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Microalgal–Bacterial Flocs and Extracellular Polymeric Substances: Two Essential and Valuable Products of Integrated Algal Pond Systems

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Abstract

The integrated algal pond system (IAPS) is a passive wastewater treatment technology that can be used to remediate liquid waste from domestic, industrial and agricultural sources. The system exploits the mutualistic interaction between microalgae and bacteria to generate water of a quality suitable for discharge and/or reuse. During the treatment process, biomass in the form of microalgal–bacterial flocs (MaB-flocs) is generated, and this can be harvested and beneficiated in downstream processing. Here, we review literature on MaB-floc and extracellular polymeric substance (EPS) formation and discuss how essential microalgal–bacterial mutualism is at effecting IAPS-based wastewater treatment. Aggregation of microalgae and bacteria into MaB-flocs is clearly an outcome of EPS production by these microorganisms and arises for purposes of chemical and developmental interaction, protection, communication, aggregation and adhesion. The polymeric compounds which form the scaffold of this extracellular matrix comprise polysaccharides, proteins, uronic acid and nucleic acid. Natural EPS can be used as bioflocculant in water purification and in the dewatering and settling of sludge and is therefore an ideal natural replacement for commercially available synthetic polymers. Additionally, EPS are considered high value and can be used in many commercial applications. Thus, and to ensure sustained MaB-floc production in IAPS-based wastewater treatment plants, it is important that correct levels of EPS are maintained to facilitate settling and biomass recovery. Furthermore, it is the associated environmental and operational conditions that most impact EPS production and in turn, MaB-floc formation, and quality of the final IAPS-treated water.

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Abbreviations

AIWPS:

Advanced integrated wastewater pond system

BOD:

Biological oxygen demand

COD:

Chemical oxygen demand

EPS:

Extracellular polymeric substance

HRAOP:

High rate algal oxidation ponds

IAPS:

Integrated algal pond system

MaB-flocs:

Microalgal–bacterial flocs

MABA:

Microalgal–bacterial aggregates

QS:

Quorum sensing

TSS:

Total suspended solids

References

  • Acién, F. G., Gómez-Serrano, C., Morales-Amaral, M. M., Fernández-Sevilla, J. M., & Molina-Grima, E. (2016). Wastewater treatment using microalgae: How realistic a contribution might it be to significant urban wastewater treatment? Applied Microbiology and Biotechnology, 100(21), 9013–9022.

    Google Scholar 

  • Ahmed, M., Moerdijk-Poortvliet, T. C. W., Wijnholds, A., & Hasnain, S. (2014). Isolation, characterization and localization of extracellular polymeric substances from the cyanobacterium Arthrospira platensis strain MMG-9. European Journal of Phycology, 49(2), 143–150.

    CAS  Google Scholar 

  • An, C., Ma, S. J., Chang, F., & Xue, W. J. (2017). Efficient production of pullulan by Aureobasidium pullulans grown on mixtures of potato starch hydrolysate and sucrose. Brazilian Journal of Microbiology, 48, 180–185.

    CAS  Google Scholar 

  • Aquino, S. F., Gloria, R. M., Silva, S. Q., & Chernicharo, C. A. L. (2009). Quantification of the inert chemical oxygen demand of raw wastewater and evaluation of soluble microbial product production in demo-scale upflow anaerobic sludge blanket reactors under different operational conditions. Water Environment Research, 81(6), 608–616.

    CAS  Google Scholar 

  • Arashiro, L. T., Montero, N., Ferrer, I., Acien, F. G., & Garfi, M. (2018). Life cycle assessment of high rate algal ponds for wastewater treatment and resource recovery. Science of the Total Environment, 622-623, 1118–1130.

    CAS  Google Scholar 

  • Arcila, J. S., & Buitrón, G. (2016). Microalgae-bacteria aggregates: Effect of the hydraulic retention time on the municipal wastewater treatment, biomass settleability and methane potential. Journal of Chemical Technology and Biotechnology, 91, 2862–2870.

    CAS  Google Scholar 

  • Arcila, J. S., & Buitrón, G. (2017). Influence of solar irradiance levels on the formation of microalgae–bacteria aggregates for municipal wastewater treatment. Algal Research, 27, 190–197.

    Google Scholar 

  • Bajaj, I. B., Survase, S. A., Saudagar, P. S., & Singhal, R. S. (2007). Gellan gum: Fermentative production, downstream processing and applications. Food Technology and Biotechnology, 45(4), 341–354.

    CAS  Google Scholar 

  • Banat, I. M., Puskas, K., Esen, I. I., & Al-Daher, R. (1990). Wastewater treatment and algal productivity in an integrated ponding system. Biological Wastes, 32, 265–275.

    CAS  Google Scholar 

  • Barros, A. I., Goncalves, A. L., Simoes, M., & Pires, J. C. M. (2015). Harvesting techniques applied to microalgae: A review. Renewable and Sustainable Energy Reviews, 41, 1489–1500.

    Google Scholar 

  • Barros, A. C., Gonçalves, A. L., & Simões, M. (2018). Microalgal/cyanobacterial biofilm formation on selected surfaces: The effects of surface physicochemical properties and culture media composition. Journal of Applied Phycology. https://doi.org/10.1007/s10811-018-1582-3.

    Google Scholar 

  • Benemann, J. R., Weissman, J. C., Koopman, B. L., & Oswald, W. J. (1977). Energy production by microbial photosynthesis. Nature, 268(5615), 19–23.

    CAS  Google Scholar 

  • Bramhachari, P. V., & Dubey, S. K. (2006). Isolation and characterization of exopolysaccharide produced by Vibrio harveyi strain VB23. Letters in Applied Microbiology, 43(5), 571–577.

