Abstract
The co-pelletization of microalgae with filamentous fungi was a promising approach for microalgae harvest. However, the real conditions of microalgae growth limited the arbitrary optimization of co-pellets formation with filamentous fungi. Therefore, it is urgent to develop an approach to manipulate the co-pelletization through treatment of A. niger spores. In this study, Aspergillus niger and Chlorella vulgaris were used as the model species of filamentous fungi and microalgae to investigate co-pellets formation using A. niger spores after by different pH solutions treatment, swelling, snailase treatment. The importance of spore treatments on C. vulgaris harvest in sequence was claimed based on response surface methodology analysis. The pH solutions treatment, swelling, snailase treatment of A. niger spore contributed 21.0%, 10.5%, 40.7% of harvest ratio of C. vulgaris respectively, which guided the application of spore treatment into co-pelletization. Treatment of spore was showed as an efficient approach to manipulate co-pelletization for microalgae harvest in diverse microalgae condition. This results promoted the application of co-pelletization technology in microalgae harvest of various conditions.
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References
Ball SR, Kwan AH, Sunde M (2020) Hydrophobin rodlets on the fungal cell wall. In: Latgé J-P (ed) The fungal cell wall: an armour and a weapon for human fungal pathogens. Springer, Cham, pp 29–51. https://doi.org/10.1007/82_2019_186
Beauvais A, Fontaine T, Aimanianda V, Latgé J-P (2014) Aspergillus cell wall and biofilm. Mycopathologia 178(5):371–377. https://doi.org/10.1007/s11046-014-9766-0
Bhattacharya A, Mathur M, Kumar P, Prajapati SK, Malik A (2017) A rapid method for fungal assisted algal flocculation: Critical parameters & mechanism insights. Algal Res 21:42–51. https://doi.org/10.1016/j.algal.2016.10.022
Cairns TC, Feurstein C, Zheng X, Zheng P, Sun J, Meyer V (2019) A quantitative image analysis pipeline for the characterization of filamentous fungal morphologies as a tool to uncover targets for morphology engineering: a case study using aplD in Aspergillus niger. Biotechnol Biofuels 12:149. https://doi.org/10.1186/s13068-019-1473-0
Castrillo M, Lucas-Salas LM, Rodriguez-Gil C, Martinez D (2013) High pH-induced flocculation-sedimentation and effect of supernatant reuse on growth rate and lipid productivity of Scenedesmus obliquus and Chlorella vulgaris. Bioresource Technol 128:324–329. https://doi.org/10.1016/j.biortech.2012.10.114
Chen J, Leng LJ, Ye CS, Lu Q, Addy M, Wang JH, Liu J, Chen P, Ruan R, Zhou WG (2018) A comparative study between fungal pellet- and spore-assisted microalgae harvesting methods for algae bioflocculation. Bioresource Technol 259:181–190. https://doi.org/10.1016/j.biortech.2018.03.040
Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, Lee D-J, Chang J-S (2017) Microalgae biorefinery: high value products perspectives. Bioresource Technol 229:53–62. https://doi.org/10.1016/j.biortech.2017.01.006
Chu RY, Li SX, Zhu LD, Yin ZH, Hu D, Liu CC, Mo F (2021) A review on co-cultivation of microalgae with filamentous fungi: Efficient harvesting, wastewater treatment and biofuel production. Renew Sust Energ Rev 139:110689. https://doi.org/10.1016/j.rser.2020.110689
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168(4265):167. https://doi.org/10.1038/168167a0
