Skip to main content
SpringerLink
Log in

The Variation of Growth Rate, Photosynthetic Activity, and Biodiesel Productivity in Synechocystis sp. PCC 6803 under Antibiotic Exposure

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

Enrichment of biomass containing high lipid content is the key limiting step for the utilization of cyanobacterial feedstock in biodiesel production. This study investigated the influence of antibiotics on the biodiesel productivity of a model biodiesel-producing cyanobacterium (Synechocystis sp. PCC 6803) through a 18-day exposure test and observed that 100 ng/L of ciprofloxacin, amoxicillin, and spiramycin significantly (p < 0.05) increased biomass, chlorophyll a content, and Fv/Fm value and rETRmax value in Synechocystis sp. PCC 6803. Due to the stimulation of photosynthesis, the 18-day dry weights of the cyanobacterial cells increased from 0.354 ± 0.039 to 0.508 ± 0.048, 0.58 ± 0.028, and 0.66 ± 0.028 g/L under exposure to ciprofloxacin, amoxicillin, and spiramycin, respectively. As a stress response to antibiotics, the lipid content in Synechocystis sp. PCC 6803 increased from 14.71 to 20.92%, 20.59%, and 15.36% under exposure to ciprofloxacin, amoxicillin, and spiramycin, respectively. Due to the increase of biomass and lipid content, the lipid productivity of Synechocystis sp. PCC 6803 increased from 2.89 to 5.90, 6.63, and 5.63 mg/L/d under exposure to ciprofloxacin, amoxicillin, and spiramycin, respectively. Exposure to each target antibiotic increased the proportion of monounsaturated fatty acids in the lipid, while exposure to spiramycin reduced the proportion of saturated fatty acid. Antibiotics regulated the lipid composition of Synechocystis sp. PCC 6803 towards an increase of combustion property. This study proved that antibiotic exposure increased the lipid productivity of cyanobacteria through hormesis, which provided new insights for promoting the production of cyanobacteria-based biodiesel.

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

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article.

References

  1. Sun J, Xiong X, Wang M, Du H, Li J, Zhou D, Zuo J (2019) Microalgae biodiesel production in China: a preliminary economic analysis. Renew Sust Energ Rev 104:296–306. https://doi.org/10.1016/j.rser.2019.01.021

    Article  Google Scholar 

  2. Chen J, Li J, Dong W, Zhang X, Tyagi RD, Drogui P, Surampalli RY (2018) The potential of microalgae in biodiesel production. Renew Sust Energ Rev 90:336–346. https://doi.org/10.1016/j.rser.2018.03.073

    Article  Google Scholar 

  3. Mubarak M, Shaija A, Suchithra TV (2019) Flocculation: an effective way to harvest microalgae for biodiesel production. Journal of Environmental Chemical Engineering 7:103221. https://doi.org/10.1016/j.jece.2019.103221

    Article  CAS  Google Scholar 

  4. Mathimani T, Baldinelli A, Rajendran K, Prabakar D, Matheswaran M, Pieter Van Leeuwen R, Pugazhendhi A (2019) Review on cultivation and thermochemical conversion of microalgae to fuels and chemicals: process evaluation and knowledge gaps. J Clean Prod 208:1053–1064. https://doi.org/10.1016/j.jclepro.2018.10.096

    Article  CAS  Google Scholar 

  5. Garlapati D, Chandrasekaran M, Devanesan A, Mathimani T, Pugazhendhi A (2019) Role of cyanobacteria in agricultural and industrial sectors: an outlook on economically important byproducts. Appl Microbiol Biot 103:4709–4721. https://doi.org/10.1007/s00253-019-09811-1

    Article  CAS  Google Scholar 

  6. Mathimani T, Pugazhendhi A (2019) Utilization of algae for biofuel, bio-products and bio-remediation. Biocatalysis and Agricultural Biotechnology. 17:326–330. https://doi.org/10.1016/j.bcab.2018.12.007

    Article  Google Scholar 

  7. Vargas SR, Santos PVD, Zaiat M, Calijuri MDC (2018) Optimization of biomass and hydrogen production by Anabaena sp. (UTEX 1448) in nitrogen-deprived cultures. Biomass Bioenergy 111:70–76. https://doi.org/10.1016/j.biombioe.2018.01.022

    Article  CAS  Google Scholar 

  8. Deshmukh S, Kumar R, Bala K (2019) Microalgae biodiesel: a review on oil extraction, fatty acid composition, properties and effect on engine performance and emissions. Fuel Process Technol 191:232–247. https://doi.org/10.1016/j.fuproc.2019.03.013

    Article  CAS  Google Scholar 

  9. Chung Y, Lee J, Chung C (2017) Molecular challenges in microalgae towards cost-effective production of quality biodiesel. Renew Sust Energ Rev 74:139–144. https://doi.org/10.1016/j.rser.2017.02.048