    CAS  Google Scholar 

  • Brownlee, C. (2002). Role of the extracellular matrix in cell–cell signalling: Paracrine paradigms. Current Opinion in Plant Biology, 5(5), 396–401.

    CAS  Google Scholar 

  • Castillo, N. A., Valdez, A. L., & Fariña, J. I. (2015). Microbial production of scleroglucan and downstream processing. Frontiers in Microbiology, 6, 1106. https://doi.org/10.3389/fmicb.2015.01106.

    Article  Google Scholar 

  • Cheng, K. C., Demirci, A., & Catchmark, J. M. (2011). Pullulan: Biosynthesis, production, and applications. Applied Microbiology and Biotechnology, 92, 29–44.

    CAS  Google Scholar 

  • Chong, B. F., Blank, L. M., Mclaughlin, R., & Nielsen, L. K. (2005). Microbial hyaluronic acid production. Applied Microbiology and Biotechnology, 66, 341–351.

    CAS  Google Scholar 

  • Coppens, J., Grunert, O., Van Den Hende, S., Vanhoutte, I., Boon, N., Haesaert, G., & De Gelder, L. (2016). The use of microalgae as a high-value organic slow-release fertilizer results in tomatoes with increased carotenoid and sugar levels. Journal of Applied Phycology, 28(4), 2367–2377.

    CAS  Google Scholar 

  • Costerton, J. W., Geesey, G. G., & Cheng, K. J. (1978). How bacteria stick. Scientific American, 238, 85–95.

    Google Scholar 

  • Cowan, A. K. (2010). Bio-refineries: Bioprocess technologies for waste-water treatment, energy and product valorization. In: Tarasenko O., (ed.) Biology, nanotechnology, toxicology and applications: Proceedings of the 4th BioNanoTox conference, AIP 1229, 80–86.

  • Craggs, R. J. (2005) Advanced integrated wastewater ponds. In: Shilton A (ed.) Pond treatment technology. IWA Scientific and Technical Report Series. IWA, London. 282–310.

  • Craggs, R. J., Davies-Colley, R. J., Tanner, C. C., & Sukias, J. P. S. (2003a). Advanced ponds systems: Performance with high rate ponds of different depths and areas. Water Science and Technology, 48, 259–267.

    CAS  Google Scholar 

  • Craggs, R., Tanner, C., Sukias, J., & Davies-Colley, R. (2003b). Dairy farm wastewater treatment by an advanced pond system. Water Science and Technology, 48, 291–297.

    CAS  Google Scholar 

  • Craggs, R., Park, J., Heubeck, S., & Sutherland, D. (2014). High rate algal pond systems for low-energy wastewater treatment, nutrient recovery and energy production. New Zealand Journal of Botany, 52(1), 60–s73.

    Google Scholar 

  • Czaczyk, K., & Myszka, K. (2007). Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Polish Journal of Environmental Study, 16(6), 799–806.

    CAS  Google Scholar 

  • De Godos, I., Guzman, H. O., Soto, R., García-Encina, P. A., Becares, E., Muñoz, R., & Vargas, V. A. (2011). Coagulation/flocculation-based removal of algal–bacterial biomass from piggery wastewater treatment. Bioresource Technology, 102, 923–927.

    Google Scholar 

  • De Schryver, P., Crab, R., Defoirdt, T., Boon, N., & Verstraete, W. (2008). The basics of bio-flocs technology: The added value for aquaculture. Aquaculture, 277(3–4), 125–137.

    Google Scholar 

  • Decho, A. W., & Gutierrez, T. (2017). Microbial extracellular polymeric substances (EPSs) in ocean systems. Frontiers in Microbiology, 8, 922. https://doi.org/10.3389/fmicb.2017.00922.

    Article  Google Scholar 

  • Delattre, C., Pierre, G., Laroche, C., & Michaud, P. (2016). Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnology Advances, 34, 1159–1179.

    CAS  Google Scholar 

  • Devi, C. S., Reddy, S., & Mohanasrinivasan, V. (2014). Fermentative production of dextran using Leuconostoc spp. isolated from fermented food products. Frontiers in Microbiology, 9(3), 244–253.

    Google Scholar 

  • Ding, Z., Bourven, I., Guibaud, G., van Hullebusch, E. D., Panico, A., Pirozzi, F., & Esposito, G. (2015). Role of extracellular polymeric substances (EPS) production in bioaggregation: Application to wastewater treatment. Applied Microbiology and Biotechnology, 99, 9883–9905.

    CAS  Google Scholar 

  • Elnahas, M. O., Amin, M. A., Hussein, M. M. D., Shanbhag, V. C., Ali, A. E., & Wall, J. D. (2017). Isolation, characterization and bioactivities of an extracellular polysaccharide produced from Streptomyces sp. MOE6. Molecules, 22(9), 1396. https://doi.org/10.3390/molecules22091396.

    Article  CAS  Google Scholar 

  • Esa, F., Tasirin, S. M., & Abd Rahman, N. (2014). Overview of bacterial cellulose production and application. Agriculture and Agricultural Science Procedia, 2, 113–119.

    Google Scholar 

  • Fallowfield, H., & Garrett, M. (1985). The photosynthetic treatment of pig slurry in temperate climatic conditions: A pilot-plant study. Agricultural Wastes, 12, 111–136.

    CAS  Google Scholar 

  • Fariña, J. I., Sinrez, F., Molina, O. E., & Perotti, N. I. (1998). High scleroglucan production by Sclerotium rolfsii: Influence of medium composition. Biotechnology Letters, 20(9), 825–831.

    Google Scholar 

  • Fialho, A. M., Moreira, L. M., Granja, A. T., Popescu, A. O., Hoffmann, K., & Sá-Correia, I. (2008). Occurrence, production, and applications of gellan: Current state and perspectives. Applied Microbiology and Biotechnology, 79, 889–900.

