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Novel Extrapolymeric Substances Biocoating on Polyvinylidene Fluoride Membrane for Enhanced Attached Growth of Navicula incerta

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Abstract

Cell adhesion is always the first step in biofilm development. With the emergence of attached cultivation systems, this study aims to promote a cost-effective approach for sustainable cultivation of microalgae, Navicula incerta, by pre-coating the main substrates, commercial polyvinylidene fluoride (PVDF) membranes with its own washed algal cells and self-produced soluble extracellular polymeric substances (EPS) for strengthened biofilm development. The effects of pH value (6 to 9), cell suspension volume (10 to 30 mL), and EPS volume (10 to 50 mL) were statistically optimized by means of response surface methodology toolkit. Model outputs revealed good agreement with cell adhesion data variation less than 1% at optimized pre-coating conditions (7.20 pH, 30 mL cell suspension volume, and 50 mL EPS volume). Throughout long-term biofilm cultivation, results demonstrated that EPS pre-coating substantially improved the attached microalgae density by as high as 271% than pristine PVDF due to rougher surface and the presence of sticky exopolymer particles. Nutrients absorbed via the available EPS coating from the bulk medium made the immobilized cells to release less polysaccharides on an average of 30% less than uncoated PVDF. This work suggests that adhesive polymer binders derived from organic sources can be effectively integrated into the development of high-performance novel materials as biocoating for immobilized microalgae cultivation.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Podola B, Li T, Melkonian M (2017) Porous substrate bioreactors: a paradigm shift in microalgal biotechnology. Trends Biotechnol 35:121–132. https://doi.org/10.1016/j.tibtech.2016.06.004

    Article  CAS  PubMed  Google Scholar 

  2. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. https://doi.org/10.1038/nrmicro2415

    Article  CAS  PubMed  Google Scholar 

  3. Cheah YT, Chan DJC (2021) Physiology of microalgal biofilm: a review on prediction of adhesion on substrates. Bioengineered 12:7577–7599. https://doi.org/10.1080/21655979.2021.1980671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Soriano-Jerez Y, López-Rosales L, Cerón-García MC, Sánchez-Mirón A, Gallardo-Rodríguez JJ, García-Camacho F, Molina-Grima E (2021) Long-term biofouling formation mediated by extracellular proteins in Nannochloropsis gaditana microalga cultures at different medium N/P ratios. Biotechnol Bioeng 118:1152–1165. https://doi.org/10.1002/bit.27632

    Article  CAS  PubMed  Google Scholar 

  5. Lorite GS, Rodrigues CM, de Souza AA, Kranz C, Mizaikoff B, Cotta MA (2011) The role of conditioning film formation and surface chemical changes on Xylella fastidiosa adhesion and biofilm evolution. J Colloid Interface Sci 359:289–295. https://doi.org/10.1016/j.jcis.2011.03.066

    Article  CAS  PubMed  Google Scholar 

  6. Liu Y, Yang C-H, Li J (2007) Influence of extracellular polymeric substances on Pseudomonas aeruginosa transport and deposition profiles in porous media. Environ Sci Technol 41:198–205. https://doi.org/10.1021/es061731n

    Article  CAS  PubMed  Google Scholar 

  7. Barranguet C, Veuger B, Van Beusekom SAM, Marvan P, Sinke JJ, Admiraal W (2005) Divergent composition of algal-bacterial biofilms developing under various external factors. Eur J Phycol 40:1–8. https://doi.org/10.1080/09670260400009882

    Article  CAS  Google Scholar 

  8. Cortez S, Nicolau A, Flickinger MC, Mota M (2017) Biocoatings: a new challenge for environmental biotechnology. Biochem Eng J 121:25–37. https://doi.org/10.1016/j.bej.2017.01.004

