{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T17:51:27Z","timestamp":1788285087077,"version":"build-2803163510"},"reference-count":44,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T00:00:00Z","timestamp":1663286400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Membranes"],"abstract":"<jats:p>Microalgae have attracted great interest recently due to their potential for nutrients removal from wastewater, renewable biodiesel production and bioactive compounds extraction. However, one major challenge in microalgal bioremediation and the algal biofuel process is the high energy cost of separating microalgae from water. Our previous studies demonstrated that forward osmosis (FO) is a promising technology for microalgae harvesting and dewatering due to its low energy consumption and easy fouling control. In the present study, two FO module configurations (side-stream and submerged) were integrated with microalgae (C. vulgaris) photobioreactor (PBR) in order to evaluate the system performance, including nutrients removal, algae harvesting efficiency and membrane fouling. After 7 days of operation, both systems showed effective nutrients removal. A total of 92.9%, 100% and 98.7% of PO4-P, NH3-N and TN were removed in the PBR integrated with the submerged FO module, and 82%, 96% and 94.8% of PO4-P, NH3-N and TN were removed in the PBR integrated with the side-stream FO module. The better nutrients removal efficiency is attributed to the greater algae biomass in the submerged FO-PBR where in situ biomass dewatering was conducted. The side-stream FO module showed more severe permeate flux loss and biomass loss (less dewatering efficiency) due to algae deposition onto the membrane. This is likely caused by the higher initial water flux associated with the side-stream FO configuration, resulting in more foulants being transported to the membrane surface. However, the side-stream FO module showed better fouling mitigation by simple hydraulic flushing than the submerged FO module, which is not convenient for conducting cleaning without interrupting the PBR operation. Taken together, our results suggest that side-stream FO configuration may provide a viable way to integrate with PBR for a microalgae-based treatment. The present work provides novel insights into the efficient operation of a FO-PBR for more sustainable wastewater treatment and effective microalgae harvesting.<\/jats:p>","DOI":"10.3390\/membranes12090892","type":"journal-article","created":{"date-parts":[[2022,9,19]],"date-time":"2022-09-19T02:06:50Z","timestamp":1663553210000},"page":"892","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["The Influence of Forward Osmosis Module Configuration on Nutrients Removal and Microalgae Harvesting in Osmotic Photobioreactor"],"prefix":"10.3390","volume":"12","author":[{"given":"Mathieu","family":"Larronde-Larretche","sequence":"first","affiliation":[{"name":"Keon Research LLC, 2151 N Northlake Way b, Seattle, WA 98103, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4887-5506","authenticated-orcid":false,"given":"Xue","family":"Jin","sequence":"additional","affiliation":[{"name":"School of Chemical Engineering, Biological Engineering & Environmental Engineering, Oregon State University, Corvallis, OR 97331, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"237","DOI":"10.5194\/essd-13-237-2021","article-title":"Country-level and gridded estimates of wastewater production, collection, treatment and reuse","volume":"13","author":"Jones","year":"2021","journal-title":"Earth Syst. Sci. Data"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/j.algal.2016.11.008","article-title":"A review on the use of microalgal consortia for wastewater treatment","volume":"24","author":"Pires","year":"2017","journal-title":"Algal Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"120744","DOI":"10.1016\/j.seppur.2022.120744","article-title":"Submerged hollow-fiber-ultrafiltration for harvesting microalgae used for bioremediation of a secondary wastewater","volume":"289","author":"Wang","year":"2022","journal-title":"Sep. Purif. Technol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"70","DOI":"10.3389\/fenvs.2017.00070","article-title":"Enhancing the Energy Efficiency of Wastewater Treatment Plants through Co-digestion and Fuel Cell Systems","volume":"5","author":"Gandiglio","year":"2017","journal-title":"Front. Environ. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1007\/s13201-012-0040-7","article-title":"Energy pattern analysis of a wastewater treatment plant","volume":"2","author":"Singh","year":"2012","journal-title":"Appl. Water Sci."},{"key":"ref_6","unstructured":"EPA, U. (2022, August 13). Energy Efficiency for Water Utilities, Available online: https:\/\/www.epa.gov\/sustainable-water-infrastructure\/energy-efficiency-water-utilities."