Influence of chitosan-based carbon dots added in MgAC-containing culture medium on green alga Tetraselmis sp.

Abstract

The aim of this study was to evaluate the growth-promoting effects of the combination of magnesium aminoclay (MgAC) and amino-functionalized carbon dots (N(CD)s) on Tetraselmis sp. cultures with an emphasis on N(CD)s. To that end, simply sol-gel-synthesized MgAC and one-pot carbonization-synthesized N(CD)s were utilized. The as-prepared N(CD)s possessed the expected amino-functional groups, exhibited strong blue emission with bright luminescence, and showed a quantum yield (QY) of 5.69%. The maximum specific growth rate and biomass productivity were achieved with the combination of 0.1 g L−1 MgAC and 40 μg mL−1 N(CD)s, which afforded improvements in lipid and protein accumulation relative to the control, whereas carbohydrate accumulation slightly decreased. At low concentrations (0.1 g L−1), MgAC demonstrated growth stimulation. The N(CD) addition to the MgAC-containing medium further supported the Tetraselmis sp. cultures in counteracting the effects of UV radiation and in improving photosynthesis activity. In these ways, increased growth and biomass productivity under UV irradiation and enhanced pigment contents under the light-irradiance condition were obtained. Therefore, use of the MgAC-N(CD) combination as a culture-medium supplement is a promising method for microalgae biorefinery applications.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abu-Ghosh S, Kumar VB, Fixler D, Dubinsky Z, Gedanken A, Iluz D (2017) Nitrogen-doped carbon dots prepared from bovine serum albumin to enhance algal astaxanthin production. Algal Res 23:161–165

    Article  Google Scholar 

  2. Aro E-M, Kangasjärvi S, Noctor G, Neukermans J, Li S (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  3. Batschauer A (1998) Photoreceptors of higher plants. Planta 206:479–492

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. Briggs WR, Huala E (1999) Blue-light photoreceptors in higher plants. Annu Rev Cell Dev Biol 15:33–62

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  5. Chandrasekaran G, Han H-K, Kim G-J, Shin H-J (2011) Antimicrobial activity of delaminated aminopropyl functionalized magnesium phyllosilicates. Appl Clay Sci 53:729–736

    CAS  Article  Google Scholar 

  6. Choi M-H, Hwang Y, Lee HU, Kim B, Lee G-W, Oh Y-K, Andersen HR, Lee Y-C, Huh YS (2014) Aquatic ecotoxicity effect of engineered aminoclay nanoparticles. Ecotoxicol Environ Saf 102:34–41

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. Chu F-F, Chu P-N, Cai P-J, Li W-W, Lam PKS, Zeng RJ (2013) Phosphorus plays an important role in enhancing biodiesel productivity of Chlorella vulgaris under nitrogen deficiency. Bioresour Technol 134:341–346

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. da Rosa GM, Moraes L, Cardias BB, Souza MRAZ, Costa JAV (2015) Chemical absorption and CO2 biofixation via the cultivation of Spirulina in semicontinuous mode with nutrient recycle. Bioresour Technol 192:321–327

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. da Rosa GM, de Morais MG, Costa JAV (2018) Green alga cultivation with monoethanolamine: Evaluation of CO2 fixation and macromolecule production. Bioresour Technol 261:206–212

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  10. Dammak M, Hadrich B, Miladi R, Barkallah M, Hentati F, Hachicha R, Laroche C, Michaud P, Fendri I, Abdelkafi S (2017) Effects of nutritional conditions on growth and biochemical composition of Tetraselmis sp. Lipids Health Dis 16:41

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  11. Datta KKR, Achari A, Eswaramoorthy M (2013) Aminoclay: a functional layered material with multifaceted applications. J Mater Chem A 1:6707–6718

    CAS  Article  Google Scholar 

  12. de Morais MG, Costa JAV (2007) Carbon dioxide fixation by Chlorella kessleri, C. vulgaris, Scenedesmus obliquus and Spirulina sp. cultivated in flasks and vertical tubular photobioreactors. Biotechnol Lett 29:1349–1352

