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Infrared spectroscopy as a tool to monitor interactions between nanoplastics and microalgae

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Abstract

The unicellular photosynthetic organisms known as microalgae are becoming one of the most important models for aquatic system studies. Among them, Chlamydomonas reinhardtii is widely used as a bioindicator of pollution or of different changes in the environment. Numerous pollutants are present in aquatic environments, particularly plastics and nanoplastics. Physiological variations after an environmental change highlight variation in the macromolecular composition of microalgae (proteins, nucleic acids, lipids and carbohydrates). Recently, Fourier transform infrared vibrational spectroscopy has been described as a reliable tool, sensitive and allowing rapid measurement of macromolecular composition of microalgae. Coupled with preprocessing and principal component analysis, it is well adapted to monitoring the effect of environmental stress on biochemical composition. In this study, infrared spectroscopy, combined with multivariate analysis, has been tested first on known environmental stresses such as light intensity variation and nitrogen limitation. Then, this technique has been applied to monitor the interaction and potential impacts of polystyrene nanoparticles on microalgae. The results showed slight variations on protein and carbohydrates bands in the presence of nanoplastics, suggesting that their presence led to modifications in the biochemical composition of the microalgae. To confirm the interaction between microalgae and nanoplastics, visualization by confocal microscopy and cytotoxicity measurement has been carried out. Results showed that polystyrene nanoparticles seemed to adsorb on microalgae surface, leading to a loss of plasma membrane integrity. The resulting chemical modifications, even if moderate, could be detected by infrared spectroscopy‚ showing that this tool could be very helpful in the understanding of nanoparticle-microalgae interaction mechanisms.

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References

  1. Irihimovitch V, Yehudai-Resheff S. Phosphate and sulfur limitation responses in the chloroplast of Chlamydomonas reinhardtii. FEMS Microbiol Lett. 2008;283:1–8. https://doi.org/10.1111/j.1574-6968.2008.01154.x.

    Article  CAS  PubMed  Google Scholar 

  2. Cid A, Prado R, Rioboo C, Suárez-Bregua P, Herrero C. Use of microalgae as biological indicators of pollution: looking for new relevant cytotoxicity endpoints. Microalgae Biotechnol Microbiol Energy 2013;311–324.

  3. Morlon H (2005) Mécanismes de prise en charge du sélénite – Se(IV)- chez l’algue verte unicellulaire Chlamydomonas reinhardtii. Bioaccumulation et effets induits sur la croissance et l’ultrastructure. Université de Bordeaux 1.

  4. Mata TM, Martins AA, Caetano NS. Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev. 2010;4:217–32. https://doi.org/10.1016/j.rser.2009.07.020.

    Article  CAS  Google Scholar 

  5. Minhas AK, Hodgson P, Barrow CJ, Adholeya A. A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front Microbiol. 2016;7:1–19. https://doi.org/10.3389/fmicb.2016.00546.

    Article  Google Scholar 

  6. Nama S, Madireddi SK, Devadasu ER, Subramanyam R. High light induced changes in organization, protein profile and function of photosynthetic machinery in Chlamydomonas reinhardtii. J Photochem Photobiol B Biol. 2015;152:367–76. https://doi.org/10.1016/j.jphotobiol.2015.08.025.

    Article  CAS  Google Scholar 

  7. Belotti G, De Caprariis B, De Filippis P, Scarsella M, Verdone N. Effect of Chlorella vulgaris growing conditions on bio-oil production via fast pyrolysis. Biomass Bioenergy. 2014;61:187–95. https://doi.org/10.1016/j.biombioe.2013.12.011.

    Article  CAS  Google Scholar 

  8. Illman A, Scragg AH, Shales SW. Increase in Chlorella strains calorific values. Enzym Microb Technol. 2000;27:631–5. https://doi.org/10.1016/S0141-0229(00)00266-0.

    Article  CAS  Google Scholar 

  9. Borowitzka MA, Huisman JM, Osborn A. Culture of the astaxanthin-producing green alga Haematococcus pluvialis. Effects of nutrients on growth and cell type. J Appl Phycol. 1991;3:295–304. https://doi.org/10.1007/BF02392882.

  10. Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS. Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol. 2009;100:833–8. https://doi.org/10.1016/j.biortech.2008.06.061.

    Article  CAS  PubMed  Google Scholar 

  11. Dubois M, Gilles KA, Hamilton JK, Pa R, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350–6.

    Article  CAS  Google Scholar 

  12. Smith P, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano M, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150:76–85.

    Article  CAS  Google Scholar 

  13. Mitić Ž, Stolić A, Stojanović S, Najman S, Ignjatović N, Nikolić G, et al. Instrumental methods and techniques for structural and physicochemical characterization of biomaterials and bone tissue: a review. Mater Sci Eng C. 2017;79:930–49. https://doi.org/10.1016/j.msec.2017.05.127.

