In this work, microalgae cultivation trials were carried out in a membrane bioreactor to investigate fouling when the cultures of Chlorellavulgaris were grown under mixotrophic, heterotrophic, and phototrophic cultivation regimes. The Chlorella cultures were cultivated in wastewater as a source of nutrients that contained a high concentration of ammonium. In mixotrophic cultivation trials, the results showed that the elevated contents of carbohydrates in the soluble microbial product and proteins in extracellular polymeric substances probably initiated membrane fouling. In this case, the highest protein content was also found in extracellular polymeric substances due to the high nitrogen removal rate. Consequently, transmembrane pressure significantly increased compared to the phototrophic and heterotrophic regimes. The data indicated that cake resistance was the main cause of fouling in all cultivations. Higher protein content in the cake layer made the membrane surface more hydrophobic, while carbohydrates had the opposite effect. Compared to a mixotrophic culture, a phototrophic culture had a larger cell size and higher hydrophobicity, leading to less membrane fouling. Based on our previous data, the highest ammonia removal rate was reached in the mixotrophic cultures; nevertheless, membrane fouling appeared to be the fundamental problem.

Chemical and Petroleum Engineering Department Sharif University of Technology P O Box 11365 8639 Tehran Iran

Department of Chemical and Materials Engineering University of Alabama in Huntsville Huntsville AL 35899 USA

Department of Chemistry Karaj Branch Islamic Azad University Karaj Iran E mail

Department of Plant Breeding and Biotechnology Science and Research Branch Islamic Azad University Tehran Iran

Laboratory of Algal Biotechnology Centre ALGATECH Institute of Microbiology AV ČR v v i Třeboň Czech Republic; Faculty of Science University of South Bohemia České Budějovice Czech Republic

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Amini E., Babaei A., Mehrnia M. R., Shayegan J. & Safdari M.-S. 2020 Municipal wastewater treatment by semi-continuous and membrane algal-bacterial photo-bioreactors. Journal of Water Process Engineering 36, 101274.

Arun S., Sinharoy A., Pakshirajan K. & Lens P. N. L. 2020 Algae based microbial fuel cells for wastewater treatment and recovery of value-added products. Renewable and Sustainable Energy Reviews 132.

Association APH 1926 Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC, USA.

Azami H., Sarrafzadeh M. H. & Mehrnia M. R. 2011 Fouling in membrane bioreactors with various concentrations of dead cells. Desalination 278, 373–380.

Babaei A. & Mehrnia M. R. 2018 Fouling in microalgal membrane bioreactor containing nitrate-enriched wastewater under different trophic conditions. Algal Research 36, 167–174. doi:10.1016/j.algal.2018.10.017.

Babaei A., Mehrnia M. R., Shayegan J. & Sarrafzadeh M. H. 2016 Comparison of different trophic cultivations in microalgal membrane bioreactor containing N-riched wastewater for simultaneous nutrient removal and biomass production. Process Biochemistry 51, 1568–1575. doi:10.1016/j.procbio.2016.06.011.

Babel S. & Takizawa S. 2010 Microfiltration membrane fouling and cake behavior during algal filtration. Desalination 261, 46–51. doi:10.1016/j.desal.2010.05.038.

Babaei A. & Mehrnia M. R. 2018 Fouling in microalgal membrane bioreactor containing nitrate-enriched wastewater under different trophic conditions. Algal Research 36, 167–174. doi:10.1016/j.algal.2018.10.017.

Benner R., Biddanda B., Black B. & Mccarthy M. 1997 Abundance, Size Distribution, and Stable Carbon and Nitrogen Isotopic Compositions of Marine Organic Matter Isolated by Tangential-Flow Ultrafiltration.

Bhatt P., Bhandari G., Turco R. F., Aminikhoei Z., Bhatt K. & Simsek H. 2022 Algae in wastewater treatment, mechanism, and application of biomass for production of value-added product. Environmental Pollution 309, 119688. doi:10.1016/j.envpol.2022.119688. PubMed

Cao S., Teng F., Wang T., Li X., Lv J., Cai Z. & Tao Y. 2020 Characteristics of an immobilized microalgae membrane bioreactor (iMBR): Nutrient removal, microalgae growth, and membrane fouling under continuous operation. Algal Research 51. doi:10.1016/j.algal.2020.102072.

Chang I.-S. & Lee C.-H. 1998 Membrane filtration characteristics in membrane-coupled activated sludge system – the effect of physiological states of activated sludge on membrane fouling. Desalination 120, 221–233.

Chew K. W., Chia S. R., Show P. L., Yap Y. J., Ling T. C. & Chang J. S. 2018 Effects of water culture medium, cultivation systems and growth modes for microalgae cultivation: A review. Journal of the Taiwan Institute of Chemical Engineers 91, 332–344.