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Dinesh Kumar S, Ro K-M, Santhanam P, Dhanalakshmi B, Latha S, Kim M-K (2018) Initial population density plays a vital role to enhance biodiesel productivity of Tetraselmis sp. under reciprocal nitrogen concentration. Bioresour Technol Rep 3:15–21

    Article  Google Scholar 

  14. Dong X, Awak MA, Tomlinson N, Tang Y, Sun Y-P, Yang L (2017) Antibacterial effects of carbon dots in combination with other antimicrobial reagents. PLoS One 12:e0185324

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. Dong X, Liang W, Meziani MJ, Sun Y-P, Yang L (2020) Carbon dots as potent antimicrobial agents. Theranostics 10:671–686

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  17. Egeland ES (2016) Carotenoids. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 507–563

    Google Scholar 

  18. Farooq W, Lee HU, Huh YS, Lee Y-C (2016) Chlorella vulgaris cultivation with an additive of magnesium-aminoclay. Algal Res 17:211–216

    Article  Google Scholar 

  19. Fu L, Datta KKR, Spyrou K, Qi G, Sardar A, Khader MM, Zboril R, Giannelis EP (2017) Phyllosilicate nanoclay-based aqueous nanoparticle sorbent for CO2 capture at ambient conditions. Appl Mater Today 9:451–455

    Article  Google Scholar 

  20. Huang H, Hu H, Qiao S, Bai L, Han M, Liu Y, Kang Z (2015) Carbon quantum dot/CuSx nanocomposites towards highly efficient lubrication and metal wear repair. Nanoscale 7:11321–11327

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. Khatoon H, Haris H, Rahman NA, Zakaria MN, Begum H, Mian S (2018) Growth, proximate composition and pigment production of Tetraselmis chuii cultured with aquaculture wastewater. J Ocean Univ China 17:641–646

    CAS  Article  Google Scholar 

  22. Kim B, Praveenkumar R, Lee J, Nam B, Kim D-M, Lee K, Lee Y-C, Oh Y-K (2016a) Magnesium aminoclay enhances lipid production of mixotrophic Chlorella sp. KR-1 while reducing bacterial populations. Bioresour Technol 219:608–613

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. Kim G, Bae J, Lee K (2016b) Nitrate repletion strategy for enhancing lipid production from marine microalga Tetraselmis sp. Bioresour Technol 205:274–279

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. Kumar SD, Santhanam P, Lewis-Oscar F, Thajuddin N (2015) A dual role of marine microalga Chlorella sp. (PSDK01) in aquaculture effluent with emphasis on initial population density. Arab J Sci Eng 40:29–35

    CAS  Article  Google Scholar 

  25. Lee Y-C, Huh YS, Farooq W, Chung J, Han J-I, Shin H-J, Jeong SH, Lee J-S, Oh Y-K, Park J-Y (2013a) Lipid extractions from docosahexaenoic acid (DHA)-rich and oleaginous Chlorella sp. biomasses by organic-nanoclays. Bioresour Technol 137:74–81

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. Lee Y-C, Jin E, Jung SW, Kim Y-M, Chang KS, Yang J-W, Kim S-W, Kim Y-O, Shin H-J (2013b) Utilizing the algicidal activity of aminoclay as a practical treatment for toxic red tides. Sci Rep 3:1–8

    Google Scholar 

  27. Lee Y-C, Kim B, Farooq W, Chung J, Han J-I, Shin H-J, Jeong SH, Park J-Y, Lee J-S, Oh Y-K (2013c) Harvesting of oleaginous Chlorella sp. by organoclays. Bioresour Technol 132:440–445

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. Li S, Wang L, Chusuei CC, Suarez VM, Blackwelder PL, Micic M, Orbulescu J, Leblanc RM (2015a) Nontoxic carbon dots potently inhibit human insulin fibrillation. Chem Mater 27:1764–1771

