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Cell Surface Energy Affects the Structure of Microalgal Biofilm

  • Xinru Zhang
    Xinru Zhang
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    Beijing Engineering Research Center of Energy Saving and Environmental Protection, Beijing 100083, China
    More by Xinru Zhang
  • Hao Yuan
    Hao Yuan
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    More by Hao Yuan
  • Yi Wang
    Yi Wang
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    More by Yi Wang
  • Libo Guan
    Libo Guan
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    More by Libo Guan
  • Ziyi Zeng
    Ziyi Zeng
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    More by Ziyi Zeng
  • Zeyi Jiang*
    Zeyi Jiang
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    Beijing Key Laboratory for Energy Saving and Emission Reduction of Metallurgical Industry, Beijing 100083, China
    *Email: [email protected]. Phone: 86-10-62334971.
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  • , and 
  • Xinxin Zhang
    Xinxin Zhang
    School of Energy and Environmental Engineering, University of Science and Technology Beijing, Beijing 100083, China
    Beijing Key Laboratory for Energy Saving and Emission Reduction of Metallurgical Industry, Beijing 100083, China
    More by Xinxin Zhang
Cite this: Langmuir 2020, 36, 12, 3057–3063
Publication Date (Web):March 11, 2020
https://doi.org/10.1021/acs.langmuir.0c00274
Copyright © 2020 American Chemical Society

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    Abstract

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    Microalgae biofilm-based culture systems have wide applications in environmental engineering and biotechnology. Biofilm structure is critical for the transport of nutrients, gas, and signaling molecules in a microalgal biofilm. This work aims to understand the influence of cell surface energy (SE) on the microalgal biofilm structure. Three microalgae species were used as model cells in the study: Chlorella sp., Nannochloris oculata, and Chlorella pyrenoidosa. First, by mediating biofilm culture conditions, we obtained Chlorella sp. cells with SEs of 40.4 ± 1.5, 44.7 ± 1.0, and 62. 7 ± 1.2 mJ/m2, N. oculata cells with SEs of 47.7 ± 0.5, 41.1 ± 1.0, and 62.6 ± 1.2 mJ/m2, and C. pyrenoidosa cells with SEs of 64.0 ± 0.6, 62.1 ± 0.7, and 62.8 ± 0.6 mJ/m2. Then, based on the characterizations of biofilm structures, we found that cell SE can significantly affect the microalgae biofilm structure. When the cell SEs ranged from 40 to 50 mJ/m2, the microalgae cells formed heterogeneous biofilms with a large number of open voids, and the biofilm porosity was higher than 20%. Alternatively, when the cell SEs ranged from 50 to 65 mJ/m2, the cells formed a flat, homogeneous biofilm with the porosity lower than 20%. Finally, the influencing mechanism of cell SE on biofilm structure was interpreted based on the thermodynamic theory via analyzing the co-adhesion energy between cells. The study has important implications in understanding factors that influence the biofilm structures.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.langmuir.0c00274.

    • Microalgal biofilm culture (Tables S1–S3 and Figure S1); determination of the SE of microalgae cells (Figure S2); measurement of microalgae morphology and size (Figure S3); characterization of surface composition of microalgae cells (Figures S4–S6 and Table S4); three-dimensional images of microalgae biofilms (Figure S7); and analysis of co-adhesion energy of microalgae cells (Table S5) (PDF)

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    Cited By

    This article is cited by 13 publications.

