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Immobilization of Diatom Phaeodactylum tricornutum with Filamentous Fungi and Its Kinetics

  • Tyler J. Barzee (Department of Biosystems and Agricultural Engineering, University of Kentucky) ;
  • Hamed M. El-Mashad (Department of Biological and Agricultural Engineering, University of California Davis) ;
  • Andrew R. Burch (Department of Chemistry, University of California) ;
  • Annaliese K. Franz (Department of Chemistry, University of California) ;
  • Ruihong Zhang (Department of Biological and Agricultural Engineering, University of California Davis)
  • Received : 2022.09.27
  • Accepted : 2022.11.15
  • Published : 2023.02.28

Abstract

Immobilizing microalgae cells in a hyphal matrix can simplify harvest while producing novel mycoalgae products with potential food, feed, biomaterial, and renewable energy applications; however, limited quantitative information to describe the process and its applicability under various conditions leads to difficulties in comparing across studies and scaling-up. Here, we demonstrate the immobilization of both active and heat-deactivated marine diatom Phaeodactylum tricornutum (UTEX 466) using different loadings of fungal pellets (Aspergillus sp.) and model the process through kinetics and equilibrium models. Active P. tricornutum cells were not required for the fungal-assisted immobilization process and the fungal isolate was able to immobilize more than its original mass of microalgae. The Freundlich isotherm model adequately described the equilibrium immobilization characteristics and indicated increased normalized algae immobilization (g algae removed/g fungi loaded) under low fungal pellet loadings. The kinetics of algae immobilization by the fungal pellets were found to be adequately modeled using both a pseudo-second order model and a model previously developed for fungal-assisted algae immobilization. These results provide new insights into the behavior and potential applications of fungal-assisted algae immobilization.

Keywords

Acknowledgement

Support for this work was provided by the California Energy Commission (ARV-15-008). The authors extend their gratitude to Dr. Zhiliang Fan and Dr. Bryan Jenkins for their review and thoughtful comments on an early version of the manuscript, and Sam Hornstein and Lin Cao for their assistance with lab experiments.

