surface coating material. Sustain Mater Technol. https://doi.org/10.1016/j.susmat.2015.06.002

    Article  Google Scholar 

  10. Pronk M, Neu TR, van Loosdrecht MCM, Lin YM (2017) The acid soluble extracellular polymeric substance of aerobic granular sludge dominated by Defluviicoccus sp. Water Res. https://doi.org/10.1016/j.watres.2017.05.068

    Article  PubMed  Google Scholar 

  11. Wang J, Ding L, Li K, Huang H, Hu H, Geng J, Xu K, Ren H (2018) Estimation of spatial distribution of quorum sensing signaling in sequencing batch biofilm reactor (SBBR) biofilms. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2017.07.277

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lin YM, Sharma PK, van Loosdrecht MCM (2013) The chemical and mechanical differences between alginate-like exopolysaccharides isolated from aerobic flocculent sludge and aerobic granular sludge. Water Res. https://doi.org/10.1016/j.watres.2012.09.017

    Article  PubMed  Google Scholar 

  13. Zhang Z, Yu Z, Dong J, Wang Z, Ma K, Xu X, Alvarezc JJ, Zhu L (2018) Stability of aerobic granular sludge under condition of low influent C/N ratio: correlation of sludge property and functional microorganism. Bioresour Technol. https://doi.org/10.1016/j.biortech.2018.09.045

    Article  PubMed  PubMed Central  Google Scholar 

  14. Felz S, Vermeulen P, van Loosdrecht MCM, Lin YM (2019) Chemical characterization methods for the analysis of structural extracellular polymeric substances (EPS). Water Res. https://doi.org/10.1016/j.watres.2019.03.068

    Article  PubMed  Google Scholar 

  15. Borazjani NJ, Tabarsa M, You SG, Rezaei M (2017) Effects of extraction methods on molecular characteristics, antioxidant properties and immunomodulation of alginates from Sargassum angustifolium. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2017.03.128

    Article  PubMed  Google Scholar 

  16. Meng F, Liu D, Pan Y, Xi L, Yang D, Huang W (2019) Enhanced amount and quality of alginate-like exopolysaccharides in aerobic granular sludge for the treatment of salty wastewater. BioRes 14(1):139–165

    CAS  Google Scholar 

  17. Seviour T, Pijuan M, Nicholson T, Keller J, Yuan Z (2009) Gel-forming exopolysaccharides explain basic differences between structures of aerobic sludge granules and floccular sludges. Water Res. https://doi.org/10.1016/j.watres.2009.07.018

    Article  PubMed  Google Scholar 

  18. RoyalHaskoning DHV (2020) Kaumera Nereda® Gum: a new innovation in resource recovery. https://www.royalhaskoningdhv.com/en-gb/specials/kaumera. Accessed 13 May 2020.

  19. Liu Y, Yang SF, Tay JH, Liu QS, Qin L, Li Y (2004) Cell hydrophobicity is a triggering force of biogranulation. Enzym Microb Technol. https://doi.org/10.1016/j.enzmictec.2003.12.009

    Article  Google Scholar 

  20. Mustafa A, Imran M, Ashraf M, Mahmood K (2018) Perspectives of using L-tryptophan for improving productivity of agricultural crops: a review. Pedosphere. https://doi.org/10.1016/S1002-0160(18)60002-5

    Article  Google Scholar 

  21. Lin YM, de Kreuk M, van Loosdrecht MCM, Adin A (2010) Characterization of alginate-like exopolysaccharides isolated from aerobic granular sludge in pilot-plant. Water Res. https://doi.org/10.1016/j.watres.2010.03.019

    Article  PubMed  Google Scholar 

  22. Schambeck CM, Magnus BS, de Souza LCR, Leite WRM, Derlon N, Guimarães LB, da Costa RHR (2020) Biopolymers recovery: dynamics and characterization of alginate-like exopolymers in an aerobic granular sludge system treating municipal wastewater without sludge inoculum. J Environ Manag. https://doi.org/10.1016/j.jenvman.2020.110394

    Article  Google Scholar 

  23. Rollemberg SLS, Barros ARM, de Lima JPM, Santos AF, Firmino PIM, dos Santos AB (2019) Influence of sequencing batch reactor configuration on aerobic granules growth: engineering and microbiological aspects. J Clean Prod. https://doi.org/10.1016/j.jclepro.2019.117906

    Article  Google Scholar 

  24. Rollemberg SLS, de Oliveira LQ, de Barros AN, Firmino PIM, dos Santos AB (2020) Pilot-scale aerobic granular sludge in the treatment of municipal wastewater: optimizations in the start-up, methodology of sludge discharge, and evaluation of resource recovery. Bioresour Technol. https://doi.org/10.1016/j.biortech.2020.123467

