Exploring The Potential of Microalgae-Fungi Co-Cultivation for Sustainable Bioprocessing in Microalgae Biorefinery

Muhammad Hizbullahi Usman; Mohd Farizal  Kamaroddin; Mohd Helmi Sani; Nik Ahmad Nizam Nik Malek

doi:10.55230/mabjournal.v52i6.2783

Authors

Muhammad Hizbullahi Usman Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia; Department of Microbiology, Faculty of Science, Sokoto State University (SSU), Sokoto State, Nigeria https://orcid.org/0000-0003-4567-1011
Mohd Farizal Kamaroddin
farizal@utm.my
Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia https://orcid.org/0000-0003-3838-5463
Mohd Helmi Sani Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia
Nik Ahmad Nizam Nik Malek Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia; Center for Sustainable Nanomaterials (CSNano), Ibnu Sina Institute for Scientific and Industrial Research (ISI-ISIR), Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia

Keywords:

Microalgae, fungi, co-cultivation, bioflocculation, wastewater, biofuels

Abstract

Developing co-cultivation systems involving microalgae and fungi has shown promising potential for microalgae harvesting technology. As discussed in this review, the co-cultivation of microalgae and fungi has emerged as a novel approach for enhancing biomass and lipid production, wastewater treatment, biofuel production, and high-value products. However, despite being used for a few years, this technique is still in its early stages of development and has yet to be widely applied in the industry. The main challenges associated with co-cultivation include designing effective cultivation systems, managing nutrient requirements, selecting compatible strains, and implementing contamination control measures. In this study, bibliometric analysis was conducted (using the Web of Science database) to examine global trends and developments in microalgae-fungi co-cultivation research between 2014 and 2023, which aimed to identify the research progression, prominent contributors, and leading countries in the research field. The dataset comprised 682 articles, 242 reviews, 31 book chapters, and 22 conference papers. The results showed a rapid increment of publications with China as an active nation in this research area, followed by India, the USA, Italy, Spain, etc. As demonstrated in this study, the immense potential of co-cultivation techniques suggests further exploration, particularly in employing different microalgae species with exceptional characteristics in conjunction with non-pathogenic and edible fungi for profitable industrialization.

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Author Biographies

Mohd Farizal Kamaroddin, Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia

Bioscience and Senior Lecturer

Nik Ahmad Nizam Nik Malek, Department of Bioscience, Faculty of Science, Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia; Center for Sustainable Nanomaterials (CSNano), Ibnu Sina Institute for Scientific and Industrial Research (ISI-ISIR), Universiti Teknologi Malaysia (UTM), 81310 Johor Bahru, Johor Malaysia

Assoc. Prof. Ts. ChM. Dr. Nik Ahmad Nizam Nik Malek Bioscience

References

Abyar, H., Younesi, H., Bahramifar, N. & Zinatizadeh, A.A. 2018. Biological CNP removal from meat-processing wastewater in an innovative high rate up-flow A2O bioreactor. Chemosphere, 213: 197–204. DOI: https://doi.org/10.1016/j.chemosphere.2018.09.047

Alam, M.A., Wan, C., Tran, D.T., Mofijur, M., Ahmed, S.F., Mehmood, M.A., Shaik, F., Vo, D.V.N. & Xu, J. 2022. Microalgae binary culture for higher biomass production, nutrients recycling, and efficient harvesting: A review. Environmental Chemistry Letters, 20(2): 1153–1168. DOI: https://doi.org/10.1007/s10311-021-01363-z

Alishahi, M., Karamifar, M. & Mesbah, M. 2015. Effects of astaxanthin and Dunaliella salina on skin carotenoids, growth performance and immune response of Astronotus ocellatus. Aquaculture International, 23(5): 1239–1248. DOI: https://doi.org/10.1007/s10499-015-9880-0

Azarpour, A., Zendehboudi, S., Mohammadzadeh, O., Rajabzadeh, A.R. & Chatzis, I. 2022. A review on microalgal biomass and biodiesel production through Co-cultivation strategy. Energy Conversion and Management, 267: 1–35. DOI: https://doi.org/10.1016/j.enconman.2022.115757

Bader, J., Mast-Gerlach, E., Popović, M.K., Bajpai, R. & Stahl, U. 2010. Relevance of microbial coculture fermentations in biotechnology. Journal of Applied Microbiology, 109(2): 371–387. DOI: https://doi.org/10.1111/j.1365-2672.2009.04659.x

Bansfield, D., Spilling, K., Mikola, A. & Piiparinen, J. 2021. Bioflocculation of Euglena gracilis via direct application of fungal filaments: a rapid harvesting method. Journal of Applied Phycology, 34(1): 321–334. DOI: https://doi.org/10.1007/s10811-021-02651-5

Bhattacharya, A., Mathur, M., Kumar, P., Prajapati, S.K. & Malik, A. 2017. A rapid method for fungal assisted algal flocculation: Critical parameters & mechanism insights. Algal Research, 21: 42–51. DOI: https://doi.org/10.1016/j.algal.2016.10.022

Bibi, F., Jamal, A., Huang, Z., Urynowicz, M. & Ishtiaq Ali, M. 2022. Advancement and role of abiotic stresses in microalgae biorefinery with a focus on lipid production. Fuel, 316: 1–13. DOI: https://doi.org/10.1016/j.fuel.2022.123192

