Abstract
Biofilm cultivation is considered a promising method to achieve higher microalgae biomass productivity with less water consumption and easier harvest compared to conventional suspended cultivation. However, studies focusing on the selection of substratum material and optimization of the growth of certain microalgae species on specific substratum are limited. This study investigated the selection of membranous and fabric fiber substrata for the attachment of unicellular microalgae Scenedesmus dimorphus and filamentous microalgae Tribonema minus in biofilm cultivation. The results indicated that both algal species preferred hydrophilic membranous substrata and nitrate cellulose/cellulose acetate membrane (CN-CA) was selected as a suitable candidate on which the obtained biomass yields were up to 10.24 and 7.81 g m−2 day−1 for S. dimorphus and T. minus, respectively. Furthermore, high-thread cotton fiber (HCF) and low-thread polyester fiber (LPEF) were verified as the potential fabric fiber substrata for S. dimorphus (5.42 g m−2 day−1) and T. minus (5.49 g m−2 day−1) attachment, respectively. The regrowth of microalgae biofilm cultivation strategy was applied to optimize the algae growth on the fabric fiber substrata, with higher biomass density and shear resistibility achieved for both algal species. The present data highlight the importance to establish the standards for selection the suitable substratum materials in ensuring the high efficiency and sustainability of the attached microalgal biomass production.
Key points
• CN-CA was suitable membranous substratum candidate for algal biofilm cultivation.
• HCF and LPEF were potential fabric fiber substrata for S. dimorphus and T. minus.
• Regrowth biofilm cultivation was effective in improving algal biomass and attachment.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
The data are available from the corresponding author on reasonable request.
References
Brennan L, Owende P (2010) Biofuels from microalgae-a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energy Rev 14(2):557–577. https://doi.org/10.1016/j.rser.2009.10.009
Carl C, Poole AJ, Sexton BA, Glenn FL, Vucko MJ, Williams MR, Whalan S, de Nys R (2012) Enhancing the settlement and attachment strength of pediveligers of Mytilus galloprovincialis by changing surface wettability and microtopography. Biofouling 28(2):175–186. https://doi.org/10.1080/08927014.2012.662676
Cheah YT, Chan DJC (2021) Physiology of microalgal biofilm: a review on prediction of adhesion on substrates. Bioengineered 12(1):7577–7599. https://doi.org/10.1080/21655979.2021.1980671
Chen X, Liu T, Wang Q (2014) The growth of Scenedesmus sp. attachment on different materials surface. Microb Cell Fact 13:142. https://doi.org/10.1186/s12934-014-0142-z
Chen J, Dai L, Mataya D, Cobb K, Chen P, Ruan R (2022) Enhanced sustainable integration of CO2 utilization and wastewater treatment using microalgae in circular economy concept. Bioresour Technol 366:128188. https://doi.org/10.1016/j.biortech.2022.128188
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306. https://doi.org/10.1016/j.biotechadv.2007.02.001
Chisti Y (2013) Constraints to commercialization of algal fuels. J Biotechnol 167(3):201–214. https://doi.org/10.1016/j.jbiotec.2013.07.020
Choudhary P, Prajapati SK, Kumar P, Malik A, Pant KK (2017) Development and performance evaluation of an algal biofilm reactor for treatment of multiple wastewaters and characterization of biomass for diverse applications. Bioresour Technol 224:276–284. https://doi.org/10.1016/j.biortech.2016.10.078
