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Physiology of microalgal biofilm: a review on prediction of adhesion on substrates

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Pages 7577-7599 | Received 17 Aug 2021, Accepted 10 Sep 2021, Published online: 04 Oct 2021

References

  • Chai WS, Tan WG, Halimatul Munawaroh HS, et al. Multifaceted roles of microalgae in the application of wastewater biotreatment: a review. Environ Pollut. 2021;269:116236.
  • Bolognesi S, Bernardi G, Callegari A, et al. Biochar production from sewage sludge and microalgae mixtures: properties, sustainability and possible role in circular economy. Biomass Convers Biorefin. 2021;11:289-299. https://www.springerprofessional.de/en/biochar-production-from-sewage-sludge-and-microalgae-mixtures-pr/17521990
  • Low SS, Bong KX, Mubashir M, et al. Microalgae cultivation in palm oil mill effluent (POME) treatment and biofuel production. Sustainability. 2021; 13.
  • Davis R, Aden A, Pienkos PT. Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energy. 2011;88(10):3524–3531.
  • Podola B, Li T, Melkonian M. Porous substrate bioreactors: a paradigm shift in microalgal biotechnology. Trends Biotechnol. 2017;35(2):121–132.
  • Chisti Y. Biodiesel from microalgae. Biotechnol Adv. 2007;25:294–306.
  • Christenson LB, Sims RC. Rotating algal biofilm reactor and spool harvester for wastewater treatment with biofuels by-products. Biotechnol Bioeng. 2012;109(7):1674–1684.
  • Sekar R, Venugopalan VP, Satpathy KK, et al. Laboratory studies on adhesion of microalgae to hard substrates. In: Ang PO, editors. Asian pacific phycology in the 21st century: prospects and challenges. Dordrecht: Springer Netherlands; 2004. p. 109–116.
  • Gómez Ramírez A, Enríquez-Ocaña L, Miranda-Baeza A, et al. Biofilm-forming capacity of two benthic microalgae, Navicula incerta and Navicula sp., on three substrates (Naviculales: naviculaceae). Rev Biol Trop. 2019;67:599–607.
  • Zhang X, Yuan H, Jiang Z, et al. Impact of surface tension of wastewater on biofilm formation of microalgae Chlorella sp. Bioresour Technol. 2018;266:498–506.
  • Becker K. Exopolysaccharide production and attachment strength of bacteria and diatoms on substrates with different surface tensions. Microb Ecol. 1996;32(1):23–33.
  • Melo M, Fernandes S, Caetano N, et al. Chlorella vulgaris (SAG 211-12) biofilm formation capacity and proposal of a rotating flat plate photobioreactor for more sustainable biomass production. J Appl Phycol. 2017;30(2):887–899.
  • Shen Y, Zhang H, Xu X, et al. Biofilm formation and lipid accumulation of attached culture of Botryococcus braunii. Bioprocess Biosyst Eng. 2015;38(3):481–488.
  • Craggs RJ, Adey WH, Jenson KR, et al. Phosphorus removal from wastewater using an algal turf scrubber. Water Sci Technol. 1996;33(7):191–198.
  • Leadbeater BSC, Callow ME. Formation, composition and physiology of algal biofilms. In: Melo LF, Bott TR, Fletcher M, et al, editors. Biofilms — science and technology. Dordrecht: Springer Netherlands; 1992. p. 149–162.
  • Watnick P, Kolter R. Biofilm, city of microbes. J Bacteriol. 2000;182(10):2675–2679.
  • Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623–633.
  • Sehar S, Naz I. Role of the biofilms in wastewater treatment. In: Dhanasekaran D, Thajuddin N, editors. Microbial biofilms: importance and applications. Germany: Books on Demand; 2016. p. 121–144.
  • Schnurr PJ, Allen DG. Factors affecting algae biofilm growth and lipid production: a review. Renew Sustain Energ Rev. 2015;52:418–429.
  • Christenson L, Sims R. Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv. 2011;29(6):686–702.
  • Cooksey KE. Extracellular polymers in biofilms. In: Melo LF, Bott TR, Fletcher M, et al, editors. Biofilms - science and technology. Dordrecht: Springer Netherlands; 1992. p. 137–147.
  • Xiao R, Zheng Y. Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv. 2016;34(7):1225–1244.
  • Parker C. The effects of environmental stressors on biofilm formation of Chlorella vulgaris. Appalachian State University, 2013.
  • Li N, Liu J, Yang R, et al. Distribution, characteristics of extracellular polymeric substances of Phanerochaete chrysosporium under lead ion stress and the influence on Pb removal. Sci Rep. 2020;10(1):17633.