Bukar, U.A., Sayeed, M.S., Razak, S.F.A., Yogarayan, S., Amodu, O.A. & Mahmood, R.A.R. 2023. A method for analyzing text using VOSviewer. MethodsX, 11: 102339. DOI: https://doi.org/10.1016/j.mex.2023.102339

Cai, W., Zhao, Z., Li, D., Lei, Z., Zhang, Z. & Lee, D.J. 2019. Algae granulation for nutrients uptake and algae harvesting during wastewater treatment. Chemosphere, 214: 55–59. DOI: https://doi.org/10.1016/j.chemosphere.2018.09.107

Chen, J., Leng, L., Ye, C., Lu, Q., Addy, M., Wang, J., Liu, J., Chen, P., Ruan, R. & Zhou, W. 2018. A comparative study between fungal pellet- and spore-assisted microalgae harvesting methods for algae bioflocculation. Bioresource Technology, 259: 181–190. DOI: https://doi.org/10.1016/j.biortech.2018.03.040

Chen, X., Zou, D., Xie, H. & Wang, F. L. 2021. Past, present, and future of smart learning: a topic-based bibliometric analysis. International Journal of Educational Technology in Higher Education, 18(1): 1–29. DOI: https://doi.org/10.1186/s41239-020-00239-6

Cheng, P., Cheng, J.J., Cobb, K., Zhou, C., Zhou, N., Addy, M., Chen, P., Yan, X. & Ruan, R. 2020. Tribonema sp. and Chlorella zofingiensis co-culture to treat swine wastewater diluted with fishery wastewater to facilitate harvest. Bioresource Technology, 297: 122516. DOI: https://doi.org/10.1016/j.biortech.2019.122516

Choi, Y.N., Cho, H.U., Utomo, J.C., Shin, D.Y., Kim, H.K. & Park, J.M. 2016. Efficient harvesting of Synechocystis sp. PCC 6803 with filamentous fungal pellets. Journal of Applied Phycology, 28(4): 2225–2231. DOI: https://doi.org/10.1007/s10811-015-0787-y

Chu, R., Li, S., Yin, Z., Hu, D., Zhang, L., Xiang, M. & Zhu, L. 2021. A fungal immobilization technique for efficient harvesting of oleaginous microalgae: Key parameter optimization, mechanism exploration and spent medium recycling. Science of the Total Environment, 790: 148174. DOI: https://doi.org/10.1016/j.scitotenv.2021.148174

Coulombier, N., Nicolau, E., Le Déan, L., Barthelemy, V., Schreiber, N., Brun, P., Lebouvier, N. & Jauffrais, T. 2020. Effects of nitrogen availability on the antioxidant activity and carotenoid content of the microalgae Nephroselmis sp. Marine Drugs, 18(9): 453. DOI: https://doi.org/10.3390/md18090453

da Silva, T.L. & Reis, A. 2015. Scale-up Problems for the Large Scale Production of Algae BT. In: Algal Biorefinery: An Integrated Approach. D. Das (Ed.). Springer International Publishing. pp. 125–149. DOI: https://doi.org/10.1007/978-3-319-22813-6_6

Das, P.K., Rani, J., Rawat, S. & Kumar, S. 2022. Microalgal co-cultivation for biofuel production and bioremediation: Current status and benefits. Bioenergy Research, 15(1): 1–26. DOI: https://doi.org/10.1007/s12155-021-10254-8

Dash, A. & Banerjee, R. 2017. Enhanced biodiesel production through phyco-myco co-cultivation of Chlorella minutissima and Aspergillus awamori: An integrated approach. Bioresource Technology, 238: 502–509. DOI: https://doi.org/10.1016/j.biortech.2017.04.039

Dawood, M.A.O., Eweedah, N.M., Khalafalla, M.M. & Khalid, A. 2020. Evaluation of fermented date palm seed meal with Aspergillus oryzae on the growth, digestion capacity and immune response of Nile tilapia (Oreochromis niloticus). Aquaculture Nutrition, 26(3): 828–841. DOI: https://doi.org/10.1111/anu.13042

Dawood, M.A.O., Eweedah, N.M., Moustafa Moustafa, E. & Shahin, M.G. 2019. Effects of feeding regimen of dietary Aspergillus oryzae on the growth performance, intestinal morphometry and blood profile of Nile tilapia (Oreochromis niloticus). Aquaculture Nutrition, 25(5): 1063–1072. DOI: https://doi.org/10.1111/anu.12923

Dhangar, K. & Kumar, M. 2020. Tricks and tracks in removal of emerging contaminants from the wastewater through hybrid treatment systems: A review. Science of the Total Environment, 738(336): 1–20. DOI: https://doi.org/10.1016/j.scitotenv.2020.140320

Dias, C., Santos, J., Reis, A. & Lopes da Silva, T. 2019. Yeast and microalgal symbiotic cultures using low-cost substrates for lipid production. Bioresource Technology Reports, 7: 100261. DOI: https://doi.org/10.1016/j.biteb.2019.100261

Ding, H., Zhang, X., Yang, H., Luo, X. & Lin, X. 2018. Highly efficient extraction of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization. Chemical Engineering Journal, 368: 37–50. DOI: https://doi.org/10.1016/j.cej.2019.02.116

Donthu, N., Kumar, S. & Pattnaik, D. 2020. Forty-five years of Journal of Business Research: A bibliometric analysis. Journal of Business Research, 109: 1–14. DOI: https://doi.org/10.1016/j.jbusres.2019.10.039