    Article  CAS  Google Scholar 

  10. Anto S, Mukherjee SS, Muthappa R, Mathimani T, Deviram G, Kumar SS, Verma TN, Pugazhendhi A (2020) Algae as green energy reserve: technological outlook on biofuel production. Chemosphere. 242:125079. https://doi.org/10.1016/j.chemosphere.2019.125079

    Article  CAS  PubMed  Google Scholar 

  11. Ramesh Kumar B, Deviram G, Mathimani T, Duc PA, Pugazhendhi A (2019) Microalgae as rich source of polyunsaturated fatty acids. Biocatalysis and Agricultural Biotechnology 17:583–588. https://doi.org/10.1016/j.bcab.2019.01.017

    Article  Google Scholar 

  12. Sharma J, V Kumar, S S Kumar, S K Malyan, T Mathimani, N R Bishnoi, and A Pugazhendhi (2020) Microalgal consortia for municipal wastewater treatment – lipid augmentation and fatty acid profiling for biodiesel production. Journal of Photochemistry and Photobiology B: Biology. 202: 111638. https://doi.org/10.1016/j.jphotobiol.2019.111638

  13. Sharma J, Kumar SS, Bishnoi NR, Pugazhendhi A (2018) Enhancement of lipid production from algal biomass through various growth parameters. J Mol Liq 269:712–720. https://doi.org/10.1016/j.molliq.2018.08.103

    Article  CAS  Google Scholar 

  14. Sharma J, Kumar SS, Bishnoi NR, Pugazhendhi A (2019) Screening and enrichment of high lipid producing microalgal consortia. J Photochem Photobiol B Biol 192:8–12. https://doi.org/10.1016/j.jphotobiol.2019.01.002

    Article  CAS  Google Scholar 

  15. Ortiz-Martínez VM, Andreo-Martínez P, García-Martínez N, Ríos APDL, Hernández-Fernández FJ, Quesada-Medina J (2019) Approach to biodiesel production from microalgae under supercritical conditions by the PRISMA method. Fuel Process Technol 191:211–222. https://doi.org/10.1016/j.fuproc.2019.03.031

    Article  CAS  Google Scholar 

  16. Yan J, Kuang Y, Gui X, Han X, Yan Y (2019) Engineering a malic enzyme to enhance lipid accumulation in Chlorella protothecoides and direct production of biodiesel from the microalgal biomass. Biomass Bioenergy 122:298–304. https://doi.org/10.1016/j.biombioe.2019.01.046

    Article  CAS  Google Scholar 

  17. Liu X, Guo X, Liu Y, Lu S, Xi B, Zhang J, Wang Z, Bi B (2019) A review on removing antibiotics and antibiotic resistance genes from wastewater by constructed wetlands: performance and microbial response. Environ Pollut 254:112996. https://doi.org/10.1016/j.envpol.2019.112996

    Article  CAS  PubMed  Google Scholar 

  18. Maul JD, Schuler LJ, Belden JB, Whiles MR, Lydy MJ (2006) Effects of the antibiotic ciprofloxacin on stream microbial communities and detritivorous macroinvertebrates. Environ Toxicol Chem 25:1598–1606. https://doi.org/10.1897/05-441R.1

    Article  CAS  PubMed  Google Scholar 

  19. Sendra M, Moreno-Garrido I, Blasco J, Araújo CVM (2018) Effect of erythromycin and modulating effect of CeO2 NPs on the toxicity exerted by the antibiotic on the microalgae Chlamydomonas reinhardtii and Phaeodactylum tricornutum. Environ Pollut 242:357–366. https://doi.org/10.1016/j.envpol.2018.07.009

    Article  CAS  PubMed  Google Scholar 

  20. Liu Y, Chen S, Zhang J, Gao B (2016) Growth, microcystin-production and proteomic responses of Microcystis aeruginosa under long-term exposure to amoxicillin. Water Res 93:141–152. https://doi.org/10.1016/j.watres.2016.01.060

    Article  CAS  PubMed  Google Scholar 

  21. Wan J, Guo P, Peng X, Wen K (2015) Effect of erythromycin exposure on the growth, antioxidant system and photosynthesis of Microcystis flos-aquae. J Hazard Mater 283:778–786. https://doi.org/10.1016/j.jhazmat.2014.10.026

    Article  CAS  PubMed  Google Scholar 

  22. Xu M, Huang H, Li N, Li F, Wang D, Luo Q (2019) Occurrence and ecological risk of pharmaceuticals and personal care products (PPCPs) and pesticides in typical surface watersheds, China. Ecotox Environ Safe 175:289–298. https://doi.org/10.1016/j.ecoenv.2019.01.131