  • Li Y, Xin M, Xie D, et al. Variation in Extracellular Polymeric Substances from Enterobacter sp. and Their Pb2+ Adsorption Behaviors. ACS Omega. 2021;6(14):9617–9628.
  • Babiak W, Krzemińska I. Extracellular polymeric substances (EPS) as microalgal bioproducts: a review of factors affecting EPS synthesis and application in flocculation processes. Energies. 2021;14.
  • Xing R-L, Ma W-W, Shao Y-W, et al. Growth and potential purification ability of Nitzschia sp. benthic diatoms in sea cucumber aquaculture wastewater. Aquac Res. 2018;49(8):2644–2652.
  • Li XZ, Hauer B, Rosche B. Single-species microbial biofilm screening for industrial applications. Appl Microbiol Biotechnol. 2007;76(6):1255–1262.
  • Wang J, Liu W, Liu T. Biofilm based attached cultivation technology for microalgal biorefineries-A review. Bioresour Technol. 2017;244:1245–1253.
  • Shen Y, Xu X, Zhao Y, et al. Influence of algae species, substrata and culture conditions on attached microalgal culture. Bioprocess Biosyst Eng. 2014;37(3):441–450.
  • Muhlenbruch M, Grossart HP, Eigemann F, et al. Mini-review: phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20(8):2671–2685.
  • Durham B, Sharma S, Luo H, et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proceedings of the National Academy of Sciences. 2014:1–5.
  • Gärdes A, Ramaye Y, Grossart H-P PU. Effects of marinobacter adhaerens HP15 on polymer exudation by Thalassiosira weissflogii at different N:P ratios. Mar Ecol Prog Ser. 2012;461:1–14.
  • Traving SJ, Thygesen UH, Riemann L, et al. A model of extracellular enzymes in free-living microbes: which strategy pays off? Appl Environ Microbiol. 2015;81(21):7385–7393.
  • Koedooder C, Stock W, Willems A, et al. Diatom-bacteria interactions modulate the composition and productivity of benthic diatom biofilms. Front Microbiol. 2019;10:1255.
  • Schnurr PJ, Molenda O, Edwards E, et al. Improved biomass productivity in algal biofilms through synergistic interactions between photon flux density and carbon dioxide concentration. Bioresour Technol. 2016;219:72–79.
  • Dora A, Immacolata G, Gabriele P, et al. Evaluating microalgae attachment to surfaces a first approach towards a laboratory integrated assessment. Chem Eng Trans. 2017;57.
  • Tong CY, Derek CJC. Biofilm formation of benthic diatoms on commercial polyvinylidene fluoride membrane. Algal Res. 2021;55:102260.
  • Rincon SM, Romero HM, Aframehr WM, et al. Biomass production in Chlorella vulgaris biofilm cultivated under mixotrophic growth conditions. Algal Res. 2017;26:153–160.
  • Shen Y, Chen C, Chen W, et al. Attached culture of Nannochloropsis oculata for lipid production. Bioprocess Biosyst Eng. 2014;37(9):1743–1748.
  • Cheng P, Wang Y, Liu T, et al. Biofilm attached cultivation of Chlorella pyrenoidosa is a developed system for swine wastewater treatment and lipid production. Front Plant Sci. 2017;8:1594.
  • Gao F, Yang ZH, Li C, et al. A novel algal biofilm membrane photobioreactor for attached microalgae growth and nutrients removal from secondary effluent. Bioresour Technol. 2015;179:8–12.
  • Gross M, Henry W, Michael C, et al. Development of a rotating algal biofilm growth system for attached microalgae growth with in situ biomass harvest. Bioresour Technol. 2013;150:195–201.
  • Blanken W, Janssen M, Cuaresma M, et al. Biofilm growth of Chlorella sorokiniana in a rotating biological contactor based photobioreactor. Biotechnol Bioeng. 2014;111(12):2436–2445.
  • Johnson MB, Wen Z. Development of an attached microalgal growth system for biofuel production. Appl Microbiol Biotechnol. 2010;85(3):525–534.
  • Mulbry W, Kondrad S, Pizarro C, et al. Treatment of dairy manure effluent using freshwater algae: algal productivity and recovery of manure nutrients using pilot-scale algal turf scrubbers. Bioresour Technol. 2008;99(17):8137–8142.
  • Hodges A, Fica Z, Wanlass J, et al. Nutrient and suspended solids removal from petrochemical wastewater via microalgal biofilm cultivation. Chemosphere. 2017;174:46–48.
