Co-Cultivation of Fungi and Microalgae for Biotechnology

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Abstract

The review examines the results of studies of the last decade on the co-cultivation of fungi and microalgae. It outlines the mechanisms of interaction between fungi and microscopic algae during associative cultivation and briefly discusses the methods for the formation of flocs. Key importance for biotechnology is the ability of fungi and algae to form granules (floccules), which are easy to separate from the culture liquid. The synergistic effect of these relationships results in a higher level of biomass accumulation, synthesis of lipids, polyunsaturated fatty acids, and other metabolites, as well as the removal of various pollutants from wastewater. By selecting specific strains and optimizing cultivation conditions, it is possible to enhance the composition of the resulting products. So far, mostly successful laboratory experiments have been carried out in this direction, which need to be expanded and transferred to production projects. For large-scale application of these systems, it is necessary to continue research into the mechanisms of interaction between fungi and microalgae, their metabolism, regulation of biosynthetic processes using modern methods of metabolomics and proteomics, and to develop engineering solutions for their cultivation.

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About the authors

N. A. Oghanesyan

Armbiotechnology Scientific and Production Center of the National Academy of Sciences of Armenia

Author for correspondence.
Email: nelliog@yahoo.fr
Armenia, Yerevan

A. V. Kurakov

Lomonosov Moscow State University

Email: kurakov57@mail.ru
Russian Federation, Moscow

N. V. Khachaturyan

Armbiotechnology Scientific and Production Center of the National Academy of Sciences of Armenia

Email: nun-khach@yandex.ru
Armenia, Yerevan

S. A. Gevorgyan

Armbiotechnology Scientific and Production Center of the National Academy of Sciences of Armenia

Email: sgevork@yahoo.com
Armenia, Yerevan

R. E. Matevosyan

Yerevan State University

Email: matevosyanruzanna@ysu.am
Armenia, Yerevan

V. A. Bagiyan

Armbiotechnology Scientific and Production Center of the National Academy of Sciences of Armenia