Dossou, S., Koshio, S., Ishikawa, M., Yokoyama, S., Dawood, M. A. O., El Basuini, M.F., Olivier, A. & Zaineldin, A.I. 2018. Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish and Shellfish Immunology, 75: 253–262. DOI: https://doi.org/10.1016/j.fsi.2018.01.032

Du, Z.Y., Alvaro, J., Hyden, B., Zienkiewicz, K., Benning, N., Zienkiewicz, A., Bonito, G. & Benning, C. 2018. Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata. Biotechnology for Biofuels, 11: 174. DOI: https://doi.org/10.1186/s13068-018-1172-2

Egede, E.J., Jones, H., Cook, B., Purchase, D. & Mouradov, A. 2016. Application of microalgae and fungal-microalgal associations for wastewater treatment. In: Fungal Applications in Sustainable Environmental Biotechnology. D. Purchase (Ed.). Springer International Publishing Switzerland. pp. 143-181. DOI: https://doi.org/10.1007/978-3-319-42852-9_7

Fayyaz, M., Chew, K.W., Show, P. L., Ling, T.C., Ng, I.S. & Chang, J.S. 2020. Genetic engineering of microalgae for enhanced biorefinery capabilities. Biotechnology Advances, 43: 1–13. DOI: https://doi.org/10.1016/j.biotechadv.2020.107554

Feng, H., Sun, C., Zhang, C., Chang, H., Zhong, N., Wu, W., Wu, H., Tan, X., Zhang, M. & Ho, S.H. 2022. Bioconversion of mature landfill leachate into biohydrogen and volatile fatty acids via microalgal photosynthesis together with dark fermentation. Energy Conversion and Management, 252: 115035. DOI: https://doi.org/10.1016/j.enconman.2021.115035

Gao, S., Hu, C., Sun, S., Xu, J., Zhao, Y. & Zhang, H. 2018. Performance of piggery wastewater treatment and biogas upgrading by three microalgal cultivation technologies under different initial COD concentration. Energy, 165: 360–369. DOI: https://doi.org/10.1016/j.energy.2018.09.190

Gao, Z., Jiang, C., Lyu, R., Yang, Z. & Zhang, T. 2020. Optimization of the preparation of fungal-algal pellets for use in the remediation of arsenic-contaminated water. Environmental Science and Pollution Research, 27(29): 36789–36798. DOI: https://doi.org/10.1007/s11356-020-09757-2

Gonçalves, A.L., Pires, J.C.M. & Simões, M. 2017. A review on the use of microalgal consortia for wastewater treatment. Algal Research, 24: 403–415. DOI: https://doi.org/10.1016/j.algal.2016.11.008

Gopal, G., Kumar, P., Mal, N., Pal, R. & Chhunji, K. 2023. Science of the Total Environment A state of the art review on the co-cultivation of microalgae-fungi in wastewater for biofuel production. Science of the Total Environment, 870: 161828. DOI: https://doi.org/10.1016/j.scitotenv.2023.161828

Goswami, R. K., Mehariya, S., Verma, P., Lavecchia, R. & Zuorro, A. 2021. Microalgae-based biorefineries for sustainable resource recovery from wastewater. Journal of Water Process Engineering, 40: 101747. DOI: https://doi.org/10.1016/j.jwpe.2020.101747

Guo, G., Cao, W., Sun, S., Zhao, Y. & Hu, C. 2017. Nutrient removal and biogas upgrading by integrating fungal–microalgal cultivation with anaerobically digested swine wastewater treatment. Journal of Applied Phycology, 29(6): 2857–2866. DOI: https://doi.org/10.1007/s10811-017-1207-2

Guo, G., Guan, J., Sun, S., Liu, J. & Zhao, Y. 2020. Nutrient and heavy metal removal from piggery wastewater and CH4 enrichment in biogas based on microalgae cultivation technology under different initial inoculum concentration. Water Environment Research, 92(6): 922–933. DOI: https://doi.org/10.1002/wer.1287

Hadiyanto, H., Widayat, W., Christwardana, M. & Pratiwi, M.E. 2022. The flocculation process of Chlorella sp. using chitosan as a bio-flocculant: Optimization of operating conditions by response surface methodology. Current Research in Green and Sustainable Chemistry, 5(February): 100291. DOI: https://doi.org/10.1016/j.crgsc.2022.100291

Han, P., Lu, Q., Fan, L. & Zhou, W. 2019. A review on the use of microalgae for sustainable aquaculture. Applied Sciences (Switzerland), 9(11): 1–20. DOI: https://doi.org/10.3390/app9112377

He, J., Ding, W., Han, W., Chen, Y., Jin, W. & Zhou, X. 2021. A bacterial strain Citrobacter W4 facilitates the bio-flocculation of wastewater cultured microalgae Chlorella pyrenoidosa. Science of the Total Environment, 806: 151336. DOI: https://doi.org/10.1016/j.scitotenv.2021.151336

Hwang, S. W., Choi, H. Il & Sim, S.J. 2019. Acidic cultivation of Haematococcus pluvialis for improved astaxanthin production in the presence of a lethal fungus. Bioresource Technology, 278: 138–144. DOI: https://doi.org/10.1016/j.biortech.2019.01.080

Jaiswal, K.K., Kumar, V., Gururani, P., Vlaskin, M.S., Parveen, A., Nanda, M., Kurbatova, A., Gautam, P. & Grigorenko, A.V. 2022. Bio-flocculation of oleaginous microalgae integrated with municipal wastewater treatment and its hydrothermal liquefaction for biofuel production. Environmental Technology and Innovation, 26: 102340. DOI: https://doi.org/10.1016/j.eti.2022.102340