Christenson LB, Sims RC (2012) Rotating algal biofilm reactor and spool harvester for wastewater treatment with biofuels by-products. Biotechnol Bioeng 109(7):1674–1684. https://doi.org/10.1002/bit.24451
Cui Y, Yuan W (2013) Thermodynamic modeling of algal cell-solid substrate interactions. Appl Energy 112:485–492. https://doi.org/10.1016/j.apenergy.2013.03.036
Cui Y, Yuan W, Pei Z (2010) Effects of carrier material and design on microalgae attachment for biofuel manufacturing: a literature review. ASME Int Manuf Sci Eng Conf 1:525–540. https://doi.org/10.1115/MSEC2010-34150
Dai G, Tang J, Liu W, Tan S, Liu B, Wang W, Liu T, Su G (2020) Influence of surface hydrophobicity of epoxy resin coatings on microalgae adhesion property. Chin J Process Eng 20(7):832–842. https://doi.org/10.12034/j.issn.1009-606X.220033
Dolganyuk V, Belova D, Babich O, Prosekov A, Ivanova S, Katserov D, Patyukov N, Sukhikh S (2020) Microalgae: a promising source of valuable bioproducts. Biomolecules 10(8):1153. https://doi.org/10.3390/biom10081153
Finlay JA, Callow ME, Ista LK, Lopez GP, Callow JA (2002) The influence of surface wettability on the adhesion strength of settled spores of the green alga Enteromorpha and the diatom Amphora. Integr Comp Biol 42:1116–1122. https://doi.org/10.1093/icb/42.6.1116
Genin SN, Aitchison JS, Allen DG (2014) Design of algal film photobioreactors: material surface energy effects on algal film productivity, colonization and lipid content. Bioresour Technol 155:136–143. https://doi.org/10.1016/j.biortech.2013.12.060
Gross M, Jarboe D, Wen Z (2015) Biofilm-based algal cultivation systems. Appl Microbio Biotechnol 99(14):5781–5789. https://doi.org/10.1007/s00253-015-6736-5
Gross M, Zhao X, Mascarenhas V, Wen Z (2016) Effects of the surface physico-chemical properties and the surface textures on the initial colonization and the attached growth in algal biofilm. Biotechnol Biofuels 9:38. https://doi.org/10.1186/s13068-016-0451-z
Guo C, Duan D, Sun Y, Han Y, Zhao S (2019) Enhancing Scenedesmus obliquus biofilm growth and CO2 fixation in a gas-permeable membrane photobioreactor integrated with additional rough surface. Algal Res 43:101620. https://doi.org/10.1016/j.algal.2019.101620
Huang Y, Zheng Y, Li J, Liao Q, Fu Q, Xia A, Fu J, Sun Y (2018) Enhancing microalgae biofilm formation and growth by fabricating microgrooves onto the substrate surface. Bioresour Technol 261:36–43. https://doi.org/10.1016/j.biortech.2018.03.139
Irving TE, Allen DG (2011) Species and material considerations in the formation and development of microalgal biofilms. Appl Microbiol Biotechnol 92:283–294. https://doi.org/10.1007/s00253-011-3341-0
Ji C, Wang J, Zhang W, Liu J, Wang H, Gao L, Liu T (2014a) An applicable nitrogen supply strategy for attached cultivation of Aucutodesmus obliquus. J Appl Phycol 26:173–180. https://doi.org/10.1007/s10811-013-0115-3
Ji B, Zhang W, Zhang N, Wang J, Lutzu GA, Liu T (2014b) Biofilm cultivation of the oleaginous microalgae Pseudochlorococcum sp. Bioprocess Biosyst Eng 37:1369–1375. https://doi.org/10.1007/s00449-013-1109-x
Karimi Z, Laughinghouse HD 4th, Davis VA, Blersch DM (2021) Substrate properties as controlling parameters in attached algal cultivation. Appl Microbiol Biotechnol 105(5):1823–1835. https://doi.org/10.1007/s00253-021-11127-y
Kim BH, Kim DH, Choi JW, Kang Z, Cho DH, Kim JY, Oh HM, Kim HS (2015) Polypropylene bundle attached multilayered Stigeoclonium biofilms cultivated in untreated sewage generate high biomass and lipid productivity. J Microbiol Biotechnol 25(9):1547–1554. https://doi.org/10.4014/jmb.1501.01033
Klein GL, Pierre G, Bellonfontaine MN, Zhao JM, Breret M, Maugard T, Graber M (2014) 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 28(17):1739–1753. https://doi.org/10.1080/01694243.2014.920461