Fontaine T, Beauvais A, Loussert C, Thevenard B, Fulgsang CC, Ohno N, Clavaud C, Prevost M-C, Latge J-P (2010) Cell wall α1-3 glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet Biol 47(8):707–712. https://doi.org/10.1016/j.fgb.2010.04.006
González-Pérez BK, Rivas-Castillo AM, Valdez-Calderón A, Gayosso-Morales MA (2021) Microalgae as biostimulants: a new approach in agriculture. World J Microbiol Biotechnol 38(1):4. https://doi.org/10.1007/s11274-021-03192-2
Gultom SO, Zamalloa C, Hu B (2014) Microalgae harvest through fungal pelletization-co-culture of Chlorella vulgaris and Aspergillus niger. Energies 7(7):4417–4429. https://doi.org/10.3390/en7074417
Hoang AT, Sirohi R, Pandey A, Nižetić S, Lam SS, Chen W-H, Luque R, Thomas S, Arıcı M, Pham VV (2023) Biofuel production from microalgae: challenges and chances. Phytochem Rev 22(4):1089–1126. https://doi.org/10.1007/s11101-022-09819-y
Ijadpanahsaravi M, Punt M, Wösten HAB, Teertstra WR (2021) Minimal nutrient requirements for induction of germination of Aspergillus niger conidia. Fungal Biol 125(3):231–238. https://doi.org/10.1016/j.funbio.2020.11.004
Kumar Awasthi A, Yuan Z, Kumar Awasthi M, Li M, Mishra S, Kumar Pandey A (2022) Bioprocess potential of eco-friendly fungal isolates converting organic waste to bioresource. Bioresour Technol 346:126586. https://doi.org/10.1016/j.biortech.2021.126586
Latge J-P, Beauvais A (2014) Functional duality of the cell wall. Curr Opin Microbiol 20:111–117
Leng L, Li W, Chen J, Leng S, Chen J, Wei L, Peng H, Li J, Zhou W, Huang H (2021) Co-culture of fungi-microalgae consortium for wastewater treatment: a review. Bioresource Technol 330:125008. https://doi.org/10.1016/j.biortech.2021.125008
Li Y, Xu Y, Liu L, Li P, Yan Y, Chen T, Zheng T, Wang H (2017) Flocculation mechanism of Aspergillus niger on harvesting of Chlorella vulgaris biomass. Algal Res 25:402–412. https://doi.org/10.1016/j.algal.2017.06.001
Li L, Liang T, Liu W, Liu Y, Ma F (2020a) A comprehensive review of the mycelial pellet: research status, applications, and future prospects. Ind Eng Chem Res 59(39):16911–16922. https://doi.org/10.1021/acs.iecr.0c01325
Li L, Liu W, Liang T, Ma F (2020b) The adsorption mechanisms of algae-bacteria symbiotic system and its fast formation process. Bioresource Technol 315:123854. https://doi.org/10.1016/j.biortech.2020.123854
Li L, Liang T, Zhao M, Lv Y, Song Z, Sheng T, Ma F (2022a) A review on mycelial pellets as biological carriers: wastewater treatment and recovery for resource and energy. Bioresource Technol 355:127200. https://doi.org/10.1016/j.biortech.2022.127200
Li N, Wang P, Wang S, Wang C, Zhou H, Kapur S, Zhang J, Song Y (2022b) Electrostatic charges on microalgae surface: mechanism and applications. J Environ Chem Eng 10(3):107516. https://doi.org/10.1016/j.jece.2022.107516
Li Y, Nie H, Zhang H, Niu W, Li S, Wang H (2022c) Promotion effect of bacteria in phycosphere on flocculation activity of Aspergillus niger on Synechocystis biomass. Aquaculture 550:737833. https://doi.org/10.1016/j.aquaculture.2021.737833
Lin W, Chen L, Tan Z, Deng Z, Liu H (2022) Application of filamentous fungi in microalgae-based wastewater remediation for biomass harvesting and utilization: from mechanisms to practical application. Algal Res 62:102614. https://doi.org/10.1016/j.algal.2021.102614
Linder MB (2009) Hydrophobins: proteins that self assemble at interfaces. Curr Opin Colloid Interface Sci 14(5):356–363. https://doi.org/10.1016/j.cocis.2009.04.001