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1023\/A:1023855710410","article-title":"Hydrocarbon production from secondarily treated piggery wastewater by the green alga Botryococcus braunii","volume":"15","author":"An","year":"2003","journal-title":"J. Appl. Phycol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.scitotenv.2017.02.224","article-title":"Performance of a microalgal photobioreactor treating toilet wastewater: Pharmaceutically active compound removal and biomass harvesting","volume":"592","author":"Vicent","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Chen, Z., Xiao, Y., Liu, T., Yuan, M., Liu, G., Fang, J., and Yang, B. (2021). Exploration of Microalgal Species for Nutrient Removal from Anaerobically Digested Swine Wastewater and Potential Lipids Production. Microorganisms, 9.","DOI":"10.3390\/microorganisms9122469"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/j.algal.2016.05.022","article-title":"Growth comparison of microalgae in tubular photobioreactor and open pond for treating anaerobic digestion piggery effluent","volume":"17","author":"Nwoba","year":"2016","journal-title":"Algal Res."},{"key":"ref_11","first-page":"73","article-title":"Bioconversion of solar energy into organic chemicals by microalgae","volume":"6","author":"Gudin","year":"1987","journal-title":"Adv. Biotechnol. Processes"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.memsci.2006.05.048","article-title":"Forward osmosis: Principles, applications, and recent developments","volume":"281","author":"Cath","year":"2006","journal-title":"J. Membr. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1283","DOI":"10.1016\/j.biotechadv.2014.07.008","article-title":"Membrane technology in microalgae cultivation and harvesting: A review","volume":"32","author":"Bilad","year":"2014","journal-title":"Biotechnol. Adv."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.algal.2016.01.014","article-title":"Microalgae (Scenedesmus obliquus) dewatering using forward osmosis membrane: Influence of draw solution chemistry","volume":"15","author":"Jin","year":"2016","journal-title":"Algal Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.algal.2016.12.020","article-title":"Microalgal biomass dewatering using forward osmosis membrane: Influence of microalgae species and carbohydrates composition","volume":"23","author":"Jin","year":"2017","journal-title":"Algal Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.biortech.2016.01.102","article-title":"Nitrogen and phosphorus removal from tertiary wastewater in an osmotic membrane photobioreactor","volume":"206","author":"Praveen","year":"2016","journal-title":"Bioresour. Technol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1039\/C5EW00103J","article-title":"The osmotic membrane bioreactor: A critical review","volume":"1","author":"Holloway","year":"2015","journal-title":"Environ. Sci. Water Res. Technol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.rser.2009.07.020","article-title":"Microalgae for biodiesel production and other applications: A review","volume":"14","author":"Mata","year":"2010","journal-title":"Renew. Sustain. Energy Rev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.12989\/mwt.2012.3.1.001","article-title":"Developments and future potentials of anaerobic membrane bioreactors (AnMBRs)","volume":"3","author":"Visvanathan","year":"2012","journal-title":"Membr. Water Treat."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.memsci.2009.11.021","article-title":"Organic fouling of forward osmosis membranes: Fouling reversibility and cleaning without chemical reagents","volume":"348","author":"Mi","year":"2010","journal-title":"J. Membr. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.rser.2012.11.030","article-title":"Nutrient recovery from wastewater streams by microalgae: Status and prospects","volume":"19","author":"Cai","year":"2013","journal-title":"Renew. Sustain. Energy Rev."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.jbiotec.2006.05.002","article-title":"High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters","volume":"126","author":"Xu","year":"2006","journal-title":"J. Biotechnol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.1016\/j.matpr.2022.04.854","article-title":"Microalgae dewatering using forward osmosis membrane: A review","volume":"65","author":"Vrasna","year":"2022","journal-title":"Mater. Today Proc."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"225","DOI":"10.5897\/JECE2011.025","article-title":"Algal density assessed by spectrophotometry: A calibration curve for the unicellular algae Pseudokirchneriella subcapitata","volume":"3","author":"Rodrigues","year":"2011","journal-title":"J. Environ. Chem. Ecotoxicol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.biortech.2003.11.006","article-title":"Sedimentological evolution in an UASB treating SYNTHES, a new representative synthetic sewage, at low loading rates","volume":"93","author":"Aiyuk","year":"2004","journal-title":"Bioresour. Technol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.desal.2005.02.036","article-title":"Concentration of brines from RO desalination plants by natural evaporation","volume":"182","author":"Arnal","year":"2005","journal-title":"Desalination"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.memsci.2016.09.026","article-title":"Calcium carbonate scaling by reverse draw solute diffusion in a forward osmosis membrane for shale gas wastewater treatment","volume":"522","author":"Lee","year":"2017","journal-title":"J. Membr. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.memsci.2011.11.018","article-title":"Direct quantification of negatively charged functional groups on membrane surfaces","volume":"389","author":"Tiraferri","year":"2012","journal-title":"J. Membr. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"4380","DOI":"10.1021\/acs.est.8b05925","article-title":"Evidence, Determination, and Implications of Membrane-Independent Limiting Flux in Forward Osmosis Systems","volume":"53","author":"Morrow","year":"2019","journal-title":"Environ. Sci. Technol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.memsci.2017.11.030","article-title":"Submerged or sidestream? The influence of module configuration on fouling and salinity in osmotic membrane bioreactors","volume":"548","author":"Morrow","year":"2018","journal-title":"J. Membr. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"123754","DOI":"10.1016\/j.biortech.2020.123754","article-title":"Co-culture of microalgae-activated sludge for wastewater treatment and biomass production: Exploring their role under different inoculation ratios","volume":"314","author":"Nguyen","year":"2020","journal-title":"Bioresour. Technol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.biortech.2015.07.013","article-title":"Membrane bioreactor: A mini review on recent R&D works","volume":"194","author":"Huang","year":"2015","journal-title":"Bioresour. Technol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/j.biortech.2013.09.090","article-title":"Osmotic membrane bioreactor for wastewater treatment and the effect of salt accumulation on system performance and microbial community dynamics","volume":"150","author":"Qiu","year":"2013","journal-title":"Bioresour. Technol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.biortech.2015.06.050","article-title":"Saline wastewater treatment by Chlorella vulgaris with simultaneous algal lipid accumulation triggered by nitrate deficiency","volume":"193","author":"Shen","year":"2015","journal-title":"Bioresour. Technol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"115196","DOI":"10.1016\/j.desal.2021.115196","article-title":"Submerged versus side-stream osmotic membrane bioreactors using an outer-selective hollow fiber osmotic membrane for desalination","volume":"515","author":"Tran","year":"2021","journal-title":"Desalination"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1016\/j.biortech.2016.09.124","article-title":"Tertiary wastewater treatment in membrane photobioreactor using microalgae: Comparison of forward osmosis & microfiltration","volume":"222","author":"Praveen","year":"2016","journal-title":"Bioresour. Technol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"128116","DOI":"10.1016\/j.chemosphere.2020.128116","article-title":"Forward osmosis membrane technology for nutrient removal\/recovery from wastewater: Recent advances, proposed designs, and future directions","volume":"263","author":"Jafarinejad","year":"2021","journal-title":"Chemosphere"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1488","DOI":"10.1007\/s12010-018-2889-x","article-title":"Microalgal cultivation and nutrient removal from digested piggery wastewater in a thin-film flat plate photobioreactor","volume":"187","author":"Sun","year":"2019","journal-title":"Appl. Biochem. Biotechnol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3213","DOI":"10.1016\/j.jece.2018.04.064","article-title":"Energetic evaluation of wastewater treatment using microalgae, Chlorella vulgaris","volume":"6","author":"Otondo","year":"2018","journal-title":"J. Environ. Chem. Eng."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"130758","DOI":"10.1016\/j.chemosphere.2021.130758","article-title":"Integrating bioremediation of textile wastewater with biodiesel production using microalgae (Chlorella vulgaris)","volume":"281","author":"Fazal","year":"2021","journal-title":"Chemosphere"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"127546","DOI":"10.1016\/j.cej.2020.127546","article-title":"Assessing the potential of microalgae for nutrients removal from a landfill leachate using an innovative tubular photobioreactor","volume":"413","author":"Porto","year":"2021","journal-title":"Chem. Eng. J."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"149988","DOI":"10.1016\/j.scitotenv.2021.149988","article-title":"Removal of nitrate and phosphate from simulated agricultural runoff water by Chlorella vulgaris","volume":"802","author":"Vazirzadeh","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"126003","DOI":"10.1016\/j.biortech.2021.126003","article-title":"Microalgae Chlorella vulgaris and Scenedesmus dimorphus co-cultivation with landfill leachate for pollutant removal and lipid production","volume":"342","author":"Hu","year":"2021","journal-title":"Bioresour. Technol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Blandin, G., Rodriguez-Roda, I., and Comas, J. (2018). Submerged Osmotic Processes: Design and Operation to Mitigate Mass Transfer Limitations. Membranes, 8.","DOI":"10.3390\/membranes8030072"}],"container-title":["Membranes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/9\/892\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:32:50Z","timestamp":1760142770000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/9\/892"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,16]]},"references-count":44,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["membranes12090892"],"URL":"https:\/\/doi.org\/10.3390\/membranes12090892","relation":{},"ISSN":["2077-0375"],"issn-type":[{"value":"2077-0375","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,16]]}}}