    CAS  Google Scholar 

  • Flemming, H.-C. (2011). The perfect slime. Colloids and Surfaces B: Biointerfaces, 86, 251–259.

    CAS  Google Scholar 

  • Flemming, H.-C. (2016). EPS—then and now. Microorganisms, 4, 41. https://doi.org/10.3390/microorganisms4040041.

    Article  CAS  Google Scholar 

  • Flemming, H. C., & Wingender, J. (2001). Relevance of microbial extracellular polymeric substances (EPSs)—part I: Structural and ecological aspects. Water Science and Technology, 43(6), 1–8.

    CAS  Google Scholar 

  • Galindo, E., Peña, C., Núñez, C., Segura, D., & Espín, G. (2007). Molecular and bioengineering strategies to improve alginate and polydydroxyalkanoate production by Azotobacter vinelandii. Microbial Cell Factories, 6, 7. https://doi.org/10.1186/1475-2859-6-7.

    Article  CAS  Google Scholar 

  • García, J., Hernández-Mariné, M., & Mujeriego, R. (2000). Influence of phytoplankton composition on biomass removal from high-rate oxidation lagoons by means of sedimentation and spontaneous flocculation. Water Environment Research, 72(2), 230–237. https://doi.org/10.2175/106143000X137392.

    Article  Google Scholar 

  • Garcia-Gonzalez, J., & Sommerfeld, M. (2016). Biofertilizer and biostimulant properties of the microalga Acutodesmus dimorphus. Journal of Applied Phycology, 28, 1051–1061.

    Google Scholar 

  • Garcia-Ochoa, F., Santos, V. E., Casa, J. A., & Gomez, E. (2000). Xanthan gum: Production, recovery, and properties. Biotechnology Advances, 18, 549–579.

    CAS  Google Scholar 

  • Ghasemi, Y., Moradian, A., Mohagheghzadeh, A., Shokravi, S., & Morowvat, M. H. (2007). Antifungal and antibacterial activity of the microalgae collected from paddy fields of Iran: Characterization of antimicrobial activity of Chlorococcus dispersus. Journal of Biological Sciences, 7(6), 904–910.

    Google Scholar 

  • Glymph, T. (2005). Wastewater microbiology: A handbook for operators. American Water Works Association, Denver, CO.

  • Golueke, C. G., Oswald, W. J., & Gotaas, H. B. (1957). Anaerobic digestion of algae. Applied and Environmental Biotechnology, 5(1), 47–55.

    CAS  Google Scholar 

  • Gonçalves, A. L., Pires, J. C. M., & Simões, M. (2017). A review on the use of microalgal consortia for wastewater treatment. Algal Research, 24, 403–415.

    Google Scholar 

  • Grzesik, M., Romanowska-Duda, M., & Kalaji, H. M. (2017). Effectiveness of cyanobacteria and green algae in enhancing the photosynthetic performance and growth of willow (Salix viminalis L.) plants under limited synthetic fertilizers application. Photosynthetica, 55(3), 510–521.

    CAS  Google Scholar 

  • Gupta, S. S., Shastri, Y., & Bhartiya, S. (2017). Integrated microalgae biorefinery: Impact of product demand profile and prospect of carbon capture. Biofuels Bioproducts & Biorefining, 11, 1065–1076.

    Google Scholar 

  • Gutzeit, G., Lorch, D., Weber, A., Engels, M., & Neis, U. (2005). Bioflocculent algal–bacterial biomass improves low-cost wastewater treatment. Water Science and Technology, 52(12), 9–18.

    CAS  Google Scholar 

  • Guzman, S., Gato, A., Lamela, M., Freire-Garabal, M., & Calleja, J. (2003). Anti-inflammatory and immunomodulatory activities of polysaccharide from Chlorella stigmatophora and Phaeodactylum tricornutum. Phytotherapy Research, 17(6), 665–670.

    CAS  Google Scholar 

  • Harvey, P. J., Psycha, M., Kokossis, A., Abubakar, A. L., Trivedi, V., Swamy, R., Cowan, A. K., Schroeder, D., Highfield, A., Reinhardt, G., Gartner, S., McNeil, J., Day, P., Brocken, M., Varrie, J. & Ben-Amotz, A. (2012). Glycerol production by halophytic microalgae: Strategy for producing industrial quantities in saline water. 20th European Biomass Conference and Exhibition Proceedings, pp 85–90.

  • Hay, I. D., Rehman, Z. U., Moradali, M. F., Wang, Y., & Rehm, B. H. A. (2013). Microbial alginate production, modification and its applications. Microbiology Biotechnology, 6(6), 637–650.

    CAS  Google Scholar 

  • Hom, E. F. Y., Aiyar, P., Schaeme, D., Mittag, M., & Sasso, S. (2015). A chemical perspective on microalgal–microbial interactions. Trends in Plant Science, 20(11), 689–693.

    CAS  Google Scholar 

  • Hu, Y., Hao, X., van Loosdrecht, M., & Chen, H. (2017). Enrichment of highly settleable microalgal consortia in mixed cultures for effluent polishing and low-cost biomass production. Water Research, 125, 11–22.

    CAS  Google Scholar 

  • Huang, H., Peng, C., Peng, P., Lin, Y., Zhang, X., & Ren, H. (2019). Towards the biofilm characterization and regulation in biological wastewater treatment. Applied Microbiology and Biotechnology, 103, 1115–1129.

    CAS  Google Scholar 

  • Irie, Y., & Parsek, M. R. (2008). Quorum sensing and microbial biofilms. Current Topics in Microbiology and Immunology, 322, 67–84.