    Article  CAS  Google Scholar 

  14. Jebsen C, Norici A, Wagner H, Palmucci M, Giordano M, Wilhelm C. FTIR spectra of algal species can be used as physiological fingerprints to assess their actual growth potential. Physiol Plant. 2012;146:427–38. https://doi.org/10.1111/j.1399-3054.2012.01636.x.

    Article  CAS  PubMed  Google Scholar 

  15. Wagner H, Liu Z, Langner U, Stehfest K, Wilhelm C. The use of FTIR spectroscopy to assess quantitative changes in the biochemical composition of microalgae. J Biophotonics. 2010;3:557–66.

    Article  CAS  PubMed  Google Scholar 

  16. Patel SA, Currie F, Thakker N, Goodacre R. Spatial metabolic fingerprinting using FT-IR spectroscopy: investigating abiotic stresses on Micrasterias hardyi. Analyst. 2008;133:1707–13. https://doi.org/10.1039/b809441a.

    Article  CAS  PubMed  Google Scholar 

  17. Driver T, Bajhaiya AK, Allwood JW, Goodacre R, Pittman JK, Dean AP. Metabolic responses of eukaryotic microalgae to environmental stress limit the ability of FT-IR spectroscopy for species identification. Algal Res. 2015;11:148–55. https://doi.org/10.1016/j.algal.2015.06.009.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dean A, Nicholson J, Sigee D. Impact of phosphorus quota and growth phase on carbon allocation in Chlamydomonas reinhardtii: an FTIR microspectroscopy study. Eur J Phycol. 2008;43:345–54. https://doi.org/10.1080/09670260801979287.

    Article  CAS  Google Scholar 

  19. Sigee DC, Bahrami F, Estrada B, Webster RE, Dean AP. The influence of phosphorus availability on carbon allocation and P quota in Scenedesmus subspicatus: a synchrotron-based FTIR analysis. Phycologia. 2007;46:583–92. https://doi.org/10.2216/07-14.1.

    Article  Google Scholar 

  20. Meng Y, Yao C, Xue S, Yang H. Application of fourier transform infrared (FT-IR) spectroscopy in determination of microalgal compositions. Bioresour Technol. 2014;151:347–54. https://doi.org/10.1016/j.biortech.2013.10.064.

    Article  CAS  PubMed  Google Scholar 

  21. Stehfest K, Toepel J, Wilhelm C. The application of micro-FTIR spectroscopy to analyze nutrient stress-related changes in biomass composition of phytoplankton algae. Plant Physiol Biochem. 2005;43:717–26. https://doi.org/10.1016/j.plaphy.2005.07.001.

    Article  CAS  PubMed  Google Scholar 

  22. Jakob T, Wagner H, Stehfest K, Wilhelm C. A complete energy balance from photons to new biomass reveals a light- and nutrient-dependent variability in the metabolic costs of carbon assimilation. J Exp Bot. 2007;58:2101–12. https://doi.org/10.1093/jxb/erm084.

    Article  CAS  PubMed  Google Scholar 

  23. Ter Halle A, Jeanneau L, Martignac M, Jardé E, Pedrono B, Brach L, et al. Nanoplastic in the North Atlantic Subtropical Gyre. Environ Sci Technol. 2017;51:13689–97. https://doi.org/10.1021/acs.est.7b03667.

    Article  PubMed  Google Scholar 

  24. Phuong NN, Zalouk-Vergnoux A, Poirier L, Kamari A, Châtel A, Mouneyrac C, et al. Is there any consistency between the microplastics found in the field and those used in laboratory experiments? Environ Pollut. 2016;211:111–23. https://doi.org/10.1016/j.envpol.2015.12.035.

    Article  CAS  PubMed  Google Scholar 

  25. Sjollema SB, Redondo-Hasselerharm P, Leslie HA, Kraak MHS, Vethaak AD. Do plastic particles affect microalgal photosynthesis and growth? Aquat Toxicol. 2016;170:259–61. https://doi.org/10.1016/j.aquatox.2015.12.002.

    Article  CAS  PubMed  Google Scholar 

  26. Bhattacharya P, Sijie L, James PT, Pu Chun K. Physical adsorption of charged plastic nanoparticles affects algal photosynthesis. J Phys Chem C. 2010;114:16556. https://doi.org/10.1021/jp1054759.

    Article  CAS  Google Scholar 

  27. Nolte TM, Hartmann NB, Kleijn JM, Garnæs J, van de Meent D, Jan Hendriks A, et al. The toxicity of plastic nanoparticles to green algae as influenced by surface modification, medium hardness and cellular adsorption. Aquat Toxicol. 2016;183:11–20. https://doi.org/10.1016/j.aquatox.2016.12.005.