    Article  CAS  Google Scholar 

  23. Le Henry M, Charton M, Alignan M, Maury P, Luniov A, Pelletier I, Pontalier P, Binder BM, Vaca-Garcia C, Chervin C (2017) Ethylene stimulates growth and affects fatty acid content of Synechocystis sp. PCC 6803. Algal Res 26:234–239. https://doi.org/10.1016/j.algal.2017.07.032

    Article  Google Scholar 

  24. Bland E, Angenent LT (2016) Pigment-targeted light wavelength and intensity promotes efficient photoautotrophic growth of cyanobacteria. Bioresour Technol 216:579–586. https://doi.org/10.1016/j.biortech.2016.05.116

    Article  CAS  PubMed  Google Scholar 

  25. Fu W, Li P, Wu Y (2012) Effects of different light intensities on chlorophyll fluorescence characteristics and yield in lettuce. Sci Hortic 135:45–51. https://doi.org/10.1016/j.scienta.2011.12.004

    Article  CAS  Google Scholar 

  26. Folch J, Lees M, Slonane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  27. Anahas AMP, Muralitharan G (2015) Isolation and screening of heterocystous cyanobacterial strains for biodiesel production by evaluating the fuel properties from fatty acid methyl ester (FAME) profiles. Bioresour Technol 184:9–17. https://doi.org/10.1016/j.biortech.2014.11.003

    Article  CAS  PubMed  Google Scholar 

  28. Casazza AA, Ferrari PF, Aliakbarian B, Converti A, Perego P (2015) Effect of UV radiation or titanium dioxide on polyphenol and lipid contents of Arthrospira (Spirulina) platensis. Algal Res 12:308–315 https://doi.org/10.1016/j.algal.2015.09.012

    Article  Google Scholar 

  29. Chi NTL, Duc PA, Mathimani T, Pugazhendhi A (2019) Evaluating the potential of green alga Chlorella sp. for high biomass and lipid production in biodiesel viewpoint. Biocatalysis and Agricultural Biotechnology. 17:184–188. https://doi.org/10.1016/j.bcab.2018.11.011

    Article  Google Scholar 

  30. Anto S, Pugazhendhi A, Mathimani T (2019) Lipid enhancement through nutrient starvation in Chlorella sp. and its fatty acid profiling for appropriate bioenergy feedstock. Biocatalysis and Agricultural. Biotechnology. 20:101179. https://doi.org/10.1016/j.bcab.2019.101179

    Article  Google Scholar 

  31. Lu H, J Cheng, Y Zhu, K Li, J Tian, and J Zhou (2019) Responses of Arthrospira ZJU9000 to high bicarbonate concentration (HCO3−: 171.2 mM): how do biomass productivity and lipid content simultaneously increase? Algal Research. 41: 101531. https://doi.org/10.1016/j.algal.2019.101531

  32. Renuka N, Guldhe A, Singh P, Ansari FA, Rawat I, Bux F (2017) Evaluating the potential of cytokinins for biomass and lipid enhancement in microalga Acutodesmus obliquus under nitrogen stress. Energ Convers Manage 140:14–23. https://doi.org/10.1016/j.enconman.2017.02.065

    Article  CAS  Google Scholar 

  33. Agathokleous E, Kitao M, Calabrese EJ (2019) Hormesis: a compelling platform for sophisticated plant science. Trends Plant Sci 24:318–327. https://doi.org/10.1016/j.tplants.2019.01.004

    Article  CAS  PubMed  Google Scholar 

  34. Agathokleous E, Calabrese EJ (2019) Hormesis: the dose response for the 21st century: the future has arrived. Toxicology. 425:152249. https://doi.org/10.1016/j.tox.2019.152249

    Article  CAS  PubMed  Google Scholar 

  35. Xie X, Zhou Q, He Z, Bao Y (2010) Physiological and potential genetic toxicity of chlortetracycline as an emerging pollutant in wheat (Triticum aestivum L.). Environ Toxicol Chem 29:922–928. https://doi.org/10.1002/etc.79

    Article  CAS  PubMed  Google Scholar 

  36. Liu Y, Chen X, Zhang J, Gao B (2015) Hormesis effects of amoxicillin on growth and cellular biosynthesis of Microcystis aeruginosa at different nitrogen levels. Microb Ecol 69:608–617. https://doi.org/10.1007/s00248-014-0528-9

    Article  CAS  PubMed  Google Scholar 

  37. Liu B, Nie X, Liu W, Snoeijs P, Guan C, Tsui MTK (2011) Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole on photosynthetic apparatus in Selenastrum capricornutum. Ecotox Environ Safe 74:1027–1035. https://doi.org/10.1016/j.ecoenv.2011.01.022

    Article  CAS  Google Scholar 

  38. Liu L, Liu Y, Liu C, Wang Z, Dong J, Zhu G, Huang X (2013) Potential effect and accumulation of veterinary antibiotics in Phragmites australis under hydroponic conditions. Ecol Eng 53:138–143. https://doi.org/10.1016/j.ecoleng.2012.12.033