    CAS  Google Scholar 

  • Islam, S. T., & Lam, J. S. (2014). Synthesis of bacterial polysaccharide via the Wzx/Wzy-dependent pathway. Canadian Journal of Microbiology, 60, 697–716.

    CAS  Google Scholar 

  • Jia, H., & Yuan, Q. (2016). Removal of nitrogen from wastewater using microalgae and microalgae–bacteria consortia. Cogent Environmental Science, 2, 1275089.

    Google Scholar 

  • Jimoh, T. A., & Cowan, A. K. (2017). Extracellular polymeric substance production in high rate algal oxidation ponds. Water Science and Technology, 76(10), 2647–2654.

    CAS  Google Scholar 

  • Jofré, E., Liaudat, J. P., Medeot, D., & Becker, A. (2018). Monitoring succinoglycan production in single Sinorhizobium meliloti cells by Calcofluor white M2R staining and time-lapse microscopy. Carbohydrate Polymers, 181, 918–922.

    Google Scholar 

  • Jones, K. M. (2012). Increased production of the exopolysaccharide succinoglycan enhances Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. Journal of Bacteriology, 194(16), 4322–4331.

    CAS  Google Scholar 

  • Kaplan, D., Christiaen, D., & Arad, S. (1987). Chelating properties of extracellular polysaccharides from Chlorella spp. Applied and Environmental Microbiology, 53(12), 2953–2956.

    CAS  Google Scholar 

  • Kehr, J. C., & Dittmann, E. (2015). Biosynthesis and function of extracellular glycans in cyanobacteria: A review. Life, 5, 164–180.

    CAS  Google Scholar 

  • Kouzuma, A., & Watanabe, K. (2015). Exploring the potential of algae/bacteria interactions. Current Opinion in Biotechnology, 33, 125–129.

    CAS  Google Scholar 

  • Kunacheva, C., & Stuckey, D. C. (2014). Analytical methods for soluble microbial products (SMP) and extracellular polymers (ECP) in wastewater treatment systems: A review. Water Research, 61, 1–18.

    CAS  Google Scholar 

  • Lakaniemi, A.-M., Tuovinen, O. H., & Puhakka, J. A. (2013). Anaerobic conversion of microalgal biomass to sustainable energy carriers—A review. Bioresource Technology, 135, 222–231.

    CAS  Google Scholar 

  • Leaungvutiviroj, C., Ruangphisarn, P., Hansanimitkul, P., Shinkawa, H., & Sasaki, K. (2010). Development of a new biofertilizer with a high capacity for N2 fixation, phosphate and potassium solubilization and auxin production. Bioscience Biotechnology and Biochemistry, 74(5), 1098–1101.

    CAS  Google Scholar 

  • Li, Y., Xu, Y., Liu, L., Jiang, X., Zhang, K., Zheng, T., & Wang, H. (2016). First evidence of bioflocculant from Shinella albus with flocculation activity on harvesting of Chlorella vulgaris biomass. Bioresource Technology, 218, 807–815.

    CAS  Google Scholar 

  • Li, Y., Xu, Y., Zheng, T., & Wang, H. (2017). Flocculation mechanism of the actinomycete Streptomyces sp. hsn06 on Chlorella vulgaris. Bioresource Technology, 239, 137–143.

    CAS  Google Scholar 

  • Li, Y., Xu, Y., Song, R., Tian, C., Liu, L., Zheng, T., & Wang, H. (2018). Flocculation characteristics of a bioflocculant produced by the actinomycete Streptomyces sp. hsn06 on microalgae biomass. BMC Biotechnology, 18, 58. https://doi.org/10.1186/s12896-018-0471-9.

    Article  CAS  Google Scholar 

  • Mambo, P. M., Westensee, D. K., Render, D. S., & Cowan, A. K. (2014a). Operation of an integrated algae pond system for the treatment of municipal sewage: A South African case study. Water Science and Technology, 69(12), 2554–2561.

    CAS  Google Scholar 

  • Mambo, P. M., Westensee, D. K., Zuma, B. M., & Cowan, A. K. (2014b). The Belmont Valley integrated algae pond system in retrospect. Water SA, 40(2), 385–393.

    Google Scholar 

  • Medina, M., & Neis, U. (2007). Symbiotic algal bacterial wastewater treatment: Effect of food to microorganism ratio and hydraulic retention time on the process performance. Water Science and Technology, 55(11), 165–171.

    CAS  Google Scholar 

  • Mehrabadi, A., Craggs, R., & Farid, M. M. (2015). Wastewater treatment high rate algal ponds (WWT HRAP) for low-cost biofuel production. Bioresource Technology, 184, 202–214.

    CAS  Google Scholar 

  • Mehrabadi, A., Farid, M. M., & Craggs, R. (2016). Variation of biomass energy yield in wastewater treatment high rate algal ponds. Algal Research, 15, 143–151.

    Google Scholar 

  • Mendez, L., Mahdy, A., Ballesteros, M., & González-Fernández, C. (2015). Chlorella vulgaris vs cyanobacterial biomasses: Comparison in terms of biomass productivity and biogas yield. Energy Conversion and Management, 92, 137–142.

    CAS  Google Scholar 

  • Milledge, J. J., & Heaven, S. (2014). Methods of energy extraction from microalgal biomass: A review. Reviews in Environmental Science and Biotechnology, 13, 301–320.

    CAS  Google Scholar 

  • Mishra, A., & Jha, B. (2009). Isolation and characterization of extracellular polymeric substances from microalgae Dunaliella salina under salt stress. Bioresource Technology, 100, 3382–3386.

    CAS  Google Scholar 

  • Moosavi-Nasab, M., Gavahian, M., Yousefi, A. R., & Askari, H. (2010). Fermentative production of dextran using food industry wastes. International Journal of Nutrition and Food Engineering, 4(8), 1921–1923.