    Article  CAS  Google Scholar 

  9. Tong CY, Lew JK, Derek CJC (2022) Algal extracellular organic matter pre-treatment enhances microalgal biofilm adhesion onto microporous substrate. Chemosphere 307:135740. https://doi.org/10.1016/j.chemosphere.2022.135740

    Article  CAS  PubMed  Google Scholar 

  10. Nongmaithem D, Tiwari R, Goud V (2021) Cultivating Scenedesmus sp. on substrata coated with cyanobacterial-derived extracellular polymeric substances for enhanced biomass productivity: a novel harvesting approach. Biomass Convers Biorefin 1–13. https://doi.org/10.1007/s13399-021-01432-x

  11. Zhuang L-L, Azimi Y, Yu D, Wang W-L, Wu Y-H, Dao G-H, Hu H-Y (2016) Enhanced attached growth of microalgae Scenedesmus. LX1 through ambient bacterial pre-coating of cotton fiber carriers. Bioresour Technol 218:643–649. https://doi.org/10.1016/j.biortech.2016.07.013

    Article  CAS  PubMed  Google Scholar 

  12. Marella TK, López-Pacheco IY, Parra-Saldívar R, Dixit S, Tiwari A (2020) Wealth from waste: diatoms as tools for phycoremediation of wastewater and for obtaining value from the biomass. Sci Total Environ 724:137960. https://doi.org/10.1016/j.scitotenv.2020.137960

    Article  CAS  PubMed  Google Scholar 

  13. Alquraishi DO, Kamil I (2019) Biosorption of cadmium, lead and nickel in their aqueous solution by Nitzschia palea and Navicula incerta. J Eng Appl Sci 14:9114–9120. https://doi.org/10.36478/jeasci.2019.9114.9120

    Article  CAS  Google Scholar 

  14. Shen Y, Xu X, Zhao Y, Lin X (2014) Influence of algae species, substrata and culture conditions on attached microalgal culture. Bioprocess Biosyst Eng 37:441–450. https://doi.org/10.1007/s00449-013-1011-6

    Article  CAS  PubMed  Google Scholar 

  15. Tong CY, Derek CJC (2021) The role of substrates towards marine diatom Cylindrotheca fusiformis adhesion and biofilm development. J Appl Phycol 33:2845–2862. https://doi.org/10.1007/s10811-021-02504-1

    Article  CAS  Google Scholar 

  16. Tong CY, Derek CJC (2022) Membrane surface roughness promotes rapid initial cell adhesion and long term microalgal biofilm stability. Environ Res 206:112602. https://doi.org/10.1016/j.envres.2021.112602

    Article  CAS  PubMed  Google Scholar 

  17. Tong CY, Derek CJC (2021) Biofilm formation of benthic diatoms on commercial polyvinylidene fluoride membrane. Algal Res 55:102260. https://doi.org/10.1016/j.algal.2021.102260

    Article  Google Scholar 

  18. Staats N, De Winder B, Stal L, Mur L (1999) Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur J Phycol 34:161–169. https://doi.org/10.1080/09670269910001736212

    Article  Google Scholar 

  19. Cheah YT, Chan DJC (2022) A methodological review on the characterization of microalgal biofilm and its extracellular polymeric substances. J Appl Microbiol 132:3490–3514. https://doi.org/10.1111/jam.15455

    Article  PubMed  Google Scholar 

  20. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017

    Article  CAS  Google Scholar 

  21. Elisabeth B, Rayen F, Behnam T (2021) Microalgae culture quality indicators: a review. Crit Rev Biotechnol 41:457–473. https://doi.org/10.1080/07388551.2020.1854672

    Article  CAS  PubMed  Google Scholar 

  22. Moheimani N (2012) Inorganic carbon and pH effect on growth and lipid productivity of Tetraselmis suecica and Chlorella sp (Chlorophyta) grown outdoors in bag photobioreactors. J Appl Phycol 25:387–398. https://doi.org/10.1007/s10811-012-9873-6