Email: valbeg@mail.ru
Armenia, Yerevan

References

  1. Al-Juburi W.J., Khalil M.I., Al-Katib M.A. Synergistic efficiency between types of fungi and algae for wastewater treatment. J. Res. Appl. Sci. Biotechnol. 2022. V. 1 (4). P. 181– 186. https://doi.org/10.55544/jrasb.1.4.26
  2. Ashtiani F.R., Jalili H., Rahaie M. et al. Effect of mixed culture of yeast and microalgae on acetyl-CoA carboxylase and Glycerol-3-phosphate acyltransferase expression. J. Biosci. Bioengin. 2021. V. 131. (4). P. 364–372. https://doi.org/10.1016/j.jbiosc.2020.11.006
  3. Bodin H., Daneshvar A., Gros M. et al. Effects of biopellets composed of microalgae and fungi on pharmaceuticals present at environmentally relevant levels in water. Ecol. Engin. 2016. V. 91. P. 169–172. https://doi.org/10.1016/j.ecoleng.2016.02.007
  4. Branyikova I., Prochazkova G., Potocar T. et al. Harvesting of microalgae by flocculation. Fermentation. 2018. V. 4 (4). Art. 93. https://doi.org/10.3390/fermentation4040093
  5. Braun S., Vecht-Lifshitz S.E. Mycelial morphology and metabolite production. Trends Biotechnol. 1991. V. 9 (1). P. 63–68.
  6. Brenner K., You L., Arnold F.H. Engineering microbial consortia: a new frontier in synthetic biology. Trends. Biotechnol. 2008. V. 26 (9). P. 483–489. https://doi.org/10.1016/j.tibtech.2008.05.004
  7. Cheirsilp B., Suwannarat W., Niyomdecha R. Mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. New Biotechnol. 2011. V. 28 (4). P. 362–368. https://doi.org/10.1016/j.nbt.2011.01.004
  8. Chu R., Li S., Yin Z. et al. A fungal immobilization technique for efficient harvesting of oleaginous microalgae: key parameter optimization, mechanism exploration and spent medium recycling. Sci. Total Environm. 2021. V. 790. P. 148–174. https://doi.org/10.1016/j.scitotenv.2021.148174
  9. Du Z.Y., Alvaro J., Hyden B. et al. Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata. Biotechnol. for Biofuels. 2018. V. 11. P. 1–16. https://doi.org/10.1186/s13068-018-1172-2
  10. Espinosa-Ortiz E.J., Rene E.R., Pakshirajan K. et al. Fungal pelleted reactors in wastewater treatment: applications and perspectives. Chem. Engin. J. 2016. V. 283. P. 553–571. https://doi.org/10.1016/j.cej.2015.07.068
  11. Grimm L.H., Kelly S., Hengstler J. et al. Kinetic studies on the aggregation of Aspergillus niger conidia. Biotechnol. Bioengin. 2004. V. 87 (2). P. 213–218. https://doi.org/10.1002/bit.20130
  12. Gultom S.O., Zamalloa C., Hu B. Microalgae harvest through fungal pelletization – co-culture of Chlorella vulgaris and Aspergillus niger. Energies. 2014. V. 7 (7). P. 4417–4429. https://doi.org/10.3390/en7074417
  13. Gultom S.O., Hu B. Review of microalgae harvesting via co-pelletization with filamentous fungus. Energies. 2013. V. 6 (11). P. 5921–5939. https://doi.org/10.3390/en6115921
  14. Hultberg M., Bodin H. Effects of fungal-assisted algal harvesting through biopellet formation on pesticides in water. Biodegradation. 2018. V. 29. (6). P. 557–565. https://doi.org/10.1007/s10532-018-9852-y
  15. Hultberg M., Bodin H., Birgersson G. Impact on wastewater quality of biopellets composed of Chlorella vulgaris and Aspergillus niger and lipid content in the harvested biomass. J. Water Resource Protect. 2019. V. 11 (7). P. 831–843. https://doi.org/10.4236/jwarp.2019.117050
  16. Kadalg N., Pawar P., Prakash G. Co-cultivation of Phaeodactylum tricornutum and Aurantiochytrium limacinum for polyunsaturated omega-3 fatty acids production. Bioresource Technol. 2022. V. 346. Art. 126544.
  17. Kitcha S., Cheirsilp B. Enhanced lipid production by co-cultivation and co-encapsulation of oleaginous yeast Trichosporonoides spathulata with microalgae in alginate gel beads. Appl. Biochem. Biotechnol. 2014. V. 173. P. 522–534. https://doi.org/10.1007/s12010-014-0859-5