    CAS  Article  Google Scholar 

  29. Li X, Rui M, Song J, Shen Z, Zeng H (2015b) Carbon and graphene quantum dots for optoelectronic and energy devices: a review. Adv Funct Mater 25:4929–4947

    CAS  Article  Google Scholar 

  30. Liu S, Tian J, Wang L, Zhang Y, Qin X, Luo Y, Asiri AM, Al-Youbi AO, Sun X (2012) Hydrothermal treatment of grass: a low-cost, green route to nitrogen-doped, carbon-rich, photoluminescent polymer nanodots as an effective fluorescent sensing platform for label-free detection of Cu(II) ions. Adv Mater 24:2037–2041

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. Liu Y, Liu YN, Park S-J, Zhang Y, Kim T, Chae S, Park M, Kim H-Y (2015) One-step synthesis of robust nitrogen-doped carbon dots: acid-evoked fluorescence enhancement and their application in Fe3+ detection. J Mater Chem A 3:17747–17754

    CAS  Article  Google Scholar 

  32. Liu X, Pang J, Xu F, Zhang X (2016) Simple approach to synthesize amino-functionalized carbon dots by carbonization of chitosan. Sci Rep 6:31100

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232

    CAS  Article  Google Scholar 

  34. Metzler DM, Erdem A, Tseng YH, Huang CP (2012) Responses of algal cells to engineered nanoparticles measured as algal cell population, chlorophyll a, and lipid peroxidation: effect of particle size and type. J Nanotechnol 2012:1–12

    Article  CAS  Google Scholar 

  35. Ming H, Ma Z, Liu Y, Pan K, Yu H, Wang F, Kang Z (2012) Large scale electrochemical synthesis of high quality carbon nanodots and their photocatalytic property. Dalton Trans 41:9526–9531

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. Nguyen MK, Moon J-Y, Bui VKH, Oh Y-K, Lee Y-C (2019) Recent advanced applications of nanomaterials in microalgae biorefinery. Algal Res 41:101522

    Article  Google Scholar 

  37. Nguyen MK, Moon J-Y, Lee Y-C (2020) Loading effects of low doses of magnesium aminoclay on microalgal Microcystis sp. KW growth, macromolecule productions, and cell harvesting. Biomass Bioenergy 139:105619

    CAS  Article  Google Scholar 

  38. Norsker N-H, Barbosa MJ, Vermuë MH, Wijffels RH (2011) Microalgal production — a close look at the economics. Biotechnol Adv 29:24–27

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  39. Panyakampol J, Cheevadhanarak S, Sutheeworapong S, Chaijaruwanich J, Senachak J, Siangdung W, Jeamton W, Tanticharoen M, Paithoonrangsarid K (2015) Physiological and transcriptional responses to high temperature in Arthrospira ( Spirulina ) platensis C1. Plant Cell Physiol 56:481–496

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. Pérez-Urria E, García AÁ (2015) Approach to a comparative study of the metabolism of porphyrins and chlorophylls. J Nat Sci 3:1–16

    Google Scholar 

  41. Rak J, Chomicz L, Wiczk J, Westphal K, Zdrowowicz M, Wityk P, Żyndul M, Makurat S, Golon Ł (2015) Mechanisms of damage to DNA labeled with electrophilic nucleobases induced by ionizing or UV radiation. J Phys Chem B 119:8227–8238

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  42. Ruiz V, Yate L, García I, Cabanero G, Grande H-J (2017) Tuning the antioxidant activity of graphene quantum dots: protective nanomaterials against dye decoloration. Carbon N Y 116:366–374

    CAS  Article  Google Scholar 

  43. Sahu S, Behera B, Maiti TK, Mohapatra S (2012) Simple one-step synthesis of highly luminescent carbon dots from orange juice: application as excellent bio-imaging agents. Chem Commun 48:8835–8837