References

  1. Mata TM, Martins AA, Caetano NS. 2010. Microalgae for biodiesel production and other applications: a review. Renew. Sustain. Energy Rev. 14: 217-232.  https://doi.org/10.1016/j.rser.2009.07.020
  2. Moreno-Garrido I. 2008. Microalgae immobilization: current techniques and uses. Bioresour. Technol. 99: 3949-3964.  https://doi.org/10.1016/j.biortech.2007.05.040
  3. Caldwell GS, In-Na P, Hart R, Sharp E, Stefanova A, Pickersgill M, et al. 2021. Immobilising microalgae and cyanobacteria as biocomposites: new opportunities to intensify algae biotechnology and bioprocessing. Energies (Basel) 14: 2566. 
  4. Luo S, Wu X, Jiang H, Yu M, Liu Y, Min A, et al. 2019. Edible fungi-assisted harvesting system for efficient microalgae bioflocculation. Bioresour. Technol. 282: 325-330.  https://doi.org/10.1016/j.biortech.2019.03.033
  5. Wang X, Yang C, Yu Y, Zhao Y. 2022. In Situ 3D Bioprinting living photosynthetic scaffolds for autotrophic wound healing. Research (Wash DC) 2022: 9794745. 
  6. 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. Sep. Purif. Technol. 107: 158-165.  https://doi.org/10.1016/j.seppur.2013.01.030
  7. Zhang J, Hu B. 2012. A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. Bioresour. Technol. 114: 529-535.  https://doi.org/10.1016/j.biortech.2012.03.054
  8. Rajendran A, Hu B. 2016. Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures. Biotechnol. Biofuels 9: 1-13.  https://doi.org/10.1186/s13068-015-0423-8
  9. Gultom S, Hu B. 2013. Review of microalgae harvesting via Co-pelletization with filamentous fungus. Energies (Basel) 6: 5921-5939.  https://doi.org/10.3390/en6115921
  10. Al-Hothaly KA, Adetutu EM, Taha M, Fabbri D, Lorenzetti C, Conti R, et al. 2015. Bio-harvesting and pyrolysis of the microalgae Botryococcus braunii. Bioresour. Technol. 191: 117-123.  https://doi.org/10.1016/j.biortech.2015.04.113
  11. Muradov N, Taha M, Miranda AF, Wrede D, Kadali K, Gujar A, et al. 2015. Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production. Biotechnol. Biofuels 8: 24. 
  12. Nasir NM, Bakar NSA, Lananan F, Abdul Hamid SH, Lam SS, Jusoh A. 2015. Treatment of African catfish, Clarias gariepinus wastewater utilizing phytoremediation of microalgae, Chlorella sp. with Aspergillus niger bio-harvesting. Bioresour. Technol. 190: 492-498.  https://doi.org/10.1016/j.biortech.2015.03.023
  13. Prajapati SK, Bhattacharya A, Kumar P, Malik A, Vijay VK. 2016. A method for simultaneous bioflocculation and pretreatment of algal biomass targeting improved methane production. Green Chem. 18: 5230-5238.  https://doi.org/10.1039/C6GC01483F
  14. 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
  15. Bhattacharya A, Malik A, Malik HK. 2017. A mathematical model to describe the fungal assisted algal flocculation process. Bioresour. Technol. 244: 975-981.  https://doi.org/10.1016/j.biortech.2017.08.062
  16. Bhattacharya A, Mathur M, Kumar P, Malik A. 2019. Potential role of N-acetyl glucosamine in Aspergillus fumigatus-assisted Chlorella pyrenoidosa harvesting. Biotechnol. Biofuels 12: 178. 
  17. Miranda AF, Taha M, Wrede D, Morrison P, Ball AS, Stevenson T, Mouradov A. 2015. Lipid production in association of filamentous fungi with genetically modified cyanobacterial cells. Biotechnol. Biofuels 8: 179. 
  18. Barzee TJ, Cao L, Pan Z, Zhang R. 2021. Fungi for future foods. J. Future Foods 1: 25-37.  https://doi.org/10.1016/j.jfutfo.2021.09.002
  19. Zhou W, Cheng Y, Li Y, Wan Y, Liu Y, Lin X, et al. 2012. Novel fungal pelletization-assisted technology for algae harvesting and wastewater treatment. Appl. Biochem. Biotechnol. 167: 214-228.  https://doi.org/10.1007/s12010-012-9667-y
  20. Zhao Y, Guo G, Sun S, Hu C, Liu J. 2019. Co-pelletization of microalgae and fungi for efficient nutrient purification and biogas upgrading. Bioresour. Technol. 289: 121656. 
  21. Wrede D, Taha M, Miranda AF, Kadali K, Stevenson T, Ball AS, et al. 2014. Co-cultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLoS One 9: e113497. 
  22. Silva A, Delerue-Matos C, Figueiredo SA, Freitas OM. 2019. The use of algae and fungi for removal of pharmaceuticals by bioremediation and biosorption processes: a review. Water (Basel) 11: 1555. 
  23. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239-244.  https://doi.org/10.1038/nature07410
  24. Maheswari U, Mock T, Armbrust EV, Bowler C. 2009. Update of the Diatom EST Database: a new tool for digital transcriptomics. Nucleic Acids Res. 37: D1001-D1005.  https://doi.org/10.1093/nar/gkn905
  25. Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R. 2012. The place of diatoms in the biofuels industry. Biofuels 3: 221-240.  https://doi.org/10.4155/bfs.11.157