  • Orandi S, Lewis DM, Moheimani NR. Biofilm establishment and heavy metal removal capacity of an indigenous mining algal-microbial consortium in a photo-rotating biological contactor. J Ind Microbiol Biotechnol. 2012;39(9):1321–1331.
  • Zhang D, Fung KY, Ng KM. Novel filtration photobioreactor for efficient biomass production. Ind Eng Chem Res. 2014;53(33):12927–12934.
  • Liu T, Wang J, Hu Q, et al. Attached cultivation technology of microalgae for efficient biomass feedstock production. Bioresour Technol. 2013;127:216–222.
  • Schultze LKP, Simon M-V, Li T, et al. High light and carbon dioxide optimize surface productivity in a twin-layer biofilm photobioreactor. Algal Res. 2015;8:37–44.
  • Murphy TE, Berberoglu H. Flux balancing of light and nutrients in a biofilm photobioreactor for maximizing photosynthetic productivity. Biotechnol Prog. 2014;30(2):348–359.
  • Ji C, Wang J, Zhang W, et al. An applicable nitrogen supply strategy for attached cultivation of Aucutodesmus obliquus. J Appl Phycol. 2013;26(1):173–180.
  • Boelee NC, Janssen M, Temmink H, et al. The effect of harvesting on biomass production and nutrient removal in phototrophic biofilm reactors for effluent polishing. J Appl Phycol. 2013;26(3):1439–1452.
  • Toninelli E, Wang J, Liu M, et al. Scenedesmus dimorphus biofilm: photoefficiency and biomass production under intermittent lighting. Sci Rep. 2016;6(1):32305.
  • Urbain V, Block JC, Manem J. Bioflocculation in activated sludge: an analytic approach. Water Res. 1993;27(5):829–838.
  • Jin C, Yu Z, Peng S, et al. The characterization and comparison of exopolysaccharides from two benthic diatoms with different biofilm formation abilities. An Acad Bras Cienc. 2018;90(2):1503–1519.
  • Bhosle NB, Sawant SS, Garg A, et al. Chemical characterization of exopolysaccharides from the marine fouling diatom Amphora coffeaeformis. Biofouling. 1996;10(4):301–307.
  • Templeton DW, Quinn M, Van Wychen S, et al. Separation and quantification of microalgal carbohydrates. J Chromatogr A. 2012;1270:225–234.
  • Decho A. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr Mar Biol Ann Rev. 1990;28:73–154.
  • Lembre P, Lorentz C, Di P. Exopolysaccharides of the biofilm matrix: a complex biophysical world. In: Karunaratne DN, editor. The complex world of polysaccharides. Germany: Books on Demand; 2012. p. 371–392.
  • Bhosle NB, Sawant SS, Garg A, et al. Isolation and partial chemical analysis of exopolysaccharides from the marine fouling diatom Navicula subinflata. Botanica Marina. 1995;38(1–6):103–110
  • Van Wychen S, Laurens LML. Total carbohydrate content determination of microalgal biomass by acid hydrolysis followed by spectrophotometry or liquid chromatography. Methods Mol Biol. 2020;1980:191–202.
  • Daniel GF, Chamberlain AHL, Jones EBG. Cytochemical and electron microscopical observations on the adhesive materials of marine fouling diatoms. Br Phycol J. 2007;22(2):101–118.
  • Decho AW, Lopez GR. Exopolymer microenvironments of microbial flora: multiple and interactive effects on trophic relationships. Limnol Oceanol. 1993;38(8):1633–1645
  • Pan M, Zhu L, Chen L, et al. Detection techniques for extracellular polymeric substances in biofilms: a review. Bioresources. 2016;11(3):8092–8115.
  • Denkhaus E, Meisen S, Telgheder U, et al. Chemical and physical methods for characterisation of biofilms. Microchim Acta. 2007;158(1–2):1–27.
  • Karunakaran E, Mukherjee J, Ramalingam B, et al. “Biofilmology”: a multidisciplinary review of the study of microbial biofilms. Appl Microbiol Biotechnol. 2011;90(6):1869–1881.
  • Patel AK, Laroche C, Marcati A, et al. Separation and fractionation of exopolysaccharides from Porphyridium cruentum. Bioresour Technol. 2013;145:345–350.
  • Henderson RK, Baker A, Parsons SA, et al. Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms. Water Res. 2008;42(13):3435–3445.
  • Alishah Aratboni H, Rafiei N, Garcia-Granados R, et al. Biomass and lipid induction strategies in microalgae for biofuel production and other applications. Microb Cell Fact. 2019;18(1):178.