    Google Scholar 

  • More, T. T., Yadav, J. S. S., Yan, S., Tyagi, R. D., & Surampalli, R. Y. (2014). Extracellular polymeric substances of bacteria and their potential environmental applications. Journal of Environmental Management, 144, 1–25.

    CAS  Google Scholar 

  • Morris, G. & Harding, S. E. (2009). Polysaccharides, microbial. In: Encyclopedia of microbiology (third edition). Elsevier, 482–494. ISBN 9780123739445.

  • Natrah, F. M. I., Bossier, P., Sorgeloos, P., Yusoff, F. M., & Defoirdt, T. (2013). Significance of microalgal–bacterial interactions for aquaculture. Reviews in Aquaculture, 5, 1–14.

    Google Scholar 

  • Neu, T. R., & Marshall, K. C. (1991). Microbial “footprint”—A new approach to adhesive polymers. Biofouling, 3, 101–112.

    Google Scholar 

  • Nguyen, V. H., Nguyen, H. K., Nguyen, T. D., Pham, T., Dang-Thi, C. H., Song, Y., & Tyagi, R. D. (2017). Sources for isolation of extracellular polymeric substances (EPS) producing bacterial strains which are capable using wastewater sludge as solo substrate. Environmental Technology, 21, 1–10. https://doi.org/10.1080/09593330.2017.1351488.

    Article  CAS  Google Scholar 

  • Nouha, K., Hoang, N. V., Song, Y., Tagi, R. D., & Surampalli, R. Y. (2015). Characterization of extracellular polymeric substances (EPS) produced by Cloacibacterium normanense isolated from wastewater sludge for sludge settling and dewatering. Journal of Civil and Environmental Engineering, 5, 191. https://doi.org/10.4172/2165-784X.1000191.

    Article  Google Scholar 

  • O’Donnell, D. R., Fey, S. B., & Cottingham, K. L. (2013). Nutrient availability influences kairomone-induced defenses in Scenedesmus acutus (Chlorophyceae). Journal of Plankton Research, 35(1), 191–200.

    Google Scholar 

  • Orellana, M. V., Pang, W. L., Durand, P. M., Whitehead, K., & Baliga, N. S. (2013). A role for programmed cell death in the microbial loop. PLoS One, 8(5), e62595.

    CAS  Google Scholar 

  • Oswald, W. J. (1990). Advanced integrated wastewater pond systems. In: Supplying water and saving the environment for six billion people: Proceedings of the 1990 ASCE convention, San Francisco, California, November. New York, American Society of Civil Engineers, Environmental Engineering Division. Pp. 78–85.

  • Oswald, W. J. (1991). Introduction to advanced wastewater ponding systems. Water Science and Technology, 24(5), 1–7.

    CAS  Google Scholar 

  • Oswald, W. J. (1995). Ponds in the twenty-first century. Water Science and Technology, 31(12), 1–8.

    CAS  Google Scholar 

  • Oswald, W. J., Gotaas, H. B., Ludwig, H. F., & Lynch, V. (1953). Algae symbiosis in oxidation ponds II: Growth characteristics of Chlorella pyrenoidosa cultured in sewage. Sewage and Industrial Wastes, 25, 26–37.

    CAS  Google Scholar 

  • Oswald, W. J., Gotaas, H. B., Golueke, C. G., Kellen, W. R., Gloyna, E. F., & Hermann, E. R. (1957). Algae in waste treatment [with discussion]. Sewage and Industrial Wastes, 29(4), 437–457.

    Google Scholar 

  • Palaniraj, A., & Jayaraman, V. (2011). Production, recovery and applications of xanthan gum by Xanthomonas campestris. Journal of Food Engineering, 106, 1–12.

    CAS  Google Scholar 

  • Parikh, A., & Madamwar, D. (2006). Partial characterization of extracellular polysaccharides from cyanobacteria. Bioresource Technology, 97, 1822–1827.

    CAS  Google Scholar 

  • Park, J. B. K., Craggs, R. J., & Shilton, A. N. (2011). Wastewater treatment high rate algal ponds for biofuel production. Bioresource Technology, 102, 35–42.

    CAS  Google Scholar 

  • Passos, F., Sole, M., Garcia, J., & Ferrer, I. (2013). Biogas production from microalgae grown in wastewater: Effect of microwave pretreatment. Applied Energy, 108, 168–175.

    CAS  Google Scholar 

  • Passos, F., Gutiérrez, R., Uggetti, E., Garfi, M., García, J., & Ferrer, I. (2017). Towards energy neutral microalgae-based wastewater treatment plants. Algal Research, 28, 235–243.

    Google Scholar 

  • Peng, Y., Gao, C., Wang, S., Ozaki, M., & Takigawa, A. (2003). Non-filamentous sludge bulking caused by a deficiency of nitrogen in industrial wastewater treatment. Water Science and Technology, 47(11), 289–295.

    CAS  Google Scholar 

  • Phasey, J., Vandamme, D., & Fallowfield, H. J. (2017). Harvesting of algae in municipal wastewater treatment by calcium phosphate precipitation mediated by photosynthesis, sodium hydroxide and lime. Algal Research, 27, 115–120.

    Google Scholar 

  • Picheth, G. F., Pirich, C. L., Sierakowski, M. R., Woehl, M. A., Sakakibara, C. N., de Souza, C. F., Martin, A. A., da Silva, R., & Freitas, R. A. (2017). Bacterial cellulose in biomedical applications: A review. International Journal of Biological Macromolecules, 104, 97–106.