    Article  CAS  Google Scholar 

  23. Bartley M, Boeing W, Holguin F, Schaub T (2014) pH effects on growth and lipid accumulation of the biofuel microalgae Nannochloropsis salina and invading organisms. J Appl Phycol 26:1431–1437. https://doi.org/10.1007/s10811-013-0177-2

    Article  CAS  Google Scholar 

  24. Bethmann B, Schönknecht G (2009) pH regulation in an acidophilic green alga – a quantitative analysis. New Phytol 183:327–339. https://doi.org/10.1111/j.1469-8137.2009.02862.x

    Article  CAS  PubMed  Google Scholar 

  25. Rani S, Gunjyal N, Ojha CSP, Singh Rajendra P (2021) Review of challenges for algae-based wastewater treatment: strain selection, wastewater characteristics, abiotic, and biotic factors. J Hazard Toxic Radioact Waste 25:03120004. https://doi.org/10.1061/(ASCE)HZ.2153-5515.0000578

    Article  CAS  Google Scholar 

  26. Jin C, Yu Z, Peng S, Feng KE, Zhang L, Zhou X (2018) The characterization and comparison of exopolysaccharides from two benthic diatoms with different biofilm formation abilities. An Acad Bras Cienc 90:1503–1519. https://doi.org/10.1590/0001-3765201820170721

    Article  CAS  PubMed  Google Scholar 

  27. Shen Y, Zhang H, Xu X, Lin X (2015) Biofilm formation and lipid accumulation of attached culture of Botryococcus braunii. Bioprocess Biosyst Eng 38:481–488. https://doi.org/10.1007/s00449-014-1287-1

    Article  CAS  PubMed  Google Scholar 

  28. Hermansson M (1999) The DLVO theory in microbial adhesion. Colloids Surf B Biointerfaces 14:105–119. https://doi.org/10.1016/S0927-7765(99)00029-6

    Article  CAS  Google Scholar 

  29. Ding Z, Bourven I, Guibaud G, van Hullebusch ED, Panico A, Pirozzi F, Esposito G (2015) Role of extracellular polymeric substances (EPS) production in bioaggregation: application to wastewater treatment. Appl Microbiol Biotechnol 99:9883–9905. https://doi.org/10.1007/s00253-015-6964-8

    Article  CAS  PubMed  Google Scholar 

  30. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55:287–333. https://doi.org/10.1016/S0079-6611(02)00138-6

    Article  Google Scholar 

  31. Hwang G, Kang S, El-Din M, Liu Y (2012) Impact of an extracellular polymeric substance (EPS) precoating on the initial adhesion of Burkholderia cepacia and Pseudomonas aeruginosa. Biofouling 28:525–538. https://doi.org/10.1080/08927014.2012.694138

    Article  CAS  PubMed  Google Scholar 

  32. Whitehead KA, Colligon J, Verran J (2005) Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf B Biointerfaces 41:129–138. https://doi.org/10.1016/j.colsurfb.2004.11.010

    Article  CAS  PubMed  Google Scholar 

  33. Bazaka K, Jacob MV, Truong VK, Crawford RJ, Ivanova EP (2011) The effect of polyterpenol thin film surfaces on bacterial viability and adhesion. Polymers 3:388–404. https://doi.org/10.3390/polym3010388

    Article  CAS  Google Scholar 

  34. Lee KS, Kwon T-H, Park T, Jeong MS (2020) Chapter 2 - microbiology and microbial products for enhanced oil recovery. In: Lee KS, Kwon T-H, Park T, Jeong MS (eds) Theory and practice in microbial enhanced oil recovery. Gulf Professional Publishing, pp 27–65. https://doi.org/10.1016/B978-0-12-819983-1.00002-8