    CAS  Article  Google Scholar 

  44. Sinha RP, Häder D-P (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  45. Torkamani S, Wani SN, Tang YJ, Sureshkumar R (2010) Plasmon-enhanced microalgal growth in miniphotobioreactors. Appl Phys Lett 97:43703

    Article  CAS  Google Scholar 

  46. Trovão M, Pereira H, Silva J, Páramo J, Quelhas P, Santos T, Silva JT, Machado A, Gouveia L, Barreira L, Varela J (2019) Growth performance, biochemical composition and sedimentation velocity of Tetraselmis sp. CTP4 under different salinities using low-cost lab- and pilot-scale systems. Heliyon 5:e01553–e01553

    PubMed  PubMed Central  Article  Google Scholar 

  47. Wang F, Kreiter M, He B, Pang S, Liu C (2010) Synthesis of direct white-light emitting carbogenic quantum dots. Chem Commun 46:3309–3311

    CAS  Article  Google Scholar 

  48. 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 25:253–260

  49. Wang W, Li Y, Cheng L, Cao Z, Liu W (2014) Water-soluble and phosphorus-containing carbon dots with strong green fluorescence for cell labeling. J Mater Chem B 2:46–48

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  50. Wu Q, Li W, Tan J, Wu Y, Liu S (2015) Hydrothermal carbonization of carboxymethylcellulose: one-pot preparation of conductive carbon microspheres and water-soluble fluorescent carbon nanodots. Chem Eng J 266:112–120

    CAS  Article  Google Scholar 

  51. Yang L, Lee Y-C, Kim MI, Park HG, Huh YS, Shao Y, Han H-K (2014) Biodistribution and clearance of aminoclay nanoparticles: implication for in vivo applicability as a tailor-made drug delivery carrier. J Mater Chem B 2:7567–7574

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. Yu X, Chen L, Zhang W (2015) Chemicals to enhance microalgal growth and accumulation of high-value bioproducts. Front Microbiol 6:56

    PubMed  PubMed Central  Google Scholar 

  53. Zhang Y, Xue C, Xue Y, Gao R, Zhang X (2005) Determination of the degree of deacetylation of chitin and chitosan by X-ray powder diffraction. Carbohydr Res 340:1914–1917

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. Zhang M, Wang H, Song Y, Huang H, Shao M, Liu Y, Li H, Kang Z (2018) Pristine carbon dots boost the growth of Chlorella vulgaris by enhancing photosynthesis. ACS Appl Bio Mater 1:894–902

    CAS  Article  Google Scholar 

Download references

Funding

This work was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF2017R1D1A1A09000642), and this research was supported by Basic Science Research Capacity Enhancement Project through Korea Basic Science Institute (National research Facilities and Equipment Center) grant funded by the Ministry of Education (2019R1A6C1010016), and this work was supported by the Gachon University research fund of 2019 (GCU-2019-0818).

Author information

Affiliations

Authors

Contributions

Study conception and design, data acquisition, analysis and interpretation (M.K.N.); drafting (M.K.N.); critical revision for important content (M.K.N.; M.-K.K.; J.-Y.M.; V.V.T.; Y.-C.L.); final approval of manuscript (M.K.N.; M.-K.K.; J.-Y.M.; V.V.T.; Y.-C.L.).

Corresponding author

Correspondence to Young-Chul Lee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Supplementary Information

ESM 1

(PDF 298 kb)

ESM 2

(PDF 366 kb)

ESM 3

(PDF 233 kb)

ESM 4

(PDF 453 kb)

ESM 5

(PDF 243 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nguyen, M.K., Kim, MK., Moon, JY. et al. Influence of chitosan-based carbon dots added in MgAC-containing culture medium on green alga Tetraselmis sp.. J Appl Phycol (2021). https://doi.org/10.1007/s10811-021-02368-5

Download citation

Keywords

  • Aminoclay
  • Carbon dots
  • Green algae
  • Cultivation
  • Macromolecules