  • Boonchai R, Kaewsuk J, Seo G. Effect of nutrient starvation on nutrient uptake and extracellular polymeric substance for microalgae cultivation and separation. Desalination Water Treat. 2014;55(2):360–367.
  • Wang M, Kuo-Dahab WC, Dolan S, et al. Kinetics of nutrient removal and expression of extracellular polymeric substances of the microalgae, Chlorella sp. and Micractinium sp., in wastewater treatment. Bioresour Technol. 2014;154:131–137.
  • Schnurr PJ, Espie GS, Allen DG. Algae biofilm growth and the potential to stimulate lipid accumulation through nutrient starvation. Bioresour Technol. 2013;136:337–344.
  • Madigan M, Martinko J, Parker JB. The biology of microorganisms. Upper Saddle River (NJ): Prentice Hall; 2003.
  • Spilling K, Tamminen T, Andersen T, et al. Nutrient kinetics modeled from time series of substrate depletion and growth: dissolved silicate uptake of baltic sea spring diatoms. Mar Biol. 2010;157(2):427–436.
  • Rodolfi L, Chini Zittelli G, Bassi N, et al. Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng. 2009;102(1):100–112.
  • Pierre G, Delattre C, Dubessay P, et al. What is in store for EPS microalgae in the next decade? Molecules. 2019;24(23):1–25.
  • Ge H, Xia L, Zhou X, et al. Effects of light intensity on components and topographical structures of extracellular polysaccharides from the cyanobacteria Nostoc sp. J Microbiol. 2014;52(2):179–183.
  • You T, Barnett S. Effect of light quality on production of extracellular polysaccharides and growth rate of Porphyridium cruentum. Biochem Eng J. 2004;19(3):251–258.
  • García-Cubero R, Cabanelas ITD, Sijtsma L, et al. Production of exopolysaccharide by Botryococcus braunii CCALA 778 under laboratory simulated Mediterranean climate conditions. Algal Res. 2018;29:330–336.
  • Liqin S, Wang C, Lei S. Effects of light regime on extracellular polysaccharide production by Porphyridium Cruentum cultured in flat plate photobioreactors. 2nd International Conference on Bioinformatics and Biomedical Engineering, 2008:1488–1491.
  • Mantzorou A, Ververidis F. Microalgal biofilms: a further step over current microalgal cultivation techniques. Sci Total Environ. 2019;651:3187–3201.
  • Gross M, Jarboe D, Wen Z. Biofilm-based algal cultivation systems. Appl Microbiol Biotechnol. 2015;99(14):5781–5789.
  • Katarzyna L, Sai G, Singh OA. Non-enclosure methods for non-suspended microalgae cultivation: literature review and research needs. 2015;Renew Sustain Energ Rev. 42:1418–1427.
  • Yuan H, Zhang X, Jiang Z, et al. Effect of light spectra on microalgal biofilm: cell growth, photosynthetic property, and main organic composition. Renew Energy. 2020;157.
  • Hultberg M, Asp H, Marttila S, et al. Biofilm formation by Chlorella vulgaris is affected by light quality. Curr Microbiol. 2014;69(5):699–702.
  • Clément-Larosière B, Lopes F, Gonçalves A, et al. Carbon dioxide biofixation by Chlorella vulgaris at different CO2 concentrations and light intensities. Eng Life Sci. 2014;14(5):509–519.
  • Tang D, Han W, Li P, et al. CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresour Technol. 2010;102(3):3071–3076.
  • Kim S, Moon M, Kwak M, et al. Statistical optimization of light intensity and CO2 concentration for lipid production derived from attached cultivation of green microalga Ettlia sp. Sci Rep. 2018;8(1):15390.
  • Schnurr PJ, Espie GS, Allen GD. The effect of photon flux density on algal biofilm growth and internal fatty acid concentrations. Algal Res. 2016;16:349–356.
  • Zhang HY, Kuang YL, Lin Z, et al. Influence on surface characteristics of microalgae cell by solution chemistry. Adv Mater Res. 2011;287-290:1938–1942.
  • Wolfstein K,J, Stal L. Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar Ecol Prog Ser. 2002;236:13–22.
  • Claquin P, Probert I, Lefebvre S, et al. Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquat Microb Ecol. 2008;51:1–11.
  • Jalal KCA, Ahmad A, Rahman MF, et al. Growth and total carotenoid, chlorophyll a and chlorophyll b of tropical microalgae (Isochrysis sp.) in laboratory cultured conditions. J Biol Sci. 2013;13(1):10–17.
