Skip to main content

Advertisement

SpringerLink
Log in

Enhanced biomass production and wastewater treatment in attached co-culture of Chlorella pyrenoidosa with nitrogen-fixing bacteria Azotobacter beijerinckii

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Algae–bacteria symbiosis can promote the growth of microalgae and improve the efficiency of wastewater treatment. Attached culture is an efficient culture technique for microalgae, with benefits of high yield, low water consumption and easy harvesting. However, the promoting effects of bacteria on microalgae in attached culture are still unclear. In this study, different forms of a nitrogen-fixing bacteria, Azotobacter beijerinckii (including bacteria supernatant, live bacteria, and broken bacteria), were co-cultured with Chlorella pyrenoidosa in an attached culture system using wastewater as the culture medium. The results showed that the broken A. beijerinckii form had the best growth promotion effect on C. pyrenoidosa. Compared with the pure algae culture, the biomass of C. pyrenoidosa increased by 71.8% and the protein increased by 28.2%. The live bacteria form had the best effect on improving the efficiency of wastewater treatment by C. pyrenoidosa, with the COD, PO43− and NH4+–N removal rates increased by 20.8%, 18.5% and 8.9%, respectively, in comparison with the pure algae culture. The attached co-culture mode promoted the growth of C. pyrenodisa better than the suspended co-culture mode. This research offers a new way for improving microalgae biomass and wastewater treatment by attached algae–bacteria symbiont.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig.1
Fig.2
Fig.3
Fig.4
Fig.5
Fig.6
Fig.7

Similar content being viewed by others

Data availability

All date generated or analyzed during this study are included in this published article or are available from the corresponding author on reasonable request.

References

  1. Paul C, Pohnert G (2011) Production and role of volatile halogenated compounds from marine algae. ChemInform 42(21):186

    Article  Google Scholar 

  2. Jia H, Yuan Q, Rein A (2016) Removal of nitrogen from wastewater using microalgae and microalgae–bacteria consortia. Cogent Environ Sci 2(1):1275089

    Article  Google Scholar 

  3. Liu W, Cui YQ, Cheng PF, Huo SH, Ma XC, Chen QF, Cobb K, Chen P, Ma JJ, Gao XG, Ruan R (2020) Microwave assisted flocculation for harvesting of Chlorella vulgaris. Bioresour Technol 314:123770

    Article  CAS  PubMed  Google Scholar 

  4. Bolch C, Subramanian TA, Green DH (2011) The toxic dinoflagellate gymnodinium catenatum (Dinophyceae) requires marine bacteria for growth. J Phycol 47(5):1009–1022

    Article  PubMed  Google Scholar 

  5. Grant MA, Kazamia E, Cicuta P, Smith AG (2014) Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. Isme J 8(7):1418–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cho DH, Ramanan R, Heo J, Lee J, Kim HS (2015) Enhancing microalgal biomass productivity by engineering a microalgal-bacterial community. Bioresour Technol 175:578–585

    Article  CAS  PubMed  Google Scholar 

  7. Tadashi T, Mari K, Tsubasa H, Naoto K, Yasuhiro T, Daisuke I, Kazunari S, Masaaki M, Kazuhiro M (2018) Growth promotion of three microalgae, Chlamydomonas reinhardtii, Chlorella vulgaris and Euglena gracilis, by in situ indigenous bacteria in wastewater effluent. Biotechnol Biofuels 11:176

    Article  Google Scholar 

  8. Xue LG, Shang H, Ma P (2018) Analysis of growth and lipid production characteristics of Chlorella vulgaris in artificially constructed consortia with symbiotic bacteria. J Basic Microbiol 58(4):358–367

    Article  CAS  PubMed  Google Scholar 

  9. Oswald WJ, Gotaas HB, Golueke CG, Kellen WR (1957) Algae in waste treatment. Sewage Ind Waste 29(4):437–455

    Google Scholar 

  10. Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14(2):557–577

    Article  CAS  Google Scholar 

  11. Wang J, Han D, Sommerfeld MR, Lu C, Hu Q (2013) Effect of initial biomass density on growth and astaxanthin production of Haematococcus pluvialis in an outdoor photobioreactor. J Appl Phycol 25(1):253–260

    Article  CAS  Google Scholar 

  12. Davis R, Aden A, Pienkos PT (2011) Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energ 88(10):3524–3531

    Article  Google Scholar 

  13. Zhang TY, Hu HY, Wu YH, Zhuang LL, Xu XQ, Wang XX, Dao GH (2016) Promising solutions to solve the bottlenecks in the large-scale cultivation of microalgae for biomass/bioenergy production. Renew Sustain Energy Rev 60:1602–1614