  18. Kumar N., Banerjee C., Negi S. et al. Microalgae harvesting techniques: updates and recent technological interventions. Critical Rev. Biotechnol. 2023. V. 43 (3). P. 342–368. https://doi.org/10.1080/07388551.2022.2031089
  19. Lal A., Banerjee S., Das D. Aspergillus sp. assisted bioflocculation of Chlorella MJ 11/11 for the production of biofuel from the algal-fungal co-pellet. Separation and Purification Technol. 2021. V. 272. Art. 118320. https://doi.org/10.1016/j.seppur.2021.118320
  20. Leng L., Wenting L., Jie C. et al. Co-culture of fungi-microalgae consortium for wastewater treatment: A review. Bioresource Technol. 2021. V. 330 Art. 125008. https://doi.org/10.1016/j.biortech.2021.125008
  21. Lennen R.M., Pfleger B.F. Microbial production of fatty acid-derived fuels and chemicals. Current Opin. Biotechnol. 2013. V. 24 (6). P. 1044–1053. https://doi.org/10.1016/j.copbio.2013.02.028
  22. Li H., Yuming Z., Qian L. et al. Co-cultivation of Rhodotorula glutinis and Chlorella pyrenoidosa to improve nutrient removal and protein content by their synergistic relationship. RSC Adv. 2019. V. 9 (25). P. 14331–14342. https://doi.org/10.1039/C9RA01884K
  23. Li S., Tianyi H., Yanzhe X. et al. A review on flocculation as an efficient method to harvest energy microalgae: mechanisms, performances, influencing factors and perspectives. Renewable and Sustainable Energy Reviews. 2020. V. 131. P. 110005. https://doi.org/10.1016/j.rser.2020.110005
  24. Luo S., Wu X., Jiang H. et al. Edible fungi-assisted harvesting system for efficient microalgae bio-flocculation. Bioreso. Technol. 2019. V. 282. P. 325–330. https://doi.org/10.1016/j.biortech.2019.03.033
  25. Magdouli S., Brar S.K., Blais J.F. Co-culture for lipid production: advances and challenges. Biomass and Bioenergy. 2016. V. 92. P. 20–30. https://doi.org/10.1016/j.biombioe.2016.06.003
  26. Miranda A.F., Ramkumar N., Andriotis C. et al. Applications of microalgal biofilms for wastewater treatment and bioenergy production. Biotechnol. for Biofuels. 2017. V. 10. P. 1–23. https://doi.org/10.1186/s13068-017-0798-9
  27. Muradov N., Mohamed T., Miranda A.F. et al. Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production. Biotechnol. for Diofuels. 2015. V. 8. P. 1–23. https://doi.org/10.1186/s13068-015-0210-6
  28. Nayak M., Suh W., Lee B. et al. Enhanced carbon utilization efficiency and FAME production of Chlorella sp. HS2 through combined supplementation of bicarbonate and carbon dioxide. Energy Convers. Manag. 2018. V. 156. P. 45–52. https://doi.org/10.1016/j.enconman.2017.11.002
  29. Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol. Adv. 2004. V. 22 (3). P. 189–259. https://doi.org/10.1016/j.biotechadv.2003.09.005
  30. Piercey-Normore M.D., Athukorala S.N. Interface between fungi and green algae in lichen associations. Botany. 2017. V. 95 (10). P. 1005–1014. https://doi.org/10.1139/cjb-2017-0037
  31. Prajapati S.K., Bhattacharya A., Kumar P. et al. A method for simultaneous bioflocculation and pretreatment of algal biomass targeting improved methane production. Green Chem. 2016. V. 18 (19). P. 5230–5238. https://doi.org/10.1039/c6gc01483f
  32. Rajendran A., Fox T., Hu B. Nutrient recovery from ethanol co-products by a novel mycoalgae biofilm: attached cultures of symbiotic fungi and algae. J. Chem. Technol. Biotechnol. 2017. V. 92 (7). P. 1766–1776. https://doi.org/10.1002/jctb.5177
  33. Rashid N., Ryu A.J., Jeong K.J. et al. Co-cultivation of two freshwater microalgae species to improve biomass productivity and biodiesel production. Energy Convers. Manag. 2019. V. 196. P. 640–648. https://doi.org/10.1016/j.enconman.2019.05.106
  34. Salbitani G., Bolinesi F., Affuso M. et al. Rapid and positive effect of bicarbonate addition on growth and photosynthetic efficiency of the green microalgae Chlorella sorokiniana (Chlorophyta, Trebouxiophyceae). Applied Sciences. 2020. V. 10(13). Art. 4515. https://doi.org/10.3390/app10134515