Ji, X., Jiang, M., Zhang, J., Jiang, X. & Zheng, Z. 2018. The interactions of algae-bacteria symbiotic system and its effects on nutrients removal from synthetic wastewater. Bioresource Technology, 247: 44–50. DOI: https://doi.org/10.1016/j.biortech.2017.09.074

Jiang, M., Li, H., Zhou, Y. & Zhang, J. 2019. The interactions of an algae–fungi symbiotic system influence nutrient removal from synthetic wastewater. Journal of Chemical Technology and Biotechnology, 94(12): 3993–3999. DOI: https://doi.org/10.1002/jctb.6205

Khan, M.I., Shin, J.H. & Kim, J.D. 2018. The promising future of microalgae: Current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microbial Cell Factories, 17: 36. DOI: https://doi.org/10.1186/s12934-018-0879-x

Khoo, K.S., Chew, K.W., Yew, G.Y., Leong, W.H., Chai, Y.H., Show, P.L. & Chen, W.H. 2020. Recent advances in downstream processing of microalgae lipid recovery for biofuel production. Bioresource Technology, 304: 122996. DOI: https://doi.org/10.1016/j.biortech.2020.122996

Kulkarni, S., Nene, S. & Joshi, K. 2017. Production of Hydrophobins from fungi. Process Biochemistry, 61: 1–11. DOI: https://doi.org/10.1016/j.procbio.2017.06.012

Kumar, G., Shekh, A., Jakhu, S., Sharma, Y., Kapoor, R. & Sharma, T. R. 2020. Bioengineering of microalgae: Recent advances, perspectives, and regulatory challenges for industrial application. Frontiers in Bioengineering and Biotechnology, 8: 1–31. DOI: https://doi.org/10.3389/fbioe.2020.00914

Laezza, C., Salbitani, G. & Carfagna, S. 2022. Fungal contamination in microalgal cultivation: biological and biotechnological aspects of fungi-microalgae interaction. Journal of Fungi, 8(10): 48–54. DOI: https://doi.org/10.3390/jof8101099

Lal, A., Banerjee, S. & Das, D. 2021. Aspergillus sp. assisted bioflocculation of Chlorella MJ 11/11 for the production of biofuel from the algal-fungal co-pellet. Separation and Purification Technology, 272: 118320. DOI: https://doi.org/10.1016/j.seppur.2021.118320

Lau, Z. L., Low, S. S., Ezeigwe, E. R., Chew, K. W., Chai, W. S., Bhatnagar, A., Yap, Y. J. & Show, P. L. 2022. A review on the diverse interactions between microalgae and nanomaterials: Growth variation, photosynthetic performance and toxicity. Bioresource Technology, 351: 127048. DOI: https://doi.org/10.1016/j.biortech.2022.127048

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 Technology, 330: 125008. DOI: https://doi.org/10.1016/j.biortech.2021.125008

Leng, L., Yang, L., Chen, J., Leng, S., Li, H., Li, H., Yuan, X., Zhou, W. & Huang, H. 2020. A review on pyrolysis of protein-rich biomass: Nitrogen transformation. Bioresource Technology, 315: 123801. DOI: https://doi.org/10.1016/j.biortech.2020.123801

Li, T., Jiang, L., Hu, Y., Paul, J.T., Zuniga, C., Zengler, K. & Betenbaugh, M.J. 2020. Creating a synthetic lichen : Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413. Algal Research, 45: 101755. DOI: https://doi.org/10.1016/j.algal.2019.101755

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 Research, 25: 402–412. DOI: https://doi.org/10.1016/j.algal.2017.06.001

Lian, J., Wijffels, R.H., Smidt, H. & Sipkema, D. 2018. The effect of the algal microbiome on industrial production of microalgae. Microbial Biotechnology, 11(5): 806–818. DOI: https://doi.org/10.1111/1751-7915.13296

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 Research, 62: 102614. DOI: https://doi.org/10.1016/j.algal.2021.102614

Liu, X. 2020. Microbial technology for the sustainable development of energy and environment. Biotechnology Reports, 27: e00486. DOI: https://doi.org/10.1016/j.btre.2020.e00486

Liu, X., Xing, X., Dong, Q., Liu, W. & Li, W. 2022. Efficient removal of nitrogen/ phosphorous by mix-cultivation of Haematococcus pluvialis and Simplicillium lanosoniveum in wastewater supplemented with NaHCO3. Biochemical Engineering Journal, 182: 108433. DOI: https://doi.org/10.1016/j.bej.2022.108433

Luo, S., Wu, X., Jiang, H., Yu, M., Liu, Y., Min, A., Li, W. & Ruan, R. 2019. Edible fungi-assisted harvesting system for efficient microalgae bio-flocculation. Bioresource Technology, 282: 325–330. DOI: https://doi.org/10.1016/j.biortech.2019.03.033

Epstein, L. & Nicholson, R. 2016. Adhesion and adhesives of fungi and oomycetes. In: Biological Adhesives. A.M. Smith (Ed.). Springer. pp. 25-55. DOI: https://doi.org/10.1007/978-3-319-46082-6_2

Martínez, M.E., Jiménez, J.M. & El Yousfi, F. 1999. Influence of phosphorus concentration and temperature on growth and phosphorus uptake by the microalga Scenedesmus obliquus. Bioresource Technology, 67(3): 233–240. DOI: https://doi.org/10.1016/S0960-8524(98)00120-5