    Article  CAS  Google Scholar 

  14. Liu TZ, Wang JF, Hu Q, Cheng PF, Bei J, Liu JL, Chen Y, Zhang W, Chen XL, Chen L, Gao LL, Ji CL, Wang H (2013) Attached cultivation technology of microalgae for efficient biomass feedstock production. Bioresour Technol 127:216–222

    Article  CAS  PubMed  Google Scholar 

  15. Ozkan A, Kinney K, Katz L, Berberoglu H (2012) Reduction of water and energy requirement of algae cultivation using an algae biofilm photobioreactor. Bioresour Technol 114:542–548

    Article  CAS  PubMed  Google Scholar 

  16. Wei ZJ, Xiao LI, Wang HN, Yin YH, Jun XL, Sheng GB (2019) Enhanced biomass production and lipid accumulation by co-cultivation of Chlorella vulgaris with Azotobacter Mesorhizobium sp. Chin Biotech 39(7):56–64

    CAS  Google Scholar 

  17. Hernandez JP, De-Bashan LE, Rodriguez DJ, Rodriguez Y, Bashan Y (2009) Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur J Soil Biol 45:88–93

    Article  CAS  Google Scholar 

  18. Xu LL, Cheng XL, Wang QX (2018) Enhanced lipid production in Chlamydomonas reinhardtii by co-culturing with Azotobacter chroococcum. Front Plant Sci 9:741

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  20. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  21. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356

    Article  CAS  Google Scholar 

  22. Bligh EG, Dyer WJ (1959) A rapid methos of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917

    Article  CAS  PubMed  Google Scholar 

  23. Eaton AD, Clesceri LS, Greenberg AE, Franson MA (1966) Standard methods for the examination of water and wastewater. Am J Public Health Nations Health 56(3):387–388

    Article  Google Scholar 

  24. Yao N, Liu Z, Chen Y, Zhou Y, Xie B (2015) A novel thermal sensor for the sensitive measurement of chemical oxygen demand. Sensors 15(8):20501–20510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Omar H, Aljudaibiand A, Elgendy A (2018) Abstract: Antimicrobial, antioxidant, anticancer activity and phytochemical analysis of the red algae, Laurencia papillosa. Int J Pharmacol 14(4):572–583

    Article  CAS  Google Scholar 

  26. Demmig-Adams B (1996) Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field. Funct Plant Biol 23(5):649–659

    Article  CAS  Google Scholar 

  27. Yu Z, Pei HY, Li YZ, Yang ZG, Zhen X, Hou QJ, Nie CL (2020) Inclined algal biofilm photobioreactor (IABPBR) for cost-effective cultivation of lipid-rich microalgae and treatment of seawater-diluted anaerobically digested effluent. Bioresour Technol 315:123761

    Article  CAS  PubMed  Google Scholar 

  28. Liu X, Zhang S, Shan XQ, Christie P (2007) Combined toxicity of cadmium and arsenate to wheat seedlings and plant uptake and antioxidative enzyme responses to cadmium and arsenate co-contamination. Ecotox Environ Safe 68(2):305–313

    Article  CAS  Google Scholar 

  29. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26(11):2027–2038

    Article  CAS  PubMed  Google Scholar 

  30. Liu CR, Chen ZP, Zhang ZW (2008) The effects of Aeromonas hydrophila-lipopolysaccharide and Sparasiscrispa-polysaccharide on the immune and digestion function of loach (Misgurnusanguillicaudatus). Mar Sci 32:1–9

    CAS  Google Scholar 

  31. Xu YJ, Shan HW, Ma S (2015) Effect of Bacillus sp. and Vibroio alginolyticus on the activities of digestive and immune enzymes disease resistance of Litopenaeus vannamei. Period Ocean Univ China 45:046–053

    Google Scholar 

  32. Zhang B, Chen JC, Su YR, Sun WX, Zhang AL (2021) Utilization of Indole-3-acetic acid–secreting bacteria in algal environment to increase biomass accumulation of ochromonas and Chlorella. Bioenerg Res 15:1–11

    Google Scholar 

  33. Fuentes-Ramirez LE, Jimenez-Salgado T, Abarca-Ocampo IR, Caballero-Mellado J (2018) Acetobacter diazotrophicus, an indoleacetic acid producing bacterium isolated from sugarcane cultivars of Mexico. Plant Soil 154:145–150

