Environmental Science and Pollution Research

, Volume 26, Issue 1, pp 514–527 | Cite as

Influence of salinity cycles in bioreactor performance and microbial community structure of membrane-based tidal-like variable salinity wastewater treatment systems

  • Alejandro Rodriguez-SanchezEmail author
  • Juan Carlos Leyva-Diaz
  • Barbara Muñoz-Palazon
  • Jose Manuel Poyatos
  • Jesus Gonzalez-Lopez
Research Article


A membrane bioreactor and two hybrid moving bed bioreactor-membrane bioreactors were operated for the treatment of variable salinity wastewater, changing in cycles of 6-h wastewater base salinity and 6-h maximum salinity (4.5 and 8.5 mS cm−1 electric conductivity, which relate to 2.4 and 4.8 g L−1 NaCl, respectively), under different hydraulic retention times (6, 9.5, and 12 h) and total solids concentrations (2500 and 3500 mg L−1). The evaluation of the performance of the systems showed that COD removal performance was unaffected by salinity conditions, while BOD5 and TN removals were significantly higher in the low-salinity scenario. The microbial community structure showed differences with respect to salinity conditions for Eukarya, suggesting their higher sensitivity for salinity with respect to Prokarya, which were similar at both salinity scenarios. Nevertheless, the intra-OTU distribution of consistently represented OTUs of Eukarya and Prokarya was affected by the different salinity maximums. Multivariate redundancy analyses showed that several genera such as Amphiplicatus (0.01–5.90%), Parvibaculum (0.27–1.19%), Thiothrix (0.30–1.19%), Rhodanobacter (2.81–5.85%), Blastocatella (0.21–2.01%), and Nitrobacter (0.80–0.99%) were positively correlated with BOD5 and TN removal, and the ecological roles of these were proposed. All these genera were substantially more represented under low-salinity conditions (10–500% higher relative abundance), demonstrating that they might be of importance for the treatment of variable salinity wastewater. Evaluation of Eukarya OTUs showed that many of them lack a consistent taxonomic classification, which highlights the lack of knowledge of the diversity and ecological role of Eukaryotes in saline wastewater treatment processes. The results obtained will be of interest for future design and operation of salinity wastewater treatment systems particularly because little is known on the effect of variable salinity conditions in wastewater treatment.


Membrane bioreactor Moving bed membrane bioreactor Salinity wastewater Eukarya Prokarya Oligotyping 


Funding information

The authors would like to acknowledge the support given by the Institute of Water Research and the Department of Civil Engineering in the University of Granada. Also, they would like to acknowledge the economic support given by the Ministry of Economy and Competitivity of the Government of Spain, which funded this project by the funding CTM2013-48154-P and grant BES-2014-067852.

Supplementary material

11356_2018_3608_MOESM1_ESM.docx (7.3 mb)
ESM 1 (DOCX 7442 kb)