Mathushika, J. & Gomes, C. 2022. Development of microalgae-based biofuels as a viable green energy source: challenges and future perspectives. Biointerface Research in Applied Chemistry, 12: 3849–3882. DOI: https://doi.org/10.33263/BRIAC123.38493882

Matter, I.A., Hoang Bui, V.K., Jung, M., Seo, J.Y., Kim, Y.E., Lee, Y.C. & Oh, Y.K. 2019. Flocculation harvesting techniques for microalgae: A review. Applied Sciences, 9(15): 3069. DOI: https://doi.org/10.3390/app9153069

Miranda, A.F., Taha, M., Wrede, D., Morrison, P., Ball, A.S., Stevenson, T. & Mouradov, A. 2015. Lipid production in association of filamentous fungi with genetically modified cyanobacterial cells. Biotechnology for Biofuels, 8: 179. DOI: https://doi.org/10.1186/s13068-015-0364-2

Mohan, K., Padmanaban, A.M., Uthayakumar, V., Chandirasekar, R., Muralisankar, T. & Santhanam, P. 2016. Effect of dietary Ganoderma lucidum polysaccharides on biological and physiological responses of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture, 464: 42–49. DOI: https://doi.org/10.1016/j.aquaculture.2016.05.046

Mohd Nasir, N., Mohd Yunos, F.H., Wan Jusoh, H.H., Mohammad, A., Lam, S.S. & 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. Journal of Environmental Management, 249: 1–7. DOI: https://doi.org/10.1016/j.jenvman.2019.109373

Morales, M., Aflalo, C. & Bernard, O. 2021. Microalgal lipids: A review of lipids potential and quantification for 95 phytoplankton species. Biomass and Bioenergy, 150: 1–25. DOI: https://doi.org/10.1016/j.biombioe.2021.106108

Muhammad, G., Douglas, A., Ngatcha, P., Lv, Y., Xiong, W., El-badry, Y. A., Asmatulu, E., Xu, J. & Alam, A. 2022. Enhanced biodiesel production from wet microalgae biomass optimized via response surface methodology and artificial neural network. Renewable Energy, 184: 753–764. DOI: https://doi.org/10.1016/j.renene.2021.11.091

Mujtaba, G. & Lee, K. 2017. Treatment of real wastewater using co-culture of immobilized Chlorella vulgaris and suspended activated sludge. Water Research, 120: 174–184. DOI: https://doi.org/10.1016/j.watres.2017.04.078

Muradov, N., Taha, M., Miranda, A.F., Wrede, D., Kadali, K., Gujar, A., Stevenson, T., Ball, A.S. & Mouradov, A. 2015. Fungal-assisted algal flocculation: Application in wastewater treatment and biofuel production. Biotechnology for Biofuels, 8: 24. DOI: https://doi.org/10.1186/s13068-015-0210-6

Musa, M., Doshi, A., Brown, R. & Rainey, T. J. 2019. Microalgae dewatering for biofuels: A comparative techno-economic assessment using single and two-stage technologies. Journal of Cleaner Production, 229: 325–336. DOI: https://doi.org/10.1016/j.jclepro.2019.05.039

Nazari, M.T., Rigueto, C.V.T., Rempel, A. & Colla, L.M. 2021. Harvesting of Spirulina platensis using an eco-friendly fungal bioflocculant produced from agro-industrial by-products. Bioresource Technology, 322(October 2020): 124525. DOI: https://doi.org/10.1016/j.biortech.2020.124525

Nguyen, M.K., Moon, J.Y., Bui, V.K.H., Oh, Y.K. & Lee, Y.C. 2019. Recent advanced applications of nanomaterials in microalgae biorefinery. Algal Research, 41: 101522. DOI: https://doi.org/10.1016/j.algal.2019.101522

Ogawa, M., Bisson, L.F., García-Martínez, T., Mauricio, J.C. & Moreno-García, J. 2019. New insights on yeast and filamentous fungus adhesion in a natural co-immobilization system: Proposed advances and applications in wine industry. Applied Microbiology and Biotechnology, 103(12): 4723–4731. DOI: https://doi.org/10.1007/s00253-019-09870-4

Ogbonna, C.N. & Nwoba, E.G. 2021. Bio-based flocculants for sustainable harvesting of microalgae for biofuel production. A review. Renewable and Sustainable Energy Reviews, 139: 110690. DOI: https://doi.org/10.1016/j.rser.2020.110690

Omoregie, A.I., Muda, K., Ojuri, O.O., Hong, C.Y., Pauzi, F.M. & Ali, N.S.B.A. 2022. The global research trend on microbially induced carbonate precipitation during 2001–2021: A bibliometric review. Environmental Science and Pollution Research, 29(60): 89899–89922. DOI: https://doi.org/10.1007/s11356-022-24046-w

Padmaperuma, G., Kapoore, R. V., Gilmour, D. J. & Vaidyanathan, S. 2018. Microbial consortia: A critical look at microalgae co-cultures for enhanced biomanufacturing. Critical Reviews in Biotechnology, 38(5): 690–703. DOI: https://doi.org/10.1080/07388551.2017.1390728

Padri, M., Boontian, N., Teaumroong, N., Piromyou, P. & Piasai, C. 2022. Application of Aspergillus niger F5 as an alternative technique to harvest microalgae and as a phosphorous removal treatment for cassava biogas effluent wastewater. Journal of Water Process Engineering, 46: 1–13. DOI: https://doi.org/10.1016/j.jwpe.2021.102524