Liu T, Wang J, Hu Q, Cheng P, Ji B, Liu J, Chen Y, Zhang W, Chen X, Chen L, Gao L, Ji C, Wang H (2013) Attached cultivation technology of microalgae for efficient biomass feedstock production. Bioresour Technol 127:216–222. https://doi.org/10.1016/j.biortech.2012.09.100
Mantzorou A, Ververidis F (2019) Microalgal biofilms: a further step over current microalgal cultivation techniques. Sci Total Environ 651:3187–3201. https://doi.org/10.1016/j.scitotenv.2018.09.355
Ozkan A, Berberoglu H (2013) Cell to substratum and cell to cell interactions of microalgae. Colloids Surf B 112:302–309. https://doi.org/10.1016/j.colsurfb.2013.08.007
Palmer J, Flint S, Brooks J (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34:577–588. https://doi.org/10.1007/s10295-007-0234-4
Podola B, Li T, Melkonian M (2016) Porous substrate bioreactors: a paradigm shift in microalgal biotechnology? Trends Biotechnol 35(2):121–132. https://doi.org/10.1016/j.tibtech.2016.06.004
Rosli SS, Kadir WNA, Wong CY, Han FY, Lim JW, Lam MK, Yusup S, Kiatkittipong W, Kiatkittipong K, Usman A (2020) Insight review of attached microalgae growth focusing on support material packed in photobioreactor for sustainable biodiesel production and wastewater bioremediation. Renew Sust Energy Rev 134:110306. https://doi.org/10.1016/j.rser.2020.110306
Sekar R, Venugopalan VP, Satpathy KK, Nair KVK, Rao VNR (2004) Laboratory studies on adhesion of microalgae to hard substrates. Hydrobiologia 512:109–116. https://doi.org/10.1023/B:HYDR.0000020315.40349.38
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(3):441–450. https://doi.org/10.1007/s00449-013-1011-6
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
Shen Y, Zhu W, Chen C, Nie Y, Lin X (2016) Biofilm formation in attached microalgal reactors. Bioprocess Biosyst Eng 39:1281–1288. https://doi.org/10.1007/s00449-016-1606-9
Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriol Rev 35(2):171–205. https://doi.org/10.1128/br.35.2.171-205.1971
Venable ME, Podbielski MR (2019) Impact of substrate material on algal biofilm biomass growth. Environ Sci Pollut Res 26:7256–7262. https://doi.org/10.1007/s11356-019-04148-8
Wang H, Gao L, Chen L, Guo F, Liu T (2013) Integration process of biodiesel production from filamentous oleaginous microalgae Tribonema minus. Bioresour Technol 142:39–44. https://doi.org/10.1016/j.biortech.2013.05.058
Wang H, Zhou W, Cheng W, Gano L, Liu T (2016) Strategy study on enhancing lipid productivity of filamentous oleaginous microalgae Tribonema. Bioresour Technol 218:161–166. https://doi.org/10.1016/j.biortech.2016.06.083
Wang J, Liu W, Liu T (2017) Biofilm based attached cultivation technology for microalgal biorefineries-a reiview. Bioresour Technol 244:1245–1253. https://doi.org/10.1016/j.biortech.2017.05.136
Wang JH, Zhuang LL, Xu XQ, Deantes-Espinosa VM, Wang XX, Hu HY (2018) Microalgal attachment and attached systems for biomass production and wastewater treatment. Renew Sust Energy Rev 92:331–342. https://doi.org/10.1016/j.rser.2018.04.081
Xia L, Li H, Song S (2016) Cell surface characterization of some oleaginous green algae. J Appl Phycol 28:2323–2332. https://doi.org/10.1007/s10811-015-0768-1
Yu Z, Pei H, Li Y, Yang Z, Xie Z, Hou Q, Nie C (2020) Inclined algal biofilm photobioreactor (IABPBR) for cost-effective cultivation of lipid-rich microalgae and treatment of seawater-diluted anaerobically digested effluent from kitchen waste with the aid of phytohormones. Bioresour Technol 315:123761. https://doi.org/10.1016/j.biortech.2020.123761