  1. APHA (2012) Standard Methods for the Examination of Water and Wastewater, 22nd ed., American Public Health Association, Washington DC.Google Scholar
  2. Bassin JP, Kleerebezem R, Muyzer G, Rosado AS, Van Loosdrecht MCM, Dezotti M (2012) Effect of different salt adaptation strategies on the microbial diversity, activity, and settling of nitrifying sludge in sequencing batch reactors. Appl Microbiol Biotechnol 93:1281–1294. CrossRefGoogle Scholar
  3. Bian G, Gloor GB, Gong A, Jia C, Zhang W, Hu J, Zhang H, Zhang Y, Zhou Z, Zhang J, Burton JP, Reid G, Xiao Y, Zeng Q, Yang K, Li J (2017) The gut microbiota of healthy aged Chinese is similar to that of the healthy young. mSphere 2:e00327–e00317. CrossRefGoogle Scholar
  4. Castillo-Carvajal LC, Sanz-Martin JL, Barragan-Huerta BE (2014) Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review. Environ Sci Pollut Res 21:9578–9588. CrossRefGoogle Scholar
  5. Cortes-Lorenzo C, Rodriguez-Diaz M, Lopez-Lopez C, Sanchez-Peinado M, Rodelas B, Gonzalez-Lopez J (2012) Effect of salinity on enzymatic activities in a submerged fixed bed biofilm reactor for municipal sewage treatment. Bioresour Technol 121:312–319. CrossRefGoogle Scholar
  6. Cortés-Lorenzo C, González-Martínez A, Smidt H, González-López J, Rodelas B (2016) Influence of salinity on fungal communities in a submerged fixed bed bioreactor for wastewater treatment. Chem Eng J 285:562–572. CrossRefGoogle Scholar
  7. Di Trapani D, Di Bella G, Mannina G, Torregrossa M, Viviani G (2014) Comparison between moving bed-membrane bioreactor (MB-MBR) and membrane bioreactor (MBR) systems: influence of wastewater salinity variation. Bioresour Technol 162:60–69. CrossRefGoogle Scholar
  8. Di Bella G, Di Prima N, Di Trapani D, Freni G, Giustra MG, Torregrossa M, Viviane G (2015) Performance of membrane bioreactor (MBR) systems for the treatment of shipboard slops: assessment of hydrocarbon biodegradation and biomass activity under salinity variation, J. Hazard. Mater. 300:765–778.Google Scholar
  9. Eren AM, Borisy GG, Huse SM, Mark Welch JL (2014) PNAS plus: from the cover: oligotyping analysis of the human oral microbiome. Proc Natl Acad Sci 111:E2875–E2884. CrossRefGoogle Scholar
  10. Esmaeli A, Jokar M, Kousha M, Daneshvar E, Zilouei H (2013) Acidic dye wastewater treatment onto a marine macroalga, Nizamuddina zanardini (phylum: Ochrophyta). Chem Eng J 217:329–336. CrossRefGoogle Scholar
  11. Gonzalez-Martinez A, Rodriguez-Sanchez A, Lotti T, Garcia-Ruiz MJ, Osorio F, Gonzalez-Lopez J, van Loosdrecht MC (2016a) Comparison of bacterial communities of conventional and A-stage activated sludge systems. Sci Rep 6:18786. CrossRefGoogle Scholar
  12. Gonzalez-Martinez A, Garcia-Ruiz MJ, Rodriguez-Sanchez A, Osorio F, Gonzalez-Lopez J (2016b) Archaeal and bacterial community dynamics and bioprocess performance of a bench-scale two-stage anaerobic digester. Appl Microbiol Biotechnol 100:6013–6033. CrossRefGoogle Scholar
  13. Hao TW, Xiang P-Y, Mackey HR, Chi K, Lu H, Chui H-K, van Loosdrecht MCM, Chen G-H (2014) A review of biological sulfate conversions in wastewater treatment. Water Res 65:1–21. CrossRefGoogle Scholar
  14. Kämpfer P, Schulze R, Jäckel U, Malik KA, Amann R, Spring S (2005) Hydrogenophaga defluvii sp. nov. and Hydrogenophaga atypica sp. nov., isolated from activated sludge. Int J Syst Evol Microbiol 55:341–344. CrossRefGoogle Scholar
  15. Kindaichi T, Yamaoka S, Uehara R, Ozaki N, Ohashi A, Albertsen M, Nielsen PH, Nielsen JL (2016) Phylogenetic diversity and ecophysiology of candidate phylum Saccharibacteria in activated sludge. FEMS Microbiol Ecol:1–11.
  16. Lee S, Song EH, Lee T (2018) Eukaryotic plankton species diversity in the Western Channel of the Korea Strait using 18S rDNA sequences and its implications for water masses. Ocean Science Journal 153:119–132CrossRefGoogle Scholar
  17. Leyva-Díaz JC, Calderón K, Rodríguez FA, González-lópez J (2013) Comparative kinetic study between moving bed biofilm reactor-membrane bioreactor and membrane bioreactor systems and their influence on organic matter and nutrients removal. Biochem Eng J 77:28–40. CrossRefGoogle Scholar
  18. Leyva-Díaz JC, Martín-Pascual J, Muñío MM, González-López J, Hontoria E, Poyatos JM (2014) Comparative kinetics of hybrid and pure moving bed reactor-membrane bioreactors. Ecol Eng 70:227–234. CrossRefGoogle Scholar
  19. Leyva-Diaz JC, Gonzalez-Martinez A, Gonzalez-Lopez J, Muñio MM, Poyatos JM (2015a) Kinetic modeling and microbiological study of two-step nitrification in a membrane bioreactor and hybrid moving bed biofilm reactor–membrane bioreactor for wastewater treatment. Chem Eng J 259:692–702. CrossRefGoogle Scholar
  20. Leyva-Diaz JC, Lopez-Lopez C, Martin-Pascual J, Muñio MM, Poyatos JM (2015b) Kinetic study of the combined processes of a membrane bioreactor and a hybrid moving bed biofilm reactor-membrane bioreactor with advanced oxidation processes as a post-treatment stage for wastewater treatment. Chem Eng Process Process Intensif 91:57–66. CrossRefGoogle Scholar