    Article  Google Scholar 

  39. Gomes MP, Gonçalves CA, de Brito JCM, Souza AM, Da Silva Cruz FV, Bicalho EM, Figueredo CC, Garcia QS (2017) Ciprofloxacin induces oxidative stress in duckweed (Lemna minor L.): implications for energy metabolism and antibiotic-uptake ability. J Hazard Mater 328:140–149. https://doi.org/10.1016/j.jhazmat.2017.01.005

    Article  CAS  PubMed  Google Scholar 

  40. Wang Z, Chen Q, Hu L, Wang M (2018) Combined effects of binary antibiotic mixture on growth, microcystin production, and extracellular release of Microcystis aeruginosa: application of response surface methodology. Environ Sci Pollut R 25:736–748. https://doi.org/10.1007/s11356-017-0475-3

    Article  CAS  Google Scholar 

  41. Dao G, Wu G, Wang X, Zhuang L, Zhang T, Hu H (2018) Enhanced growth and fatty acid accumulation of microalgae Scenedesmus sp. LX1 by two types of auxin. Bioresour Technol 247:561–567. https://doi.org/10.1016/j.biortech.2017.09.079

    Article  CAS  PubMed  Google Scholar 

  42. Sierra-Cantor JF, Guerrero-Fajardo CA (2017) Methods for improving the cold flow properties of biodiesel with high saturated fatty acids content: a review. Renew Sust Energ Rev 72:774–790. https://doi.org/10.1016/j.rser.2017.01.077

    Article  CAS  Google Scholar 

  43. EN E S. (2004) Automotive fuels-fatty acid methyl esters (FAME) for diesel engines-requirements and test methods

  44. Yu Z, Pei H, Jiang L, Hou Q, Nie C, Zhang L (2018) Phytohormone addition coupled with nitrogen depletion almost tripled the lipid productivities in two algae. Bioresour Technol 247:904–914. https://doi.org/10.1016/j.biortech.2017.09.192

    Article  CAS  PubMed  Google Scholar 

  45. Longworth J, Wu D, Huete-Ortega M, Wright PC, Vaidyanathan S (2016) Proteome response of Phaeodactylum tricornutum, during lipid accumulation induced by nitrogen depletion. Algal Res 18:213–224. https://doi.org/10.1016/j.algal.2016.06.015

    Article  PubMed  PubMed Central  Google Scholar 

  46. Li T, Gargouri M, Feng J, Park J, Gao D, Miao C, Dong T, Gang DR, Chen S (2015) Regulation of starch and lipid accumulation in a microalga Chlorella sorokiniana. Bioresour Technol 180:250–257. https://doi.org/10.1016/j.biortech.2015.01.005

    Article  CAS  PubMed  Google Scholar 

  47. Udayan A, Kathiresan S, Arumugam M (2018) Kinetin and Gibberellic acid (GA3) act synergistically to produce high value polyunsaturated fatty acids in Nannochloropsis oceanica CASA CC201. Algal Res 32:182–192. https://doi.org/10.1016/j.algal.2018.03.007

    Article  Google Scholar 

  48. Gao F, Yang H, Li C, Peng Y, Lu M, Jin W, Bao J, Guo Y (2019) Effect of organic carbon to nitrogen ratio in wastewater on growth, nutrient uptake and lipid accumulation of a mixotrophic microalgae Chlorella sp. Bioresour Technol 282:118–124. https://doi.org/10.1016/j.biortech.2019.03.011

    Article  CAS  PubMed  Google Scholar 

  49. Adu-Mensah D, Mei D, Zuo L, Zhang Q, Wang J (2019) A review on partial hydrogenation of biodiesel and its influence on fuel properties. Fuel 251:660–668. https://doi.org/10.1016/j.envpol.2019.112996

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the National Natural Science Foundation of China (51679130) and the Fundamental Research Funds of Shandong University (2017WLJH35).

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, Shandong University, Qingdao, 266237, People’s Republic of China

    Mengwen Cui, Ying Liu & Jian Zhang

Authors
  1. Mengwen Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Investigation and original draft writing were performed by Mengwen Cui. Ying Liu was responsible for methodology and project administration. Jian Zhang was responsible for supervision. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ying Liu.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Informed Consent

All authors were informed and consented to the manuscript publishment.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cui, M., Liu, Y. & Zhang, J. The Variation of Growth Rate, Photosynthetic Activity, and Biodiesel Productivity in Synechocystis sp. PCC 6803 under Antibiotic Exposure. Bioenerg. Res. 13, 955–962 (2020). https://doi.org/10.1007/s12155-020-10114-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-020-10114-x

Keywords

Search

Navigation