Classics Lowry O., Rosebrough N., Farr A. & Randall R. 1951 Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275. PubMed

Coronado-Reyes J. A., Salazar-Torres J. A., Juárez-Campos B. & González-Hernández J. C. 2022

Díaz O., Vera L., Fernández L. J., Díaz-Marrero A. R. & Fernández J. J. 2016 Effect of sludge characteristics on membrane fouling during start-up of a tertiary submerged membrane bioreactor. Environmental Science and Pollution Research 23, 8951–8962. doi:10.1007/s11356-016-6138-y.

Díaz O., González E., García E. & Rodríguez-Sevilla J. 2023 Recirculating packed-bed biofilm photobioreactor combined with membrane ultrafiltration as advanced wastewater treatment. Environmental Science and Pollution Research 30, 69977–69990. doi:10.1007/s11356-023-27309-2.. PMC

DuBois M., Gilles K. A., Hamilton J. K., Rebers P. A. & Smith F. 1956 Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.

Elcik H., Cakmakci M. & Ozkaya B. 2016 The fouling effects of microalgal cells on crossflow membrane filtration. Journal of Membrane Science 499, 116–125. doi:10.1016/j.memsci.2015.10.043.

Fakhimi N. & Mehrnia M. R. 2016 Control of mixing for optimal formation of dynamic membrane in MBRs. Desalination Water Treat 57, 15759–15771.

Feng H. J., Chen L., Ying X., Bin, Yu S. S. & Ding Y. C. 2022 The impact of powdered activated carbon types on membrane anti-fouling mechanism in membrane bioreactors. Applied Microbiology and Biotechnology 106, 7337–7345. doi:10.1007/s00253-022-12186-5. PubMed

Ghernaout B., Ghernaout D. & Saiba A. 2010 Algae and cyanotoxins removal by coagulation/flocculation: A review. Desalination Water Treat 20, 133–143.

Gkotsis P. K. & Zouboulis A. I. 2019 Biomass characteristics and their effect on membrane bioreactor fouling. Molecules 24 (16).

Juang R.-S., Chen H.-L. & Chen Y.-S. 2008 Resistance-in-series analysis in cross-flow ultrafiltration of fermentation broths of

Low S. L., Ong S. L. & Ng H. Y. 2016 Characterization of membrane fouling in submerged ceramic membrane photobioreactors fed with effluent from membrane bioreactors. Chemical Engineering Journal 290, 91–102.

Maaz M., Aslam M., Yasin M., Khan A. L., Mushtaq A., Fazal T., Aljuwayid A. M., Habila M. A. & Kim J. 2023 Macroalgal biochar synthesis and its implication on membrane fouling mitigation in fluidized bed membrane bioreactor for wastewater treatment. Chemosphere 324, 138197. doi:10.1016/j.chemosphere.2023.138197. PubMed

Marbelia L., Bilad M. R., Passaris I., Discart V., Vandamme D., Beuckels A., Muylaert K. & Vankelecom I. F. J. 2014 Membrane photobioreactors for integrated microalgae cultivation and nutrient remediation of membrane bioreactors effluent. Bioresource Technology 163, 228–235. doi:10.1016/j.biortech.2014.04.012. PubMed

Mofijur M., Hasan M. M., Sultana S., Kabir Z., Djavanroodi F., Ahmed S. F., Jahirul M. I., Badruddin I. A. & Khan T. M. Y. 2023 Advancements in algal membrane bioreactors: Overcoming obstacles and harnessing potential for eliminating hazardous pollutants from wastewater. Chemosphere 336, 139291. doi:10.1016/j.chemosphere.2023.139291. PubMed

Mohsenpour S. F., Hennige S., Willoughby N., Adeloye A. & Gutierrez T. 2021 Integrating micro-algae into wastewater treatment: A review. Science of the Total Environment 752.

Morgan J. W., Forster C. F. & Evison L. 1990 A comparative study of the nature of biopolymers extracted from anaerobic and activated sludges. Water Research 24, 743–750.

Najafi Chaleshtori S., Shamskilani M., Babaei A. & Behrang M. 2022 Municipal wastewater treatment and fouling in microalgal-activated sludge membrane bioreactor: Cultivation in raw and treated wastewater. Journal of Water Process Engineering 49. doi:10.1016/j.jwpe.2022.103069.

Negaresh E., Le-Clech P. & Chen V. 2006 Fouling mechanisms of model extracellular polymeric substances in submerged membrane reactor. Desalination 200, 715–717. doi:10.1016/j.desal.2006.03.508.