Pei, X.Y., Ren, H.Y. & Liu, B.F. 2021. Flocculation performance and mechanism of fungal pellets on harvesting of microalgal biomass. Bioresource Technology, 321(October 2020): 124463. DOI: https://doi.org/10.1016/j.biortech.2020.124463

Pereira, A.G., Otero, P., Echave, J., Carreira-Casais, A., Chamorro, F., Collazo, N., Jaboui, A., Lourenço-Lopes, C., Simal-Gandara, J. & Prieto, M.A. 2021. Xanthophylls from the Sea: Algae as Source of Bioactive Carotenoids. Marine Drugs, 19(4): 188. DOI: https://doi.org/10.3390/md19040188

Piercey-Normore, M.D. & Athukorala, S.N.P. 2017. Interface between fungi and green algae in lichen associations. Botany, 95: 1005–1014. DOI: https://doi.org/10.1139/cjb-2017-0037

Prajapati, S. K., Kumar, P., Malik, A. & Choudhary, P. 2014. Exploring pellet forming filamentous fungi as tool for harvesting non-flocculating unicellular microalgae. Bioenergy Research, 7(4): 1430–1440. DOI: https://doi.org/10.1007/s12155-014-9481-1

Pranckutė, R. 2021. Web of Science (WoS) and Scopus: the titans of bibliographic information in today’s academic world. Publications, 9(1): 12. DOI: https://doi.org/10.3390/publications9010012

Premaratne, M., Kankanamalage, G., Hasara, S., Arachchige, R., Praveen, D., Chamilka, V., Thevarajah, B., Nimarshana, P.H.V, Malik, A. & Ariyadasa, T.U. 2022. Bioresource technology reports resource recovery from waste streams for production of microalgae biomass : A sustainable approach towards high-value biorefineries. Bioresource Technology Reports, 18(March): 101070. DOI: https://doi.org/10.1016/j.biteb.2022.101070

Rahimi, S., Modin, O. & Mijakovic, I. 2020. Technologies for biological removal and recovery of nitrogen from wastewater. Biotechnology Advances, 43: 107570. DOI: https://doi.org/10.1016/j.biotechadv.2020.107570

Ray, A., Nayak, M. & Ghosh, A. 2022. A review on co-culturing of microalgae: A greener strategy towards sustainable biofuels production. Science of the Total Environment, 802: 149765. DOI: https://doi.org/10.1016/j.scitotenv.2021.149765

Rösch, C., Roßmann, M. & Weickert, S. 2019. Microalgae for integrated food and fuel production. GCB Bioenergy, 11(1): 326–334. DOI: https://doi.org/10.1111/gcbb.12579

Sahin, D., Altindag, U.H. & Tas, E. 2018. Enhancement of docosahexaenoic acid (DHA) and beta-carotene production in Schizochytrium sp. using symbiotic relationship with Rhodotorula glutinis. Process Biochemistry, 75: 10–15. DOI: https://doi.org/10.1016/j.procbio.2018.09.004

Senko, O., Stepanov, N., Maslova, O. & Efremenko, E. 2023. Transformation of enzymatic hydrolysates of Chlorella – Fungus mixed biomass into poly (hydroxyalkanoates ). Catalysts, 13(118): 1–18. DOI: https://doi.org/10.3390/catal13010118

Shahid, A., Malik, S., Zhu, H., Xu, J., Nawaz, M.Z., Nawaz, S., Asraful Alam, M. & Mehmood, M.A. 2020. Cultivating microalgae in wastewater for biomass production, pollutant removal, and atmospheric carbon mitigation; A review. Science of the Total Environment, 704: 135303. DOI: https://doi.org/10.1016/j.scitotenv.2019.135303

Singh, G. & Patidar, S. K. 2018. Microalgae harvesting techniques: A review. Journal of Environmental Management, 217: 499–508. DOI: https://doi.org/10.1016/j.jenvman.2018.04.010

Srinuanpan, S., Chawpraknoi, A., Chantarit, S., Cheirsilp, B. & Prasertsan, P. 2018a. A rapid method for harvesting and immobilization of oleaginous microalgae using pellet-forming filamentous fungi and the application in phytoremediation of secondary effluent. International Journal of Phytoremediation, 20(10): 1017–1024. DOI: https://doi.org/10.1080/15226514.2018.1452187

Srinuanpan, S., Cheirsilp, B., Prasertsan, P., Kato, Y. & Asano, Y. 2018b. Photoautotrophic cultivation of oleaginous microalgae and co-pelletization with filamentous fungi for cost-effective harvesting process and improved lipid yield. Aquaculture International, 26(6): 1493–1509. DOI: https://doi.org/10.1007/s10499-018-0300-0

Suchitra, R. & Karthikeyan, S. 2019. Co-cultivation of microalgae with oleaginous yeast for economical biofuel production. Journal of Farm Sciences, 32(2): 125–130.