  • Ras M, Steyer JP, Bernard O. Temperature effect on microalgae: a crucial factor for outdoor production. Rev Environ Sci Biotechnol. 2013;12.
  • Staehr P, Birkeland M. Temperature acclimation of growth, photosynthesis and respiration in two mesophilic phytoplankton species. Phycologia. 2006;45(6):648–656.
  • Atkinson D, Ciotti BJ, Montagnes DJS. Protists decrease in size linearly with temperature: ca. 2.5% °C−1. Proc R Soc Lond B Biol Sci. 2003;270(1533):2605–2611.
  • Ozkan A, Kinney K, Katz L, et al. Reduction of water and energy requirement of algae cultivation using an algae biofilm photobioreactor. Bioresour Technol. 2012;114:542–548.
  • Lappin‐Scott HM, Costerton JW. Bacterial biofilms and surface fouling. Biofouling. 1989;1(4):323–342.
  • Bos R, van der Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions – its mechanisms and methods for study. FEMS Microbiol Rev. 1999;23(2):179–230.
  • Van Oss JC. Polar or lewis acid-base interactions. Interfacial forces in aqueous media. New York: Marcel Dekker, 1994:18–46.
  • Klein GL, Pierre G, M-n B-F, et al. Marine diatom Navicula jeffreyi from biochemical composition and physico-chemical surface properties to understanding the first step of benthic biofilm formation. J Adhes Sci Technol. 2014;28(17):1739–1753.
  • Ozkan A, Berberoglu H. Adhesion of algal cells to surfaces. Biofouling. 2013;29(4):469–482.
  • Sirmerova M, Prochazkova G, Siristova L, et al. Adhesion of Chlorella vulgaris to solid surfaces, as mediated by physicochemical interactions. J Appl Phycol. 2013;25(6):1687–1695.
  • Cheng Y, Feng G, Moraru CI. Micro- and nanotopography sensitive bacterial attachment mechanisms: a review. Front Microbiol. 2019;10:191.
  • Carniello V, Peterson BW, van der Mei HC, et al. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv Colloid Interface Sci. 2018;261:1–14.
  • Van Oss CJ. Hydrophobicity of biosurfaces — origin, quantitative determination and interaction energies. Colloids Surf B Biointerfaces. 1995;5(3–4):91–110.
  • Van Loosdrecht MC, Lyklema J, Norde W, et al. Bacterial adhesion: a physicochemical approach. Microb Ecol. 1989;17(1):1–15.
  • Hao W, Yanpeng L, Zhou S, et al. Surface characteristics of microalgae and their effects on harvesting performance by air flotation. Int J Agric Biol Eng. 2017;10:9.
  • Cui Y, Yuan W. Thermodynamic modeling of algal cell–solid substrate interactions. Appl Energy. 2013;112:485–492.
  • Boström M, Williams DRM, Ninham B. Specific ion effects: why DLVO theory fails for biology and colloid systems. Phys Rev Lett. 2001;87(16):168103.
  • Perni S, Preedy EC, Prokopovich P. Success and failure of colloidal approaches in adhesion of microorganisms to surfaces. Adv Colloid Interface Sci. 2014;206:265–274.
  • Zhang Q, Liu C, Li Y, et al. Cultivation of algal biofilm using different lignocellulosic materials as carriers. Biotechnol Biofuels. 2017;10(1):115.
  • Percival SL, Knapp JS, Wales DS. The effect of turbulent flow and surface roughness on biofilm formation in drinking water. J Ind Microbiol Biotechnol. 1999;22(3):152–159.
  • Liu Y, Strauss J, Camesano TA. Adhesion forces between Staphylococcus epidermidis and surfaces bearing self-assembled monolayers in the presence of model proteins. Biomaterials. 2008;29(33):4374–4382.
  • Seviour T, Derlon N, Dueholm MS, et al. Extracellular polymeric substances of biofilms: suffering from an identity crisis. Water Res. 2019;151:1–7.
  • Neu TR, Swerhone GDW, Lawrence JR. Assessment of lectin-binding analysis for in situ detection of glycoconjugates in biofilm systems. Microbiology. 2001;147(2):299–313.
  • Garny K, Neu TR, Horn H, et al. Combined application of 13C NMR spectroscopy and confocal laser scanning microscopy—Investigation on biofilm structure and physico-chemical properties. Chem Eng Sci. 2010;65(16):4691–4700.
  • Naumann T, Çebi Z, Podola B, et al. Growing microalgae as aquaculture feeds on twin-layers: a novel solid-state photobioreactor. J Appl Phycol. 2012;25(5):1413–1420.