  26. Burch AR, Franz AK. 2016. Combined nitrogen limitation and hydrogen peroxide treatment enhances neutral lipid accumulation in the marine diatom Phaeodactylum tricornutum. Bioresour. Technol. 219: 559-565.  https://doi.org/10.1016/j.biortech.2016.08.010
  27. Branco-Vieira M, Martin SS, Agurto C, Santos MA, Freitas MAV, Caetano NS. 2017. Analyzing Phaeodactylum tricornutum lipid profile for biodiesel production. Energy Procedia 136: 369-373.  https://doi.org/10.1016/j.egypro.2017.10.251
  28. Burch AR, Yothers CW, Salemi MR, Phinney BS, Pandey P, Franz AK. 2021. Quantitative label-free proteomics and biochemical analysis of Phaeodactylum tricornutum cultivation on dairy manure wastewater. J. Appl. Phycol. 33: 2105-2121.  https://doi.org/10.1007/s10811-021-02483-3
  29. APHA, AWWA, WEF. 2017. Standard Methods for the Examination of Water and Wastewater. 23rd Ed. American Public Health Association, Washington D.C. 
  30. Bechet Q, Laviale M, Arsapin N, Bonnefond H, Bernard O. 2017. Modeling the impact of high temperatures on microalgal viability and photosynthetic activity. Biotechnol. Biofuels 10: 136. 
  31. Petruzzi L, Campaniello D, Speranza B, Corbo MR, Sinigaglia M, Bevilacqua A. 2017. Thermal treatments for fruit and vegetable juices and beverages: a literature overview. Compr. Rev. Food Sci. Food Saf. 16: 668-691.  https://doi.org/10.1111/1541-4337.12270
  32. Zepka LQ, Borsarelli CD, da Silva MAAP, Mercadante AZ. 2009. Thermal degradation kinetics of carotenoids in a cashew apple juice model and its impact on the system color. J. Agric. Food Chem. 57: 7841-7845.  https://doi.org/10.1021/jf900558a
  33. Tseng RL, Wu FC. 2008. Inferring the favorable adsorption level and the concurrent multi-stage process with the Freundlich constant. J. Hazard. Mater. 155: 277-287.  https://doi.org/10.1016/j.jhazmat.2007.11.061
  34. Chaudhry SA, Khan TA, Ali I. 2017. Zirconium oxide-coated sand based batch and column adsorptive removal of arsenic from water: isotherm, kinetic and thermodynamic studies. Egypt. J. Pet. 26: 553-563.  https://doi.org/10.1016/j.ejpe.2016.11.006
  35. Chaudhry SA, Khan TA, Ali I. 2017. Equilibrium, kinetic and thermodynamic studies of Cr(VI) adsorption from aqueous solution onto manganese oxide coated sand grain (MOCSG). J. Mol. Liq. 236: 320-330.  https://doi.org/10.1016/j.molliq.2017.04.029
  36. Ho YS. 2004. Citation review of Lagergren kinetic rate equation on adsorption reactions. Scientometrics 59: 171-177.  https://doi.org/10.1023/B:SCIE.0000013305.99473.cf
  37. Du ZY, Alvaro J, Hyden B, Zienkiewicz K, Benning N, Zienkiewicz A, et al. 2018. Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata. Biotechnol. Biofuels 11: 174. 
  38. Hallab NJ, Bundy KJ, O'Connor K, Moses RL, Jacobs JJ. 2001. Evaluation of metallic and polymeric biomaterial surface energy and surface roughness characteristics for directed cell adhesion. Tissue Eng. 7: 55-71.  https://doi.org/10.1089/107632700300003297
  39. Kobayashi Y, Harada N, Nishimura Y, Saito T, Nakamura M, Fujiwara T, et al. 2014. Algae sense exact temperatures: small heat shock proteins are expressed at the survival threshold temperature in Cyanidioschyzon merolae and Chlamydomonas reinhardtii. Genome Biol. Evol. 29: 2731-2740.  https://doi.org/10.1093/gbe/evu216
  40. Keller JU, Staudt R. 2005. Adsorption Isotherms, pp. 359-404. In Gas Adsorption Equilibria: Experimental Methods and Adsorptive Isotherms. Springer Science + Business Media, Inc, Boston, MA. 
  41. Brennan JK, Bandosz TJ, Thomson KT, Gubbins KE. 2001. Water in porous carbons. Colloids and Surfaces A: Physicochem. Eng. Aspects 187-188: 539-568.  https://doi.org/10.1016/S0927-7757(01)00644-6
  42. 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
  43. Negm NA, Abd El Wahed MG, Hassan ARA, Abou Kana MTH. 2018. Feasibility of metal adsorption using brown algae and fungi: effect of biosorbents structure on adsorption isotherm and kinetics. J. Mol. Liq. 264: 292-305.  https://doi.org/10.1016/j.molliq.2018.05.027
  44. Uggetti E, Sialve B, Latrille E, Steyer JP. 2014. Anaerobic digestate as substrate for microalgae culture: the role of ammonium concentration on the microalgae productivity. Bioresour. Technol. 152: 437-443.  https://doi.org/10.1016/j.biortech.2013.11.036
  45. Xie S, Sun S, Dai SY, S.Yuan J. 2013. Efficient coagulation of microalgae in cultures with filamentous fungi. Algal. Res. 2: 28-33.  https://doi.org/10.1016/j.algal.2012.11.004
  46. Choi YN, Cho HU, Utomo JC, Shin DY, Kim HK, Park JM. 2016. Efficient harvesting of Synechocystis sp. PCC 6803 with filamentous fungal pellets. J. Appl. Phycol. 28: 2225-2231.  https://doi.org/10.1007/s10811-015-0787-y
  47. Ogawa, M, Garcia, JM, Nitin, N, Baar, K, Block, DE. 2022. Assessing edible filamentous fungal carriers as cell supports for growth of yeast and cultivated meat. Foods 11: 3142.