Ozkan A. & Berberoglu H. 2013 Cell to substratum and cell to cell interactions of microalgae. Colloids Surf B Biointerfaces 112, 302–309. PubMed

Pan J. R., Su Y.-C., Huang C. & Lee H.-C. 2010 Effect of sludge characteristics on membrane fouling in membrane bioreactors. Journal of Membrane Science 349, 287–294.

Pratt R. & Fong J. 1940 Studies on

Rohit M. V. & Mohan S. V. 2016 Tropho-metabolic transition during Chlorella sp. cultivation on synthesis of biodiesel. Renew Energy 98, 84–91.

Robles Á., Capson-Tojo G., Gales A., Viruela A., Sialve B., Seco A., Steyer J. P. & Ferrer J. 2020 Performance of a membrane-coupled high-rate algal pond for urban wastewater treatment at demonstration scale. Bioresource Technology 301.

Roccaro P. & Vagliasindi F. G. A. 2020 Techno-economic feasibility of membrane bioreactor (MBR).

Shafiquzzaman M., Hasan M. M., Haider H., Ahmed A. T. & Razzak S. A. 2023 Comparative evaluation of low-cost ceramic membrane and polymeric micro membrane in algal membrane photobioreactor for wastewater treatment. Journal of Environmental Management 345.

Shariati S. R. P., Bonakdarpour B., Zare N. & Ashtiani F. Z. 2011 The effect of hydraulic retention time on the performance and fouling characteristics of membrane sequencing batch reactors used for the treatment of synthetic petroleum refinery wastewater. Bioresource Technology 102, 7692–7699. PubMed

Shariati F. P., Heran M., Sarrafzadeh M. H., Mehrnia M. R., Sarzana G., Ghommidh C. & Grasmick A. 2013 Biomass characterization by dielectric monitoring of viability and oxygen uptake rate measurements in a novel membrane bioreactor. Bioresource Technology 140, 357–362. PubMed

Shi Y., Huang J., Zeng G., Gu Y., Hu Y., Tang B., Zhou J., Yang Y. & Shi L. 2018 Evaluation of soluble microbial products (SMP) on membrane fouling in membrane bioreactors (MBRs) at the fractional and overall level: A review. Reviews in Environmental Science and Biotechnology 17, 71–85.

Sudhakar K. & Premalatha M. 2015 Characterization of micro algal biomass through FTIR/TGA/CHN analysis: Application to Scenedesmus sp. Energy Sources, Part A: Recovery, Utilization, and Environmental Effects 37, 2330–2337.

Suparmaniam U., Lam M. K., Uemura Y., Lim J. W., Lee K. T. & Shuit S. H. 2019 Insights into the microalgae cultivation technology and harvesting process for biofuel production: A review. Renewable and Sustainable Energy Reviews 115.

Tan J. S., Lee S. Y., Chew K. W., Lam M. K., Lim J. W., Ho S. H. & Show P. L. 2020 A review on microalgae cultivation and harvesting, and their biomass extraction processing using ionic liquids. Bioengineered 11, 116–129. doi:10.1080/21655979.2020.1711626. PubMed PMC

Trabelsi L., Ben Ouada H., Zili F., Mazhoud N. & Ammar J. 2013 Evaluation of Arthrospira platensis extracellular polymeric substances production in photoautotrophic, heterotrophic and mixotrophic conditions. Folia Microbiol (Praha) 58, 39–45. PubMed

Yang S., Wang J., Cong W., Cai Z. & Ouyang F. 2004 Utilization of nitrite as a nitrogen source by PubMed

Yu H., Qu F., Liang H., Han Z., shuang, Ma J., Shao S., Chang H. & Li G. 2014 Understanding ultrafiltration membrane fouling by extracellular organic matter of

Zahmatkesh S., Karimian M., Pourhanasa R., Ghodrati I., Hajiaghaei-Keshteli M. & Ismail M. A. 2023 Wastewater treatment with algal based membrane bioreactor for the future: Removing emerging containments. Chemosphere 335.

Zhang J., Chua H. C., Zhou J. & Fane A. G. 2006 Factors affecting the membrane performance in submerged membrane bioreactors. Journal of Membrane Science 284, 54–66.

Zhang M., Leung K. T., Lin H. & Liao B. 2022 Evaluation of membrane fouling in a microalgal-bacterial membrane photobioreactor: Effects of SRT. Science of the Total Environment 839. doi:10.1016/j.scitotenv.2022.156414.

Zhao Z., Muylaert K. & Vankelecom I. F. J. 2022 Applying Membrane Technology in Microalgae Industry: A Comprehensive Review.

Zheng W., Yu Z., Xia Y. & Wen X. 2018 Influence of polyaluminum chloride on microbial characteristics in anaerobic membrane bioreactors for sludge digestion. Applied Microbiology and Biotechnology 102, 1005–1017. doi:10.1007/s00253-0a17-8613-x. PubMed