Miyazawa K, Yoshimi A, Abe K (2020) The mechanisms of hyphal pellet formation mediated by polysaccharides, α-1,3-glucan and galactosaminogalactan, in Aspergillus species. Fungal Biol Biotechnol 7:10. https://doi.org/10.1186/s40694-020-00101-4
Nasir NM, Yunos FHM, Jusoh HHW, Mohammad A, Lam SS, Jusoh A (2019) Subtopic: advances in water and wastewater treatment harvesting of Chlorella sp. microalgae using Aspergillus niger as bio-flocculant for aquaculture wastewater treatment. J Environ Manage 249:109373. https://doi.org/10.1016/j.jenvman.2019.109373
Nyyssola A, Suhonen A, Ritala A, Oksman-Caldentey K-M (2022) The role of single cell protein in cellular agriculture. Curr Opin Biotechnol 75:102686. https://doi.org/10.1016/j.copbio.2022.102686
Patel AK, Albarico FPJB, Perumal PK, Vadrale AP, Nian CT, Chau HTB, Anwar C, Wani HMUD, Pal A, Saini R, Ha LH, Senthilkumar B, Tsang Y-S, Chen C-W, Dong C-D, Singhania RR (2022) Algae as an emerging source of bioactive pigments. Bioresource Technol 351:126910. https://doi.org/10.1016/j.biortech.2022.126910
Pei X-Y, Ren H-Y, Liu B-F (2021) Flocculation performance and mechanism of fungal pellets on harvesting of microalgal biomass. Bioresource Technol 321:124463. https://doi.org/10.1016/j.biortech.2020.124463
Priegnitz BE, Wargenau A, Brandt U, Rohde M, Dietrich S, Kwade A, Krull R, Fleissner A (2012) The role of initial spore adhesion in pellet and biofilm formation in Aspergillus niger. Fungal Genet Biol 49(1):30–38. https://doi.org/10.1016/j.fgb.2011.12.002
Rosero-Chasoy G, Rodríguez-Jasso RM, Aguilar CN, Buitrón G, Chairez I, Ruiz HA (2021) Microbial co-culturing strategies for the production high value compounds, a reliable framework towards sustainable biorefinery implementation—an overview. Bioresource Technol 321:124458. https://doi.org/10.1016/j.biortech.2020.124458
Sadovskaya I, Guérardel Y (2019) Simple protocol to purify cell wall polysaccharide from gram-positive bacteria and assess its structural integrity. Methods Mol Biol 1954:37–45. https://doi.org/10.1007/978-1-4939-9154-9_4
Satpati GG, Dikshit PK, Mal N, Pal R, Sherpa KC, Rajak RC, Rather S-U, Raghunathan S, Davoodbasha M (2023) A state of the art review on the co-cultivation of microalgae-fungi in wastewater for biofuel production. Sci Total Environ 870:161828. https://doi.org/10.1016/j.scitotenv.2023.161828
Shu L, Li J, Xu J, Zheng Z (2023) Nutrient removal and biogas upgrade using co-cultivation of Chlorella vulgaris and three different bacteria under various GR24 concentrations by induction with 5-deoxystrigol. World J Microbiol Biotechnol 39(9):245. https://doi.org/10.1007/s11274-023-03647-8
Singh T, Saikia R, Jana T, Arora DK (2004) Hydrophobicity and surface electrostatic charge of conidia of the mycoparasitic Trichoderma species. Mycol Prog 3(3):219–228
Smith SN, Chohan R, Armstrong RA, Whipps JM (1998) Hydrophobicity and surface electrostatic charge of conidia of the mycoparasite Coniothyrium minitans. Mycol Res 102:243–249. https://doi.org/10.1017/s0953756297004796
Srinuanpan S, Chawpraknoi A, Chantarit S, Cheirsilp B, Prasertsan P (2018) A rapid method for harvesting and immobilization of oleaginous microalgae using pellet-forming filamentous fungi and the application in phytoremediation of secondary effluent. Int J Phytoremediation 20(10):1017–1024. https://doi.org/10.1080/15226514.2018.1452187