    Article  Google Scholar 

  25. Rollemberg SLS, de Oliveira LQ, Barros ARM, Melo VMM, Firmino PIM, dos Santos AB (2019) Effects of carbon source on the formation, stability, bioactivity and biodiversity of the aerobic granule sludge. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.01.071

    Article  PubMed  Google Scholar 

  26. APHA (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington

    Google Scholar 

  27. Rollemberg SLS, Ferreira TJT, Firmino PIM, dos Santos AB (2020) Impact of cycle type on aerobic granular sludge formation, stability, removal mechanisms and system performance. J Environ Manag 256:109970. https://doi.org/10.1016/j.jenvman.2019.109970

    Article  CAS  Google Scholar 

  28. Yang YC, Liu X, Wan C, Sun S, Lee DJ (2014) Accelerated aerobic granulation using alternating feed loadings: alginate-like exopolysaccharides. Bioresour Technol. https://doi.org/10.1016/j.biortech.2014.08.092

    Article  PubMed  Google Scholar 

  29. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem. https://doi.org/10.1021/ac60111a017

    Article  Google Scholar 

  30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275

    Article  CAS  Google Scholar 

  31. Felz S, Al-Zuhairy S, Aarstad OA, van Loosdrecht MCM, Lin YM (2016) Extraction of structural extracellular polymeric substances from aerobic granular sludge. J Vis Exp. https://doi.org/10.3791/54534

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wang BB, Chang Q, Peng DC, Hou YP, Li HJ, Pei LY (2014) A new classification paradigm of extracellular polymeric substances (EPS) in activated sludge: separation and characterization of exopolymers between floc level and microcolony level. Water Res. https://doi.org/10.1016/j.watres.2014.07.003

    Article  PubMed  Google Scholar 

  33. Peltre C, Gregorich EG, Bruun S, Jensen LS, Magid J (2017) Repeated application of organic waste affects soil organic matter composition: Evidence from thermal analysis, FTIR-PAS, amino sugars and lignin biomarkers. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2016.10.016

    Article  Google Scholar 

  34. Pishgar R, Dominic JA, Sheng Z, Tay JH (2019) Influence of operation mode and wastewater strength on aerobic granulation at pilot scale: start-up period, granular sludge characteristics, and effluent quality. Water Res. https://doi.org/10.1016/j.watres.2019.05.026

    Article  PubMed  Google Scholar 

  35. He Q, Chen L, Zhang S, Wang L, Liang J, Xia W, Zhou J (2018) Simultaneous nitrification, denitrification and phosphorus removal in aerobic granular sequencing batch reactors with high aeration intensity: Impact of aeration time. Bioresour Technol. https://doi.org/10.1016/j.biortech.2018.05.007

    Article  PubMed  Google Scholar 

  36. Franca RDG, Pinheiro HM, van Loosdrecht MCM, Lourenço ND (2018) Stability of aerobic granules during long-term bioreactor operation. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2017.11.005

    Article  PubMed  Google Scholar 

  37. Bassin JP, Winkler MKH, Kleerebezem R, Dezotti M, van Loosdrecht MCM (2012) Improved phosphate removal by selective sludge discharge in aerobic granular sludge reactors. Biotechnol Bioeng. https://doi.org/10.1002/bit.24457

    Article  PubMed  Google Scholar 

  38. Wu L, Peng C, Peng Y, Li L, Wang S, Ma Y (2012) Effect of wastewater COD/N ratio on aerobic nitrifying sludge granulation and microbial population shift. J Environ Sci. https://doi.org/10.1016/S1001-0742(11)60719-5

    Article  Google Scholar 

  39. Ali M, Wang Z, Salam KW, Hari AR, Pronk M, van Loosdrecht MCM, Saikaly PE (2019) Importance of species sorting and immigration on the bacterial assembly of different-sized aggregates in a full-scale aerobic granular sludge plant. Environ Sci Technol. https://doi.org/10.1021/acs.est.8b07303

    Article  PubMed  PubMed Central  Google Scholar 

  40. Metcalf L, Eddy HP (2003) Wastewater engineering: treatment and reuse, 4th edn. McGraw-Hill, Boston

    Google Scholar 

  41. Guimarães LB (2017) Microbiological characterization of granular sludge for nutrient removal and potential of exopolymer recovery from effluents in sequencing batch reactors (Doctoral dissertation) Universidade Federal de Santa Catarina, Florianópolis. https://repositorio.ufsc.br/xmlui/handle/123456789/178973. Accessed 10 May 2020.