  21. Leyva-Diaz JC, Gonzalez-Martinez A, Calderon K, Gonzalez-Lopez J, Muñio MM, Poyatos JM (2016) Microbial kinetics and enzymatic activities in hybrid moving-bed biofilm reactor-membrane bioreactor systems. Chem Eng Technol 39:1067–1076. CrossRefGoogle Scholar
  22. Li E, Lu S (2017) Denitrification processes and microbial communities in a sequencing batch reactor treating nanofiltration (NF) concentrate from coking wastewater. Water Sci. Technol. 76:11-12.
  23. McIlroy SJ, Kirkegaard RH, Mcilroy B, Nierychlo M, Kristensen JM, Karst SM (2017) MiDAS 2.0: an ecosystem-specific taxonomy and online database for the organisms of wastewater treatment systems expanded for anaerobic digester groups. Database (Oxford):1–9.
  24. Niu W, Guo J, Lian J, Hao H, Li H, Song Y, Li H, Yin P (2018) Effect of fluctuating hydraulic retention time (HRT) on denitrification in the UASB reactors. Biochem Eng J 132:29–37. CrossRefGoogle Scholar
  25. Okazaki Y, Fujinaga S, Tanaka A, Kohzu A, Oyagi H (2017) Ubiquity and quantitative significance of bacterioplankton lineages inhabiting the oxygenated hypolimnion of deep freshwater lakes. Nat Publ Gr 11:2279–2293. CrossRefGoogle Scholar
  26. Ouyang E, Liu Y, Ouyang J, Wang X (2017) Effects of different wastewater characteristics and treatment techniques on the bacterial community structure in three pharmaceutical wastewater treatment systems. Environ. Technol. 1:1–13.
  27. Rodriguez-Sanchez A, Leyva-Diaz JC, Gonzalez-Martinez A, Poyatos JM (2017) Linkage of microbial kinetics and bacterial community structure of MBR and hybrid MBBR-MBR systems to treat salinity-amended urban wastewater. Biotechnol Prog 33:1–13. CrossRefGoogle Scholar
  28. Rodriguez-Sanchez A, Leyva-Diaz JC, Gonzalez-Lopez J, Poyatos JM (2018a) Membrane bioreactor and hybrid moving bed biofilm reactor-membrane bioreactor for the treatment of variable salinity wastewater: influence of biomass concentration and hydraulic retention time. Chem Eng J 336:102–111. CrossRefGoogle Scholar
  29. Rodriguez-Sanchez A, Leyva-Diaz JC, Poyatos JM, Gonzalez-Lopez J (2018b) Influent salinity conditions affect the bacterial communities of biofouling in hybrid MBBR-MBR systems. J Water Proc Engineer.
  30. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. CrossRefGoogle Scholar
  31. Schloss PD (2016) Application of a database-independent approach to assess the quality of. mSystems 1:2–5. CrossRefGoogle Scholar
  32. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. CrossRefGoogle Scholar
  33. Schoenle A, Nitsche F, Werner J, Arndt H (2017) Deep-sea ciliates: recorded diversity and experimental studies on pressure tolerance. Deep Sea Res I 128:55–66. CrossRefGoogle Scholar
  34. Tao R, Kinnunen V, Praveenkumar R, Lakaniemi A (2017).Comparison of Scenedesmus acuminatus and Chlorella vulgaris cultivation in liquid digestates from anaerobic digestion of pulp and paper industry and municipal wastewater treatment sludge. 2845–2856.
  35. Teske A, Salman V (2014) The family Leucotrichaceae. The Prokaryotes. Springer-Verlag Berlin Heidelberg.Google Scholar
  36. Unno T (2015) Bioinformatic suggestions on MiSeq-based microbial community analysis. J Microbiol Biotechnol 25:765–770CrossRefGoogle Scholar
  37. Welles L, Lopez-Vazquez CM, Hooijmans CM, van Loosdrecht MCM, Brdjanovic D (2015) Impact of salinity on the aerobic metabolism of phosphate-accumulating organisms. Appl Microbiol Biotechnol 99:3659–3672. CrossRefGoogle Scholar
  38. Westcott SL, Schloss PD (2015) De novo clustering methods outperform reference-based methods for assigning 16S rRNA gene sequences to operational taxonomic units. PeerJ 3:e1487. CrossRefGoogle Scholar
  39. Wu Y-J, Whang L-M, Fukushima T, Chang S-H (2013) Responses of ammonia-oxidizing archaeal and betaproteobacterial populations to wastewater salinity in a full-scale municipal wastewater treatment plant. J Biosci Bioeng 115:424–432. CrossRefGoogle Scholar
  40. Yabuki A, Ishida K (2018) An orphan protist Quadricilia rotundata finally finds its phylogenetic home in Cercozoa. J Eukaryot Microbiol 65:729–732. CrossRefGoogle Scholar
  41. Zhang B, Xu X, Zhu L (2017) Structure and function of the microbial consortia of activated sludge in typical municipal wastewater treatment plants in winter. Sci Rep 7:1–11. CrossRefGoogle Scholar
  42. Zhen-Li Z, Xin-Qi Z, Nan W, Wen-Wu Z, Xu-Fen Z, Yi C, Min W (2018) Amphiplicatus metriothermophilus gen. nov., sp. nov., a thermotolerant alphaproteobacterium isolated from a hot spring. Int J Syst Evol Microbiol 64:2805–2811. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Water ResearchUniversity of GranadaGranadaSpain
  2. 2.Department of Civil EngineeringUniversity of GranadaGranadaSpain
  3. 3.Department of Chemical Engineering and Environmental TechnologyUniversity of OviedoOviedoSpain

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