  35. Salih F.M. Microalgae tolerance to high concentrations of carbon dioxide: a review. J. Environm. Protection. 2011. V. 2 (5). Art. 648. https://doi.org/10.4236/jep.2011.25074
  36. Santos C.A., Caldeira M., da Silva T.L. et al. Enhanced lipidic algae biomass production using gas transfer from a fermentative Rhodosporidium toruloides culture to an autotrophic Chlorella protothecoides culture. Bioresource Technol. 2013. V. 138. P. 48–54. https://doi.org/10.1016/j.biortech.2013.03.135
  37. Shen L., Li Z., Wang J. et al. Characterization of extracellular polysaccharide/protein contents during the adsorption of Cd (II) by Synechocystis sp. PCC6803. Environm. Sci. Pollut. Res. 2018. V. 25. P. 20713–20722. https://doi.org/10.1016/j.gexplo
  38. Shen N., Chirwa E.M. Live and lyophilized fungi-algae pellets as novel biosorbents for gold recovery: Critical parameters, isotherm, kinetics and regeneration studies. Bioresource Technol. 2020. V. 306. Art. 123041. https://doi.org/10.1016/j.biortech.2020.123041
  39. Shu C.H., Tsai C.C., Chen K.Y. et al. Enhancing high quality oil accumulation and carbon dioxide fixation by a mixed culture of Chlorella sp. and Saccharomyces cerevisiae. J. Taiwan Instit. Chem. Engineers. 2013. V. 44 (6). P. 936–942. https://doi.org/10.1016/j.jtice.2013.04.001
  40. Silva A., Delerue-Matos C., Figueiredo S.A. et al. The use of algae and fungi for removal of pharmaceuticals by bioremediation and biosorption processes: a review. Water. 2019. V. 11 (8). Art. 1555. https://doi.org/10.3390/w11081555
  41. Šimonovicová A., Takáčová A., Šimkovic I. et al. Experimental treatment of hazardous ash waste by microbial consortium Aspergillus niger and Chlorella sp.: decrease of the Ni content and identification of adsorption sites by Fourier-transform infrared spectroscopy. Front. Microbiol. 2021. V. 12. Art. 792987. https://doi.org/10.3389/fmicb.2021.792987
  42. Slusarczyk J., Adamska E., Czerwik-Marcinkowska J. Fungi and algae as sources of medicinal and other biologically active compounds: a review. Nutrients. 2021. V. 13. Art. 3178. https://doi.org/10.3390/nu13093178
  43. Smirnov I.A., Lobakova E.S. Morphophysiological characteristics of a mixed culture of Pleurotus ostreatus and nitrogen-fixing cyanobacterium Anabaena variabilis. In: Proceedings of the jubilee conference dedicated to the 100th M.V. Gorlenko anniversary “Higher basidiomycetes: individuals, populations, communities”. Vostok-Zapad, Moscow, 2008, pp. 198–199. (In Russ.).
  44. Srinuanpan S., Chawpraknoi A., Chantarit S. et al. 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. 2018. V. 20 (10). P. 1017–1024. https://doi.org/10.1080/15226514.2018.1452187
  45. Szotkowski M., Holub J., Šimanský S. et al. Bioreactor co-cultivation of high lipid and carotenoid producing yeast Rhodotorula kratochvilovae and several microalgae under stress. Microorganisms. 2021. V. 9 (6). P. 1160. https://doi.org/10.3390/microorganisms9061160
  46. Takáčová A., Bajuszová M., Šimonovicová A. et al. Biocoagulation of dried algae Chlorella sp. and pellets of Aspergillus niger in decontamination process of wastewater, as a presumed source of biofuel. J. Fungi. 2022. V. 8 (12). Art. 1282. https://doi.org/10.3390/jof8121282
  47. Vona V., Di Martino Rigano V., Andreoli C. et al. Comparative analysis of photosynthetic and respiratory parameters in the psychrophilic unicellular green alga Koliella antarctica, cultured in indoor and outdoor photo-bioreactors. Physiol. Molec. Biol. Plants. 2018. V. 24. P. 1139–1146.
  48. Walls L.E., Velasquez-Orta S.B., Romero-Frasca E. et al. Non-sterile heterotrophic cultivation of native wastewater yeast and microalgae for integrated municipal wastewater treatment and bioethanol production. Biochem. Engin. J. 2019. V. 151. Art. 107319. https://doi.org/10.1016/j.bej.2019.107319