    Article  Google Scholar 

  34. Zhang B, Chen J, Su Y, Sun W, Zhang A (2021) Utilization of Indole-3-acetic acid–secreting bacteria in algal environment to increase biomass accumulation of Ochromonas and Chlorella. Bioenerg Res 2021:1–11

    Google Scholar 

  35. Li T, Mahmoud G, Feng J (2015) Regulation of starch and lipid accumulation in a microalgal Chorellasorokiniana. Bioresour Technol 180:250–257

    Article  CAS  PubMed  Google Scholar 

  36. Yun H, Wei X, Qiang L, Qian F, Xia A, Zhu X, Sun YH (2016) Comparison of Chlorella vulgaris biomass productivity cultivated in biofilm and suspension from the aspect of light transmission and microalgae affinity to carbon dioxide. Bioresour Technol 222:367–373

    Article  Google Scholar 

  37. Gross M, Henry W, Michael C, Wen Z (2013) Development of a rotating algal biofilm growth system for attached microalgae growth with in situ biomass harvest. Bioresour Technol 150:195–201

    Article  CAS  PubMed  Google Scholar 

  38. Wang JF, Liu JL, Liu TZ (2015) The difference in effective light penetration may explain the superiority in photosynthetic efficiency of attached cultivation over the conventional open pond for microalgae. Biotechnol Biofuels 8:49

    Article  PubMed  PubMed Central  Google Scholar 

  39. Song XY, Luo WH, Mcdonald J (2018) An anaerobic membrane bioreactor-membrane distillation hybrid system for energy recovery and water reuse: removal performance of organic carbon, nutrients, and trace organic contaminants. Sci Total Environ 628–629:358–365

    Article  PubMed  Google Scholar 

  40. Zhang L, Chen L, Wang J, Chen Y, Gao X, Zhang Z, Liu TZ (2015) Attached cultivation for improving the biomass productivity of Spirulina platensis. Bioresour Technol 181:136–142

    Article  CAS  PubMed  Google Scholar 

  41. Singhl G, Patidar SK (2020) Development and applications of attached growth system for microalgae biomass production. Bioenerg Res 14(3):709–722

    Article  Google Scholar 

Download references

Acknowledgements

The current study was partly funded by the Innovation Ability Improvement Project of Small and Medium-sized High-tech Company in Shandong Province (2022TSGC2199); Natural Science Foundation of Shandong Province (ZR2022MC204; ZR2019MB073); Major Science and Technology Innovation Projects in Shandong Province (2019JZZY010723); and National Natural Science Foundation of China (22176104).

Funding

This study was supported by the Innovation Ability Improvement Project of Small and Medium-sized High-tech Company in Shandong Province, 2022TSGC2199, Natural Science Foundation of Shandong Province, ZR2022MC204, ZR2019MB073, Major Science and Technology Innovation Projects in Shandong Province, 2019JZZY010723, and National Natural Science Foundation of China, 22176104.

Author information

Authors and Affiliations

  1. Qilu University of Technology (Shandong Academy of Sciences), Shandong Analysis and Test Center, Jinan, 250014, Shandong, China

    Haiwen Dong, Wei Liu, Hao Zhang, Zhenhua Wang, Lixiu Zhou, Huijie Duan, Tongtong Xu, Xiaomeng Li & Junjian Ma

  2. Faculty of Environmental Science and Technology, Qilu University of Technology (Shandong Academy of Sciences), Jinan, 250353, Shandong, China

    Haiwen Dong, Wei Liu, Zhenhua Wang, Lixiu Zhou, Huijie Duan, Tongtong Xu & Xiaomeng Li

  3. Shandong Tiantai Environmental Technology Co. LTD, Jinan, 250101, Shandong, China

    Fei Feng

Authors
  1. Haiwen Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fei Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lixiu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huijie Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tongtong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaomeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Junjian Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HD: conceptualization, data curation, formal analysis, and writing—original draft. WL: supervision, funding acquisition, data curation, and writing—review and editing. HZ: methodology and data curation. ZW: investigation. FF: data curation. LZ: data curation and investigation. HD: data curation and investigation. TX: data curation. XL: investigation. JM: data curation and investigation.

Corresponding author

Correspondence to Wei Liu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval and consent to participate

This manuscript does not involve any human participants, human data, human tissue, individual person’s data or animal experiment.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, H., Liu, W., Zhang, H. et al. Enhanced biomass production and wastewater treatment in attached co-culture of Chlorella pyrenoidosa with nitrogen-fixing bacteria Azotobacter beijerinckii. Bioprocess Biosyst Eng 46, 707–716 (2023). https://doi.org/10.1007/s00449-023-02855-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-023-02855-8

Keywords

Search

Navigation