Yuan H, Zhang X, Jiang Z, Wang X, Chen X, Cao L, Zhang X (2019) Analyzing the effect of pH on microalgae adhesion by identifying the dominant interaction between cell and surface. Colloids Surf B Biointerfaces 177:479–486. https://doi.org/10.1016/j.colsurfb.2019.02.023
Zhang L, Chen L, Wang J, Chen Y, Gao X, Zhang Z, Liu T (2015) Attached cultivation for improving the biomass productivity of Spirulina platensis. Bioresour Technol 181:136–142. https://doi.org/10.1016/j.biortech.2015.01.025
Zhang X, Yuan H, Jiang Z, Lin D, Zhang X (2018a) Impact of surface tension of wastewater on biofilm formation of microalgae Chlorella sp. Bioresour Technol 266:498–506. https://doi.org/10.1016/j.biortech.2018.06.082
Zhang Q, Li X, Guo D, Ye T, Xiong M, Zhu L, Liu C, Jin S, Hu Z (2018b) Operation of a vertical algal biofilm enhanced raceway pond for nutrient removal and microalgae-based byproducts production under different wastewater loadings. Bioresour Technol 253:323–332. https://doi.org/10.1016/j.biortech.2018.01.014
Zhang Q, Yu Z, Jin S, Zhu L, Liu C, Zheng H, Zhou T, Liu Y, Ruan R (2019) Lignocellulosic residue as bio-carrier for algal biofilm growth: effects of carrier physicochemical proprieties and toxicity on algal biomass production and composition. Bioresour Technol 293:122091. https://doi.org/10.1016/j.biortech.2019.122091
Zhang Q, Yu Z, Jin S, Liu C, Li Y, Guo D, Hu M, Ruan R, Liu Y (2020a) 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
Zhang Y, Ji C, Zhou W, Wang H, Wang J, Liu T (2020b) Studies on the attached cultivation of filamentous oleaginous microalga Tribonema minus. J Ocean Univ China 19(3):691–699. https://doi.org/10.1007/s11802-020-4256-0
Zhang Y, Ma R, Chu H, Zhou X, Yao T, Zhang Y (2022) Evaluation of the performance of different membrane materials for microalgae cultivation on attached biofilm reactors. RSC Adv 12(3):1451–1459. https://doi.org/10.1039/d1ra07335d
Zheng Y, Huang Y, Liao Q, Zhu X, Fu Q, Xia A (2016) Effects of wettability on the growth of Scenedesmus obliquus biofilm attached on glass surface coated with polytetrafluoroethylene emulsion. Int J Hydrogen Energy 41:21728–21735. https://doi.org/10.1016/j.ijhydene.2016.07.007
Zhou W, Wang H, Chen L, Cheng W, Liu T (2017) Heterotrophy of filamentous oleaginous microalgae Tribonema minus for potential production of lipid and palmitoleic acid. Bioresour Technol 239:250–257. https://doi.org/10.1016/j.biortech.2017.05.045
Zhuang LL, Azimi Y, Yu D, Wang WL, Wu YH, Dao GH, Hu HY (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
Zhuang L, Yu D, Zhang J, Liu FF, Wu YH, Zhang TY, Dao GH, Hu HY (2018) The characteristics and influencing factors of the attached microalgae cultivation: a review. Renew Sust Energy Rev 94:1110–1119. https://doi.org/10.1016/j.rser.2018.06.006
Funding
This work was funded by the National Natural Science Foundation of China (Grant No. 31902344), Scientific and Technological Innovation Programs of Higher Education Institutions in Shanxi (Grant No. 2019L0376), and Science and Technology Innovation Fund of Shanxi Agricultural University (Grant No. 2016YJ01).
Author information
Authors and Affiliations
Contributions
CLJ, HW, and TZL conceived and designed the research. CLJ conducted the experiments, collected the data, and prepared the original draft of the manuscript. CLJ, HW, HLC, and CHZ analyzed data. RZL and TZL reviewed and edited the manuscript. All authors have read and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ji, C., Wang, H., Cui, H. et al. Characterization and evaluation of substratum material selection for microalgal biofilm cultivation. Appl Microbiol Biotechnol 107, 2707–2721 (2023). https://doi.org/10.1007/s00253-023-12475-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-023-12475-7