  49. Wang S.K., Yang K.X., Zhu Y.R. et al. One-step co-cultivation and flocculation of microalgae with filamentous fungi to valorize starch wastewater into high-value biomass. Bioresource Technol. 2022. V. 361. Art. 127625. https://doi.org/10.1016/j.biortech.2022.127625
  50. Wang Y., Yang Y., Ma F. et al. Optimization of Chlorella vulgaris and bioflocculant-producing bacteria co-culture: enhancing microalgae harvesting and lipid content. Lett. Appl. Microbiol. 2015. V. 60. (5). P. 497–503. https://doi.org/10.1111/lam.12403
  51. Wang J., Chen R., Fan L. et al. Construction of fungi-microalgae symbiotic system and adsorption study of heavy metal ions. Separation Purification Technol. 2021. V. 268. Art. 118689. https://doi.org/10.1016/j.seppur.2021.118689
  52. Ward O., Singh A. Omega-3/6 fatty acids: alternative sources of production. Process Biochem. 2005. V. 40 (12). P. 3627–3652. https://doi.org/10.1016/j.procbio.2005.02.020
  53. Wrede D., Taha M., Miranda A.F. et al. Co-cultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLOS One. 2014. V. 9 (11). e113497. https://doi.org/10.1371/journal.pone.0113497
  54. Xie S., Su S., Dai S.Y. et al. Efficient coagulation of microalgae in cultures with filamentous fungi. Algal Res. 2013. V. 2 (1). P. 28–33. https://doi.org/10.1016/j.algal.2012.11.004
  55. Xue F., Miao J., Zhang X. et al. A new strategy for lipid production by mix cultivation of Spirulina platensis and Rhodotorula glutinis. Appl. Biochem. Biotech. 2010. V. 160. P. 498–503. https://doi.org/10.1007/s12010-008-8376-z
  56. Yang L., Li H., Wang Q. A novel one-step method for oil-rich biomass production and harvesting by co-cultivating microalgae with filamentous fungi in molasses wastewater. Bioresource Technol. 2019. V. 275. P. 35–43. https://doi.org/10.1016/j.biortech.2018.12.036
  57. Yen H.W., Chen P.W., Chen L.J. The synergistic effects for the co-cultivation of oleaginous yeast-Rhodotorula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresource Technol. 2015. V. 184. P. 148–152. https://doi.org/10.1016/j.biortech.2014.09.113
  58. Zhan J., Rong J., Wang Q. Mixotrophic cultivation, a preferable microalgae cultivation mode for biomass/bioenergy production, and bioremediation, advances and prospect. Int. J. Hydrogen Energy. 2017. V. 42 (12). P. 8505–8517. https://doi.org/10.1016/j.ijhydene.2016.12.021
  59. Zhang J., Zhang J. The filamentous fungal pellet and forces driving its formation. Crit. Rev. Biotechnol. 2016. V. 36 (6). P. 1066–1077. https://doi.org/10.3109/07388551.2015.1084262
  60. Zhang J., Feng L., Ouyang Y. et al. Phosphate-solubilizing bacteria and fungi in relation to phosphorus availability under different land uses for some latosols from Guangdong, China. Catena. 2020. V. 195. Art. 104686. https://doi.org/10.1016/j.catena.2020.104686
  61. Zhang Z., Pang Z., Xu S. et al. Improved carotenoid productivity and COD removal efficiency by co-culture of Rhodotorula glutinis and Chlorella vulgaris using starch wastewaters as raw material. Appl. Biochem. Biotechnol. 2019. V. 189. P. 193–205.
  62. Zhou W., Cheng Y., Li Y. et al. Novel fungal pelletization-assisted technology for algae harvesting and wastewater treatment. Appl. Biochem. Biotechnol. 2012. V. 167. P. 214–228. https://doi.org/10.1007/s12010-012-9667-y
  63. Zorn S.M., Reis C.E., Silva M.B. et al. Consortium growth of filamentous fungi and microalgae: evaluation of different cultivation strategies to optimize cell harvesting and lipid accumulation. Energies. 2020. V. 13. (14). Art. 3648. https://doi.org/10.3390/en13143648
  64. Смирнов И.А., Лобакова Е.С. (Smirnov, Lobakova) Морфофизиологическая характеристика смешанной культуры Pleurotus ostreatus и азотофикирующей цианобактерии Anabaena variabilis // Мат-лы юбилейной конф., посв. 100-летию со дня рожд. М.В. Горленко “Высшие базидиальные грибы: индивидуумы, популяции, сообщества”. М.: Восток-Запад, 2008. С. 198–199.

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