Sui, Y., Muys, M., Van de Waal, D. B., D’Adamo, S., Vermeir, P., Fernandes, T. V. & Vlaeminck, S. E. 2019. Enhancement of co-production of nutritional protein and carotenoids in Dunaliella salina using a two-phase cultivation assisted by nitrogen level and light intensity. Bioresource Technology, 287: 1–9. DOI: https://doi.org/10.1016/j.biortech.2019.121398

Sun, H., Ren, Y., Lao, Y., Li, X. & Chen, F. 2020. A novel fed-batch strategy enhances lipid and astaxanthin productivity without compromising biomass of Chromochloris zofingiensis. Bioresource Technology, 308, 1–9. DOI: https://doi.org/10.1016/j.biortech.2020.123306

Suparmaniam, U., Lam, M.K., Uemura, Y., Shuit, S.H., Lim, J.W., Show, P.L., Lee, K.T., Matsumura, Y. & Le, P.T.K. 2020. Flocculation of Chlorella vulgaris by shell waste-derived bioflocculants for biodiesel production: Process optimization, characterization and kinetic studies. Science of the Total Environment, 702: 134995. DOI: https://doi.org/10.1016/j.scitotenv.2019.134995

Sutherland, D.L., McCauley, J., Labeeuw, L., Ray, P., Kuzhiumparambil, U., Hall, C., Doblin, M., Nguyen, L.N. & Ralph, P.J. 2021. How microalgal biotechnology can assist with the UN Sustainable Development Goals for natural resource management. Current Research in Environmental Sustainability, 3: 100050. DOI: https://doi.org/10.1016/j.crsust.2021.100050

Szotkowski, M., Byrtusova, D., Haronikova, A., Vysoka, M., Rapta, M., Shapaval, V. & Marova, I. 2019. Study of metabolic adaptation of red yeasts to waste animal fat substrate. Microorganisms, 7(11): 578. DOI: https://doi.org/10.3390/microorganisms7110578

Talukder, M.M.R., Das, P. & Wu, J.C. 2014. Immobilization of microalgae on exogenous fungal mycelium: A promising separation method to harvest both marine and freshwater microalgae. Biochemical Engineering Journal, 91: 53–57. DOI: https://doi.org/10.1016/j.bej.2014.07.001

Tan, J. Sen, Lee, S.Y., Chew, K.W., Lam, M.K., Lim, J. W., Ho, S.H. & Show, P.L. 2020. A review on microalgae cultivation and harvesting, and their biomass extraction processing using ionic liquids. Bioengineered, 11(1): 116–129. DOI: https://doi.org/10.1080/21655979.2020.1711626

Trivedi, J., Aila, M., Bangwal, D.P., Kaul, S. & Garg, M.O. 2015. Algae based biorefinery - How to make sense? Renewable and Sustainable Energy Reviews, 47: 295–307. DOI: https://doi.org/10.1016/j.rser.2015.03.052

Trovão, M., Schüler, L.M., Machado, A., Bombo, G., Navalho, S., Barros, A., Pereira, H., Silva, J., Freitas, F. & Varela, J. 2022. Random Mutagenesis as a Promising Tool for Microalgal Strain Improvement towards Industrial Production. Marine Drugs, 20(440): 1–25. DOI: https://doi.org/10.3390/md20070440

Ummalyma, S.B., Gnansounou, E., Sukumaran, R.K., Sindhu, R., Pandey, A. & Sahoo, D. 2017. Bioflocculation: An alternative strategy for harvesting of microalgae – An overview. Bioresource Technology, 242: 227–235. DOI: https://doi.org/10.1016/j.biortech.2017.02.097

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. Separation and Purification Technology, 268: 118689. DOI: https://doi.org/10.1016/j.seppur.2021.118689

Wang, J.H., Zhuang, L.L., Xu, X.Q., Deantes-Espinosa, V.M., Wang, X.X. & Hu, H.Y. 2018. Microalgal attachment and attached systems for biomass production and wastewater treatment. Renewable and Sustainable Energy Reviews, 92: 331–342. DOI: https://doi.org/10.1016/j.rser.2018.04.081

Wang, J., Tian, Q., Zhou, H., Kang, J., Yu, X. & Shen, L. 2023. Key metabolites and regulatory network mechanisms in co-culture of fungi and microalgae based on metabolomics analysis. Bioresource Technology, 388: 129718. DOI: https://doi.org/10.1016/j.biortech.2023.129718

Wang, L., Yu, T., Ma, F., Vitus, T., Bai, S. & Yang, J. 2019. Novel self-immobilized biomass mixture based on mycelium pellets for wastewater treatment: A review. Water Environment Research, 91(2): 93–100. DOI: https://doi.org/10.1002/wer.1026

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. Bioresource Technology, 361: 127625. DOI: https://doi.org/10.1016/j.biortech.2022.127625

Wang, S., Mukhambet, Y., Esakkimuthu, S. & Abomohra, A.E. 2022. Integrated microalgal biorefinery – Routes, energy, economic and environmental perspectives. Journal of Cleaner Production, 348(May 2020): 131245. DOI: https://doi.org/10.1016/j.jclepro.2022.131245

Wang, Y., Ho, S.H., Cheng, C.L., Nagarajan, D., Guo, W.Q., Lin, C., Li, S., Ren, N. & Chang, J.S. 2017. Nutrients and COD removal of swine wastewater with an isolated microalgal strain Neochloris aquatica CL-M1 accumulating high carbohydrate content used for biobutanol production. Bioresource Technology, 242: 7–14. DOI: https://doi.org/10.1016/j.biortech.2017.03.122

Wang, Z., Zhao, Y., Ge, Z., Zhang, H. & Sun, S. 2016. Selection of microalgae for simultaneous biogas upgrading and biogas slurry nutrient reduction under various photoperiods. Journal of Chemical Technology and Biotechnology, 91(7): 1982–1989. DOI: https://doi.org/10.1002/jctb.4788