    CAS  Google Scholar 

  • Poli, A., Donato, P. D., Abbamondi, G. R. & Nicolaus, B. (2011). Synthesis, production and biotechnological applications of exopolysaccharides and polyhydroxyalkanoates by archaea. Archaea, 2011, article ID 693253, 13 pages. https://doi.org/10.1155/2011/693253 .

    Google Scholar 

  • Prajapati, S. K., Kaushik, P., Malik, A., & Vijay, V. K. (2013). Phycoremediation and biogas potential of native algal isolates from soil and wastewater. Bioresource Technology, 135, 232–238.

    CAS  Google Scholar 

  • Psycha, M., Pyrgakis, K., Harvey, P. J., Ben-Amotz, A., Cowan, A. K., & Kokossis, A. C. (2014). Design analysis of integrated microalgae biorefineries. Computer Aided Chemical Engineering, 34, 591–596.

    CAS  Google Scholar 

  • Quijano, G., Arcilaa, J. S., & Buitrón, G. (2017). Microalgal–bacterial aggregates: Applications and perspectives for wastewater treatment. Biotechnology Advances, 35, 772–781.

    CAS  Google Scholar 

  • Ramanan, R., Kim, B.-H., Cho, D.-H., Oh, H.-M., & Kim, H.-S. (2016). Algae–bacteria interactions: Evolution, ecology and emerging applications. Biotechnology Advances, 34, 14–29.

    CAS  Google Scholar 

  • Rose, P., Maart, B., Dunn, K., Rowswell, R., & Britz, P. (1996). High rate algal oxidation ponding for the treatment of tannery effluents. Water Science and Technology, 33, 219–227.

    CAS  Google Scholar 

  • Rose, P., Boshoff, G., Van Hille, R., Wallace, L., Dunn, K., & Duncan, J. (1998). An integrated algal sulphate reducing high rate ponding process for the treatment of acid mine drainage wastewaters. Biodegradation, 9, 247–257.

    CAS  Google Scholar 

  • Rosselló-Mora, R. A., Wagner, M., Amann, R., & Schleifer, K.-H. (1995). The abundance of Zoogloea ramigera in sewage treatment plants. Applied and Environmental Microbiology, 61(2), 702–707.

    Google Scholar 

  • Rossi, F., & De Philippis, R. (2015). Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life, 5, 1218–1238.

    CAS  Google Scholar 

  • Rühmann, B., Schmid, J., & Sieber, V. (2015). Methods to identify the unexplored diversity of microbial exopolysaccharides. Frontiers in Microbiology, 6(565). https://doi.org/10.3389/fmicb.2015.00565.

  • Sarwat, F., Qader, S. A. U., Aman, A., & Ahmed, N. (2008). Production & characterization of a unique dextran from an indigenous Leuconostoc mesenteroides CMG713. International Journal of Biological Sciences, 4(6), 379–386.

    CAS  Google Scholar 

  • Schlafer, S., & Meyer, R. L. (2017). Confocal microscopy imaging of the biofilm matrix. Journal of Microbiological Methods, 138, 50–59.

    Google Scholar 

  • Schmid, J., Sieber, V. & Rehm, B. (2015). Bacterial exopolysaccharides: Biosynthesis pathways and engineering strategies. Frontier in Microbiology, 6 (496). doi: https://doi.org/10.3389/fmicb.2015.00496.

  • Sfez, S., Van Den Hende, S., Taelman, S. E., De Meester, S., & Dewulf, J. (2015). Environmental sustainability assessment of a microalgae raceway pond treating aquaculture wastewater: From up-scaling to system integration. Bioresource Technology, 190, 321–331.

    CAS  Google Scholar 

  • Sheng, G.-P., Yu, H.-Q., & Li, X.-Y. (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: A review. Biotechnology Advances, 28, 882–894.

    CAS  Google Scholar 

  • Shi, Y., Huang, J., Zeng, G., Gu, Y., Chen, Y., Hu, Y., Tang, B., Zhou, J., Yang, Y., & Shi, L. (2017). Exploiting extracellular polymeric substances (EPS) controlling strategies for performance enhancement of biological wastewater treatments: An overview. Chemosphere, 180, 396–411.

    CAS  Google Scholar 

  • Shih, I. L., Yu, J. Y., Hsieh, C., & Wu, J. Y. (2009). Production and characterization of curdlan by Agrobacterium sp. Biochemical Engineering Journal, 43, 33–40.

    CAS  Google Scholar 

  • Singh, J. S., Kumar, A., Rai, A. N., & Singh, D. P. (2016). Cyanobacteria: A precious bio-resource in agriculture, ecosystem, and environmental sustainability. Frontiers in Microbiology, 7, 529.

    Google Scholar 

  • Singha, T. K. (2012). Microbial extracellular polymeric substances: Production, isolation and applications. IOSR Journal of Pharmacy, 2(2), 276–281.

    Google Scholar 

  • Sobeck, D. C., & Higgins, M. J. (2002). Examination of three theories for mechanisms of cation-induced bioflocculation. Water Research, 36, 527–538.

    CAS  Google Scholar 

  • Spolaore, P., Joannis-Cassan, C., Duran, E., & Isambet, A. (2006). Commercial applications of microalgae. Journal of Bioscience and Bioengineering, 101(2), 87–96.

    CAS  Google Scholar 

  • Subashchandrabose, S. R., Ramakrishnan, B., Megharaj, M., Venkateswarlu, K., & Naidu, R. (2011). Consortia of cyanobacteria/microalgae and bacteria: Biotechnological potential. Biotechnology Advances, 29, 896–907.

    CAS  Google Scholar 

  • Sugumaran, K. R., & Ponnusami, V. (2017). Review on production, downstream processing and characterization of microbial pullulan. Carbohydrate Polymers, 173, 573–591.