    1. Paula Araujo Gomes, Jean-Baptiste d’Espinose de Lacaillerie, Bruno Lartiges, Martin Maliet, Valérie Molinier, Nicolas Passade-Boupat, Nicolas Sanson. Microalgae as Soft Permeable Particles. Langmuir 2022, 38 (46) , 14044-14052. https://doi.org/10.1021/acs.langmuir.2c01735
    2. Weida Zeng, Peirong Li, Yun Huang, Ao Xia, Xianqing Zhu, Xun Zhu, Qiang Liao. How Interfacial Properties Affect Adhesion: An Analysis from the Interactions between Microalgal Cells and Solid Substrates. Langmuir 2022, 38 (10) , 3284-3296. https://doi.org/10.1021/acs.langmuir.2c00042
    3. Michela Castigliano, Federica Recupido, Maria Petala, Margaritis Kostoglou, Sergio Caserta, Thodoris D. Karapantsios. Wetting of Dehydrated Hydrophilic Pseudomonas fluorescens Biofilms under the Action of External Body Forces. Langmuir 2021, 37 (37) , 10890-10901. https://doi.org/10.1021/acs.langmuir.1c00528
    4. Yan Gao, Olivier Bernard, Andrea Fanesi, Patrick Perré, Filipa Lopes. The effect of light intensity on microalgae biofilm structures and physiology under continuous illumination. Scientific Reports 2024, 14 (1) https://doi.org/10.1038/s41598-023-50432-6
    5. Yi Wang, Xinru Zhang, Yuyang Wu, Guangpu Sun, Zeyi Jiang, Siyuan Hao, Shiya Ye, Hu Zhang, Fan Zhang, Xinxin Zhang. Improving biomass yields of microalgae biofilm by coculturing two microalgae species via forming biofilms with uniform microstructures and small cell-clusters. Bioresource Technology 2024, 393 , 130052. https://doi.org/10.1016/j.biortech.2023.130052
    6. Linda O’Higgins, Imen Hamed. Attached Biofilm Cultivation (ABC) of Mixotrophic Microalgae for the Sustainable Supply of Innovative New Bioproducts. 2024, 229-244. https://doi.org/10.1007/978-3-031-43969-8_18
    7. Haijian Yang, Denghua Wu, Hua Li, Chunxiang Hu. The extracellular polysaccharide determine the physico-chemical surface properties of Microcystis. Frontiers in Microbiology 2023, 14 https://doi.org/10.3389/fmicb.2023.1285229
    8. Peirong Li, Yun Huang, Ao Xia, Xianqing Zhu, Xun Zhu, Qiang Liao. Bio-decarbonization by microalgae: a comprehensive analysis of CO2 transport in photo-bioreactor. DeCarbon 2023, 2 , 100016. https://doi.org/10.1016/j.decarb.2023.100016
    9. Hemamalini Rawindran, Rabbani Syed, Abdulaziz Alangari, Kuan Shiong Khoo, Jun Wei Lim, Nurul Tasnim Sahrin, Uganeeswary Suparmaniam, Ratchaprapa Raksasat, Chin Seng Liew, Wai Hong Leong, Worapon Kiatkittipong, Muhammad Kashif Shahid, Hirofumi Hara, Maizatul Shima Shaharun. Mechanistic behaviour of Chlorella vulgaris biofilm formation onto waste organic solid support used to treat palm kernel expeller in the recent Anthropocene. Environmental Research 2023, 222 , 115352. https://doi.org/10.1016/j.envres.2023.115352
    10. Yi Wang, Xinru Zhang, Libo Guan, Zeyi Jiang, Xiaomin Gao, Siyuan Hao, Xinxin Zhang. A novel method to harvest microalgae biofilms by interfacial interaction. Algal Research 2023, 70 , 103000. https://doi.org/10.1016/j.algal.2023.103000
    11. Fathiah Mohamed Zuki, Hamed Pourzolfaghar, Robert G. J. Edyvean, J. E. Hernandez. Interpretation of Initial Adhesion of Pseudomonas putida on Hematite and Quartz Using Surface Thermodynamics, DLVO, and XDLVO Theories. Surface Engineering and Applied Electrochemistry 2022, 58 (5) , 478-490. https://doi.org/10.3103/S1068375522050131
    12. Yi Wang, Zeyi Jiang, Zhijian Lai, Hao Yuan, Xinru Zhang, Yan Jia, Xinxin Zhang. The self-adaption capability of microalgal biofilm under different light intensities: Photosynthetic parameters and biofilm microstructures. Algal Research 2021, 58 , 102383. https://doi.org/10.1016/j.algal.2021.102383
    13. Hao Yuan, Yi Wang, Zhijian Lai, Xinru Zhang, Zeyi Jiang, Xinxin Zhang. Analyzing microalgal biofilm structures formed under different light conditions by evaluating cell–cell interactions. Journal of Colloid and Interface Science 2021, 583 , 563-570. https://doi.org/10.1016/j.jcis.2020.09.057

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