  35. Bosak S, Pletikapić G, Hozic A, Svetlicic V, Sarno D, Viličić D (2012) A novel type of colony formation in marine planktonic diatoms revealed by atomic force microscopy. PLoS ONE 7:e44851. https://doi.org/10.1371/journal.pone.0044851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang Q, Yu Z, Jin S, Liu C, Li Y, Guo D, Hu M, Ruan R, Liu Y (2020) Role of surface roughness in the algal short-term cell adhesion and long-term biofilm cultivation under dynamic flow condition. Algal Res 46:101787. https://doi.org/10.1016/j.algal.2019.101787

    Article  Google Scholar 

  37. González-Camejo J, Paches M, Marin Á, Jiménez-Benítez A, Seco A, Barat R (2020) Production of microalgal external organic matter in a Chlorella -dominated culture: influence of temperature and stress factors. Environ Sci Water Res Technol 6:1828–1841. https://doi.org/10.1039/D0EW00176G

    Article  Google Scholar 

  38. Miranda AF, Ramkumar N, Andriotis C, Höltkemeier T, Yasmin A, Rochfort S, Wlodkowic D, Morrison P, Roddick F, Spangenberg G, Lal B, Subudhi S, Mouradov A (2017) Applications of microalgal biofilms for wastewater treatment and bioenergy production. Biotechnol Biofuels 10:120. https://doi.org/10.1186/s13068-017-0798-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Zhuang L-L, Yu D, Zhang J, Liu F-f, Wu Y-H, Zhang T-Y, Dao G-H, Hu H-Y (2018) The characteristics and influencing factors of the attached microalgae cultivation: A review. Renew Sustain Energ Rev 94:1110–1119. https://doi.org/10.1016/j.rser.2018.06.006

    Article  CAS  Google Scholar 

  40. Zarrinmehr MJ, Farhadian O, Heyrati FP, Keramat J, Koutra E, Kornaros M, Daneshvar E (2020) Effect of nitrogen concentration on the growth rate and biochemical composition of the microalga, Isochrysis galbana. Egypt J Aquat Res 46:153–158. https://doi.org/10.1016/j.ejar.2019.11.003

    Article  Google Scholar 

  41. Cao F (2017) Hydrophobic features of extracellular polymeric substances (EPS) extracted from biofilms: an investigation based on DAX-8 resin technique. Université Paris-Est. https://tel.archives-ouvertes.fr/tel-01630489/document

  42. Tong CY, Chang YS, Ooi BS, Chan DJC (2021) Physico-chemistry and adhesion kinetics of algal biofilm on polyethersulfone (PES) membrane with different surface wettability. J Environ Chem Eng 9:106531. https://doi.org/10.1016/j.jece.2021.106531

    Article  CAS  Google Scholar 

  43. Ozkan A, Berberoglu H (2013) Adhesion of algal cells to surfaces. Biofouling 29:469–482. https://doi.org/10.1080/08927014.2013.782397

    Article  PubMed  Google Scholar 

  44. Mirani ZA, Fatima A, Urooj S, Aziz M, Khan MN, Abbas T (2018) Relationship of cell surface hydrophobicity with biofilm formation and growth rate: a study on Pseudomonas aeruginosa, Staphylococcus aureus, and Escherichia coli. Iran J Basic Med Sci 21:760–769. https://doi.org/10.22038/IJBMS.2018.28525.6917

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors acknowledge Universiti Sains Malaysia for the Research University Grant with Project Code: RUI/8014065.

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C. Y. Tong: conceptualization, investigation, data curation, formal analysis, methodology, resources, validation, writing—original draft, writing—review & editing, and conceived the experiments. C. J. C. Derek: funding acquisition, project administration, supervision, conceptualization, data curation, validation, resources, and writing—review & editing.

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Correspondence to C. J. C. Derek.

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Tong, C.Y., Derek, C.J.C. Novel Extrapolymeric Substances Biocoating on Polyvinylidene Fluoride Membrane for Enhanced Attached Growth of Navicula incerta. Microb Ecol 86, 549–562 (2023). https://doi.org/10.1007/s00248-022-02091-9

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