Wrede, D., Taha, M., Miranda, A.F., Kadali, K., Stevenson, T., Ball, A.S. & Mouradov, A. 2014. Co-cultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLoS ONE, 9(11): 0113497. DOI: https://doi.org/10.1371/journal.pone.0113497

Xie, S., Sun, S., Dai, S.Y. & S.Yuan, J. 2013. Efficient coagulation of microalgae in cultures with filamentous fungi. Algal Research, 2(1); 28–33. DOI: https://doi.org/10.1016/j.algal.2012.11.004

Yan, R., Xing, X., Dong, Q., Yu, X. & Shi, K. 2021. Enhancing algal biomass, lipid and astaxanthin production by mix-cultivation of. Applied Biochemistry and Biotechnology, 1–25. DOI: https://doi.org/10.21203/rs.3.rs-180975/v1

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 Technology, 275: 35–43. DOI: https://doi.org/10.1016/j.biortech.2018.12.036

Yao, S., Lyu, S., An, Y., Lu, J., Gjermansen, C. & Schramm, A. 2019. Microalgae–bacteria symbiosis in microalgal growth and biofuel production: A review. Journal of Applied Microbiology, 126(2): 359–368. DOI: https://doi.org/10.1111/jam.14095

Yen, H.W., Chen, P.W. & Chen, L.J. 2015. The synergistic effects for the co-cultivation of oleaginous yeast-Rhodotorula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresource Technology, 184: 148–152. DOI: https://doi.org/10.1016/j.biortech.2014.09.113

Zamalloa, C., Gultom, S.O., Rajendran, A. & Hu, B. 2017. Ionic effects on microalgae harvest via microalgae-fungi co-pelletization. Biocatalysis and Agricultural Biotechnology, 9: 145–155. DOI: https://doi.org/10.1016/j.bcab.2016.12.007

Zhang, H., Zhao, Z., Kang, P., Wang, Y., Feng, J., Jia, J. & Zhang, Z. 2018. Biological nitrogen removal and metabolic characteristics of a novel aerobic denitrifying fungus Hanseniaspora uvarum strain KPL108. Bioresource Technology, 267: 569–577. DOI: https://doi.org/10.1016/j.biortech.2018.07.073

Zhang, J. & Hu, B. 2012. A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. Bioresource Technology, 114: 529–535. DOI: https://doi.org/10.1016/j.biortech.2012.03.054

Zhang, J., Zhao, C., Sun, S., Zhao, Y. & Liu, J. 2021. Performance of different microalgae-based technologies in nutrient removal and biogas upgrading in response to various GR24 concentrations. International Biodeterioration and Biodegradation, 158: 105166. DOI: https://doi.org/10.1016/j.ibiod.2020.105166

Zhang, S. & Liu, Z. 2021. Advances in the biological fixation of carbon dioxide by microalgae. Journal of Chemical Technology and Biotechnology, 96(6): 1475–1495. DOI: https://doi.org/10.1002/jctb.6714

Zhang, Z., Pang, Z., Xu, S., Wei, T., Song, L., Wang, G., Zhang, J. & Yang, X. 2019. Improved carotenoid productivity and cod removal efficiency by co-culture of Rhodotorula glutinis and Chlorella vulgaris using starch wastewaters as raw material. Applied Biochemistry and Biotechnology, 189(1): 193–205. DOI: https://doi.org/10.1007/s12010-019-03016-y

Zhao, Y., Guo, G., Sun, S., Hu, C. & Liu, J. 2019. Co-pelletization of microalgae and fungi for efficient nutrient purification and biogas upgrading. Bioresource Technology, 289: 121656. DOI: https://doi.org/10.1016/j.biortech.2019.121656

Zhao, Y., Li, Q., Gu, D., Yu, L. & Yu, X. 2022. The synergistic effects of gamma-aminobutyric acid and salinity during the enhancement of microalgal lipid production in photobioreactors. Energy Conversion and Management, 267: 115928. DOI: https://doi.org/10.1016/j.enconman.2022.115928

Zhou, K., Zhang, Y. & Jia, X. 2018. Co-cultivation of fungal-microalgal strains in biogas slurry and biogas purification under different initial CO2 concentrations. Scientific Reports: 8: 7786. DOI: https://doi.org/10.1038/s41598-018-26141-w

Zhou, W., Cheng, Y., Li, Y., Wan, Y., Liu, Y., Lin, X. & Ruan, R. 2012. Novel fungal pelletization-assisted technology for algae harvesting and wastewater treatment. Applied Biochemistry and Biotechnology, 167(2): 214–228. DOI: https://doi.org/10.1007/s12010-012-9667-y

Zhou, W., Min, M., Hu, B., Ma, X., Liu, Y., Wang, Q., Shi, J., Chen, P. & Ruan, R. 2013. Filamentous fungi assisted bio-flocculation: A novel alternative technique for harvesting heterotrophic and autotrophic microalgal cells. Separation and Purification Technology, 107: 158–165. DOI: https://doi.org/10.1016/j.seppur.2013.01.030

Zorn, S., Carvalho, A., Bento, H., Gambarato, B., Pedro, G., da Silva, A., Gonçalves, R., Da Rós, P. & Silva, M. 2022. Use of fungal mycelium as biosupport in the formation of lichen-like structure: recovery of algal grown in sugarcane molasses for lipid accumulation and balanced fatty acid profile. Membranes, 12(3): 258. DOI: https://doi.org/10.3390/membranes12030258