Valsecchi I, Lai JI, Stephen-Victor E, Pillé A, Beaussart A, Lo V, Pham CLL, Aimanianda V, Kwan AH, Duchateau M, Gianetto QG, Matondo M, Lehoux M, Sheppard DC, Dufrene YF, Bayry J, Guijarro JI, Sunde M, Latgé JP (2019) Assembly and disassembly of Aspergillus fumigatus conidial rodlets. Cell Surf 5:100023. https://doi.org/10.1016/j.tcsw.2019.100023
Vandamme D, Foubert I, Fraeye I, Meesschaert B, Muylaert K (2012) Flocculation of Chlorella vulgaris induced by high pH: Role of magnesium and calcium and practical implications. Bioresour Technol 105:114–119. https://doi.org/10.1016/j.biortech.2011.11.105
Wang J, Chen R, Fan L, Cui L, Zhang Y, Cheng J, Wu X, Zeng W, Tian Q, Shen L (2021) Construction of fungi-microalgae symbiotic system and adsorption study of heavy metal ions. Sep Purif Technol 268:118689. https://doi.org/10.1016/j.seppur.2021.118689
Wang S-K, Yang K-X, Zhu Y-R, Zhu X-Y, Nie D-F, Jiao N, Angelidaki I (2022) One-step co-cultivation and flocculation of microalgae with filamentous fungi to valorize starch wastewater into high-value biomass. Bioresour Technol 361:127625. https://doi.org/10.1016/j.biortech.2022.127625
Wargenau A, Fleißner A, Bolten CJ, Rohde M, Kampen I, Kwade A (2011) On the origin of the electrostatic surface potential of Aspergillus niger spores in acidic environments. Res Microbiol 162(10):1011–1017
Yang L, Li H, Wang Q (2019) A novel one-step method for oil-rich biomass production and harvesting by co-cultivating microalgae with filamentous fungi in molasses wastewater. Bioresource Technol 275:35–43. https://doi.org/10.1016/j.biortech.2018.12.036
Zamalloa C, Gultom SO, Rajendran A, Hu B (2017) Ionic effects on microalgae harvest via microalgae-fungi co-pelletization. Biocatal Agric Biotechnol 9:145–155. https://doi.org/10.1016/j.bcab.2016.12.007
Zhang J, Hu B (2012) A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. Bioresource Technol 114:529–535. https://doi.org/10.1016/j.biortech.2012.03.054
Zhang J, Zhang J (2016) The filamentous fungal pellet and forces driving its formation. Crit Rev Biotechnol 36(6):1066–1077. https://doi.org/10.3109/07388551.2015.1084262
Zhang Y, Ouyang L, Nan Y, Chu J (2019) Efficient gene deletion and replacement in Aspergillus niger by modified in vivo CRISPR/Cas9 systems. Bioresour Bioprocess 6(1):4. https://doi.org/10.1186/s40643-019-0239-7
Zheng X, Zheng P, Zhang K, Cairns TC, Meyer V, Sun J, Ma Y (2019) 5S rRNA promoter for guide RNA expression enabled highly efficient CRISPR/Cas9 genome editing in Aspergillus niger. ACS Synth Biol 8(7):1568–1574. https://doi.org/10.1021/acssynbio.7b00456
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This work was supported by the International Science and Technology Cooperation Foundation of Shanghai (Grant No. 19230742900).
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XZ and ZJ conceived the study. XZ performed all the experiments and drafted the original manuscript. WC and MW monitored methodology validation part, supervised the experiments. SG, HZ and JG prepared, reviewed, and edited the manuscript.
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Zheng, X., Cong, W., Gultom, S.O. et al. Manipulation of co-pelletization for Chlorela vulgaris harvest by treatment of Aspergillus niger spore. World J Microbiol Biotechnol 40, 83 (2024). https://doi.org/10.1007/s11274-023-03878-9
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DOI: https://doi.org/10.1007/s11274-023-03878-9