  42. Luo J, Hao T, Wei L, Mackey HR, Lin Z, Chen GH (2014) Impact of influent COD/N ratio on disintegration of aerobic granular sludge. Water Res. https://doi.org/10.1016/j.watres.2014.05.037

    Article  PubMed  Google Scholar 

  43. Yang SF, Tay JH, Liu Y (2005) Effect of substrate nitrogen/chemical oxygen demand ratio on the formation of aerobic granules. J Environ Eng. https://doi.org/10.1061/(ASCE)0733-9372(2005)131:1(86)

    Article  Google Scholar 

  44. Nancharaiah YV, Reddy GKK (2018) Aerobic granular sludge technology: Mechanisms of granulation and biotechnological applications. Bioresour Technol. https://doi.org/10.1016/j.biortech.2017.09.131

    Article  PubMed  Google Scholar 

  45. Kocaturk I, Erguder TH (2016) Influent COD/TAN ratio affects the carbon and nitrogen removal efficiency and stability of aerobic granules. Ecol Eng. https://doi.org/10.1016/j.ecoleng.2016.01.077

    Article  Google Scholar 

  46. Willems A (2014) In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes: alphaproteobacteria and Betaproteobacteria. Springer, Berlin

    Google Scholar 

  47. Wang X, Wang S, Xue T, Li B, Dai X, Peng Y (2015) Treating low carbon/nitrogen (C/N) wastewater in simultaneous nitrification-endogenous denitrification and phosphorous removal (SNDPR) systems by strengthening anaerobic intracellular carbon storage. Water Res. https://doi.org/10.1016/j.watres.2015.03.019

    Article  PubMed  PubMed Central  Google Scholar 

  48. Xia J, Ye L, Ren H, Zhang X (2018) Microbial community structure and function in aerobic granular sludge. Appl Microbiol Biot. https://doi.org/10.1007/s00253-018-8905-9

    Article  Google Scholar 

  49. Roager HM, Licht TR (2018) Microbial tryptophan catabolites in health and disease. Nat Commun. https://doi.org/10.1038/s41467-018-05470-4

    Article  PubMed  PubMed Central  Google Scholar 

  50. Stokholm-Bjerregaard M, McIlroy SJ, Nierychlo M, Karst SM, Albertsen M, Nielsen PH (2017) A critical assessment of the microorganisms proposed to be important to enhanced biological phosphorus removal in full-scale wastewater treatment systems. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00718

    Article  PubMed  PubMed Central  Google Scholar 

  51. Murujew O, Whitton R, Kube M, Fan L, Roddick F, Jefferson B, Pidou M (2019) Recovery and reuse of alginate in an immobilized algae reactor. Environ Technol. https://doi.org/10.1080/09593330.2019.1673827

    Article  PubMed  Google Scholar 

  52. Meng F, Huang W, Liu D, Zhao Y, Huang W, Lei Z, Zhang Z (2020) Application of aerobic granules-continuous flow reactor for saline wastewater treatment: Granular stability, lipid production and symbiotic relationship between bacteria and algae. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.122291

    Article  PubMed  Google Scholar 

  53. von Sperling M (2007) Basic principles of wastewater treatment. IWA Publishing, London

    Google Scholar 

  54. Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol. https://doi.org/10.1007/s10811-010-9529-3

    Article  Google Scholar 

  55. van Leeuwen K, de Vries E, Koop S, Roest K (2018) The energy & raw materials factory: Role and potential contribution to the circular economy of the Netherlands. Environ Manag. https://doi.org/10.1007/s00267-018-0995-8

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the support obtained from the following Brazilian institutions: CNPq, Capes, Fapemig, INCT Sustainable Sewage Treatment Plants, and Central Analítica and CeGenBio of UFC.

Author information

Authors and Affiliations

  1. Department of Hydraulic and Environmental Engineering, Federal University of Ceará, Campus do Pici, Bloco 713. Pici., Fortaleza, CE, 60455-900, Brazil

    Silvio Luiz de Sousa Rollemberg, Amanda Ferreira dos Santos, Tasso Jorge Tavares Ferreira, Paulo Igor Milen Firmino & André Bezerra dos Santos

Authors
  1. Silvio Luiz de Sousa Rollemberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda Ferreira dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tasso Jorge Tavares Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paulo Igor Milen Firmino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. André Bezerra dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to André Bezerra dos Santos.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 5600 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rollemberg, S.L.d.S., dos Santos, A.F., Ferreira, T.J.T. et al. Evaluation of the production of alginate-like exopolysaccharides (ALE) and tryptophan in aerobic granular sludge systems. Bioprocess Biosyst Eng 44, 259–270 (2021). https://doi.org/10.1007/s00449-020-02439-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-020-02439-w

Keywords

Search

Navigation