    CAS  Google Scholar 

  • Survase, S. A., Saudagar, P. S., & Singhal, R. S. (2007). Enhanced production of scleroglucan by Sclerotium rolfsii MTCC 2156 by use of metabolic precursors. Bioresource Technology, 98, 410–415.

    CAS  Google Scholar 

  • Sutherland, I. W. (2001). The biofilm matrix—an immobilized but dynamic microbial environment. Trends in Microbiology, 9(3), 222–227.

    CAS  Google Scholar 

  • Sutherland, D. L., Howard-Williams, C., Turnbull, M. H., Broady, P. A., & Craggs, R. J. (2013). Seasonal variation in light utilisation, biomass production and nutrient removal by wastewater microalgae in a full-scale high rate algal pond. Journal of Applied Phycology, 26(3), 1317–1329.

    Google Scholar 

  • Sutherland, D. L., Howard-Williams, C., Turnbull, M. H., Broady, P. A., & Craggs, R. J. (2015). Enhancing microalgal photosynthesis and productivity in wastewater treatment high rate algal ponds for biofuel production. Bioresource Technology, 184, 222–229.

    CAS  Google Scholar 

  • Sze, J. H., Brownlie, J. C., & Love, C. A. (2016). Biotechnological production of hyaluronic acid: A mini review. 3 Biotech, 6, 67(1). https://doi.org/10.1007/s13205-016-0379-9.

  • Theocharis, A. D., Skandalis, S. S., Gialeli, C., & Karamanos, N. K. (2016). Extracellular matrix structure. Advanced Drug Delivery Reviews, 97, 4–27.

    CAS  Google Scholar 

  • Tiron, O., Bumbac, C., Manea, E., Stefanescu, M., & Lazar, M. N. (2017). Overcoming microalgae harvesting barrier by activated algae granules. Scientific Reports, 7, 4646.

    Google Scholar 

  • Tourney, J., & Ngwenya, B. T. (2014). The role of bacterial extracellular polymeric substances in geomicrobiology. Chemical Geology, 386, 115–132.

    CAS  Google Scholar 

  • Trabelsi, I., Slima, S. B., Chaabane, H., & Riadh, B. S. (2015). Purification and characterization of a novel exopolysaccharides produced by Lactobacillus sp. Ca6. International Journal of Biological Macromolecules, 74, 541–546.

    CAS  Google Scholar 

  • Trabelsi, I., Ktari, N., Slima, S. B., Triki, M., Bardaa, S., Mnif, H., & Salah, R. B. (2017). Evaluation of dermal wound healing activity and in vitro antibacterial and antioxidant activities of a new exopolysaccharide produced by Lactobacillus sp. Ca6. International Journal of Biological Macromolecules, 103, 194–201.

    CAS  Google Scholar 

  • Trivedi, J., Mounika, A., Bangwal, D. P., Kaul, S., & Garg, M. O. (2015). Algae based biorefinery—how to make sense? Renewable and Sustainable Energy Reviews, 47, 295–307.

    CAS  Google Scholar 

  • Tseng, B. S., Majerczyk, C. D., Passos da Silva, D., Chandler, J. R., Greenberg, E. P., & Parsek, M. R. (2016). Quorum sensing influences Burkholderia thailandensis biofilm development and matrix production. Journal of Bacteriology, 198(19), 2643–2650. https://doi.org/10.1128/JB.00047-16.

    Article  CAS  Google Scholar 

  • Turtin, I., Vatansever, A., & Sanin, F. D. (2006). Phosphorus defficiency and sludge bulking. Environmental Technology, 27(6), 613–621.

    CAS  Google Scholar 

  • Ummalyma, S. B., Gnansounou, E., Sukumaran, R. K., Sindhu, R., Pandey, A., & Sahoo, D. (2017). Bioflocculation: An alternative strategy for harvesting of microalgae—An overview. Bioresource Technology, 242, 227–235.

    CAS  Google Scholar 

  • Unc, A., Monfet, E., Potter, A., Camargo-Valero, M. A., & Smith, S. R. (2017). Note to editor: Microalgae cultivation for wastewater treatment and biofuel production: A bibliographic overview of past and current trends. Algal Research, 24, A2–A7.

    Google Scholar 

  • Urtuvia, V., Maturana, N., Acevedo, F., Peña, C., & Díaz-Barrera, A. (2017). Bacterial alginate production: An overview of its biosynthesis and potential industrial production. World Journal of Microbiology and Biotechnology, 33(11), 198. https://doi.org/10.1007/s11274-017-2363-x.

    Article  CAS  Google Scholar 

  • Van Den Hende, S., Vervaeren, H., Saveyn, H., Maes, G., & Boon, N. (2011). Microalgal bacterial floc properties are improved by a balanced inorganic/organic carbon ratio. Biotechnology and Bioengineering, 108(3), 549–558.

    Google Scholar 

  • Van Den Hende, S., Carré, E., Cocaud, E., Beelen, V., Boon, N., & Vervaeren, H. (2014a). Treatment of industrial wastewaters by microalgal bacterial flocs in sequencing batch reactors. Bioresource Technology, 161, 245–254.

    Google Scholar 

  • Van Den Hende, S., Claessens, L., De Muylder, E., Boon, N., & Vervaeren, H. (2014b). Microalgal bacterial flocs originating from aquaculture wastewater treatment as diet ingredient for Litopenaeus vannamei (Boone). Aquaculture Research, 47(4), 1075–1089.

    Google Scholar 

  • Van Den Hende, S., Laurent, C., & Bégué, M. (2015). Anaerobic digestion of microalgal bacterial flocs from a raceway pond treating aquaculture wastewater: Need for a biorefinery. Bioresource Technology, 196, 184–193.

    Google Scholar 

  • Van Den Hende, S., Beelen, V., Julien, L., Lefoulon, A., Vanhoucke, T., Coolsaet, C., Sonnenholzner, S., Vervaeren, H., & Rousseau, D. P. L. (2016a). Technical potential of microalgal bacterial floc raceway ponds treating food-industry effluents while producing microalgal bacterial biomass: An outdoor pilot-scale study. Bioresource Technology, 218, 969–979.

    Google Scholar 

  • Van Den Hende, S., Beyls, J., De Buyck, P.-J., & Rousseau, D. P. L. (2016b). Food-industry-effluent-grown microalgal bacterial flocs as a bioresource for high-value phycochemicals and biogas. Algal Research, 18, 25–32.

    Google Scholar 

  • Van Hille, R. P., Boshoff, G. A., Rose, P. D., & Duncan, J. R. (1999). A continuous process for the biological treatment of heavy metal contaminated acid mine water. Resources Conservation and Recycling, 27, 157–167.

    Google Scholar 

  • Vandamme, D., Foubert, I., & Muylaert, K. (2013). Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends in Biotechnology, 31(4), 233–239.

    CAS  Google Scholar 

  • Vanthoor-Koopmans, M., Wijffels, R. H., Barbosa, M. J., & Eppink, M. H. M. (2013). Biorefinery of microalgae for food and fuel. Bioresource Technology, 135, 142–149.

    CAS  Google Scholar 

  • Vázquez, J. A., Pastrana, L., Piñeiro, C., Teixeira, J. A., Pérez-Martín, R. I., & Amado, I. R. (2015). Production of hyaluronic acid by Streptococcus zooepidemicus on protein substrates obtained from Scyliorhinus canicula discards. Marine Drugs, 13, 6537–6549.

    Google Scholar 

  • Wan, C., Zhao, X.-Q., Guo, S.-L., Alam, M. A., & Bai, F.-W. (2013). Bioflocculant production from Solibacillus silvestris W01 and its application in cost-effective harvest of marine microalga Nannochloropsis oceanica by flocculation. Bioresource Technology, 135, 207–212.

    CAS  Google Scholar 

  • Wan, C., Alam, M. A., Zhao, X.-Q., Zhang, X.-Y., Guo, S.-L., Ho, S.-H., Chang, J.-S., & Bai, F.-W. (2015). Current progress and future prospect of microalgal biomass harvest using various flocculation technologies. Bioresource Technology, 184, 251–257.

    CAS  Google Scholar 

  • Wang, Z.-P., & Zhang, T. (2010). Characterization of soluble microbial products (SMP) under stressful conditions. Water Research, 44, 5499–5509.

    CAS  Google Scholar 

  • Wang, H., Hill, R. T., Zheng, T., Hu, X., & Wang, B. (2014). Effects of bacterial communities on biofuel-producing microalgae: Stimulation, inhibition and harvesting. Critical Reviews in Biotechnology, 36(2), 341–352.

    Google Scholar 

  • Wang, Z., Wu, J., Zhu, L., & Zhan, X. (2017). Characterization of xanthan gum produced from glycerol by a mutant strain Xanthomonas campestris CCTCC M2015714. Carbohydrate Polymers, 157, 521–526.

    CAS  Google Scholar 

  • West, T. P., & Peterson, J. L. (2014). Production of the polysaccharide curdlan by an Agrobacterium strain grown on a plant biomass hydrolysate. Canadian Journal of Microbiology, 60, 53–56.

    CAS  Google Scholar 

  • Wieczorek, N., Kucuker, M. A., & Kuchta, K. (2015). Microalgae–bacteria flocs (MaB-flocs) as a substrate for fermentative biogas production. Bioresource Technology, 194, 130–136.

    CAS  Google Scholar 

  • Wingender, J., Neu, T. R., & Flemming, H.-C. (1999). What are bacterial extracellular polymeric substances? In J. Wingender, T. Neu, & H.-C. Flemming (Eds.), Microbial extracellular polymeric substances (pp. 1–19). Heidelberg: Springer.

    Google Scholar 

  • Xiao, R., & Zheng, Y. (2016). Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnology Advances, 34, 1225–1244.

    CAS  Google Scholar 

  • Young, P., Taylor, M., & Fallowfield, H. J. (2017). Mini-review: High rate algal ponds, flexible systems for sustainable wastewater treatment. World Journal of Microbiology and Biotechnology, 33(6), 117–129.

    CAS  Google Scholar 

  • Yu, L., Wu, J., Liu, J., Zhan, X., Zheng, Z., & Lin, C. C. (2011). Enhanced curdlan production in Agrobacterium sp. ATCC 31749 by addition of low-polyphosphates. Biotechnology and Bioprocess Engineering, 16, 34–41.

    CAS  Google Scholar 

  • Zhu, L. (2015). Biorefinery as a promising approach to promote microalgae industry: An innovative framework. Renewable and Sustainable Energy Reviews, 41, 1376–1384.

    Google Scholar 

  • ZoBell, C. E. (1943). The effect of solid surfaces upon bacterial activity. Journal of Bacteriology, 46, 39–56.

    CAS  Google Scholar 

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Funding

The research was funded by Rhodes University and a grant from the Water Research Commission (WRC) of South Africa through WRC Project No. 7164 awarded to A.K.C. of Rhodes University. T.A.J. and O.K. acknowledge receipt of doctoral bursaries from EBRU.

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Jimoh, T.A., Keshinro, M.O. & Cowan, K.A. Microalgal–Bacterial Flocs and Extracellular Polymeric Substances: Two Essential and Valuable Products of Integrated Algal Pond Systems. Water Air Soil Pollut 230, 95 (2019). https://doi.org/10.1007/s11270-019-4148-3

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