    Article  CAS  PubMed  Google Scholar 

  28. Libralato G, Galdiero E, Falanga A, Carotenuto R, de Alteriis E, Guida M. Toxicity effects of functionalized quantum dots, gold and polystyrene nanoparticles on target aquatic biological models: a review. Molecules. 2017;22:1439. https://doi.org/10.3390/molecules22091439.

    Article  CAS  PubMed Central  Google Scholar 

  29. Bergami E, Pugnalini S, Vannuccini ML, Manfra L, Faleri C, Savorelli F, et al. Long-term toxicity of surface-charged polystyrene nanoplastics to marine planktonic species Dunaliella tertiolecta and Artemia franciscana. Aquat Toxicol. 2017;189:159–69. https://doi.org/10.1016/j.aquatox.2017.06.008.

    Article  CAS  PubMed  Google Scholar 

  30. Casado MP, Macken A, Byrne HJ. Ecotoxicological assessment of silica and polystyrene nanoparticles assessed by a multitrophic test battery. Environ Int. 2013;51:97–105. https://doi.org/10.1016/j.envint.2012.11.001.

    Article  CAS  PubMed  Google Scholar 

  31. Sack L, Zeyl C, Bell G, Sharbel T, Reboud X, Bernhardt T, et al. Isolation of four new strains of Chlamydomonas reinhardtii (Chlorophyta) from soil samples. J Phycol. 1994;30:770–3. https://doi.org/10.1088/1742-6596/194/4/042018.

    Article  CAS  Google Scholar 

  32. Gorman SD, Levine RP. Cytochrome F and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc Natl Acad Sci. 1965;54:1665–9. https://doi.org/10.1104/pp.126.1.69.

    Article  CAS  PubMed  Google Scholar 

  33. Pakrashi S, Dalai S, TC P, Trivedi S, Myneni R, Raichur AM, Chandrasekaran N, Mukherjee A (2013) Cytotoxicity of aluminium oxide nanoparticles towards fresh water algal isolate at low exposure concentrations. Aquat Toxicol 132–133:34–45 . https://doi.org/10.1016/j.aquatox.2013.01.018.

  34. Rammal A (2017) Mathématiques appliquées et traitement du signal pour l’évaluation de la dégradation de la biomasse lignocellulosique. Université de Reims Champagne-Ardenne.

  35. Giordano M, Ratti S, Domenighini A, Vogt F. Spectroscopic classification of 14 different microalga species: first steps towards spectroscopic measurement of phytoplankton biodiversity. Plant Ecol Divers. 2009;2:155–64. https://doi.org/10.1080/17550870903353088.

    Article  Google Scholar 

  36. Hu Q (2004) Environmental effects on cell composition. In: Handbook of microalgal culture: biotechnology and applied phycology, Richmond A. Oxford.

  37. Benavente-Valdés JR, Aguilar C, Contreras-Esquivel JC, Méndez-Zavala A, Montañez J. Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Reports. 2016;10:117–25. https://doi.org/10.1016/j.btre.2016.04.001.

    Article  Google Scholar 

  38. Markou G, Angelidaki I, Georgakakis D. Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biotechnol. 2012;96:631–45. https://doi.org/10.1007/s00253-012-4398-0.

    Article  CAS  PubMed  Google Scholar 

  39. Wiercigroch E, Szafraniec E, Czamara K, Pacia MZ, Majzner K, Kochan K, et al. Raman and infrared spectroscopy of carbohydrates: a review. Spectrochim Acta - Part A Mol Biomol Spectrosc. 2017;185:317–35. https://doi.org/10.1016/j.saa.2017.05.045.

    Article  CAS  Google Scholar 

  40. Mitić Ž, Nikolić GS, Cakić M, Premović P, Ilić L. FTIR spectroscopic characterization of cu(II) coordination compounds with exopolysaccharide pullulan and its derivatives. J Mol Struct. 2009;924–926:264–73. https://doi.org/10.1016/j.molstruc.2009.01.019.

    Article  CAS  Google Scholar 

  41. He M, Yan Y, Pei F, Wu M, Gebreluel T, Zou S, et al. Improvement on lipid production by Scenedesmus obliquus triggered by low dose exposure to nanoparticles. Sci Rep. 2017;7:15526. https://doi.org/10.1038/s41598-017-15667-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rueler JG, Ades DR. The role of iron nutrition in photosynthesis and nitrogen assimilation in Scenedesmus quadricauda (Chlorophyceae) 1. J Phycol. 1987;23:452–7.

    Article  Google Scholar 

  43. Wagner H, Dunker S, Liu Z, Wilhelm C. Subcommunity FTIR-spectroscopy to determine physiological cell states. Curr Opin Biotechnol. 2013;24:88–94. https://doi.org/10.1016/j.copbio.2012.09.008.

    Article  CAS  PubMed  Google Scholar 

  44. Murdock JN, Wetzel DL. FT-IR microspectroscopy enhances biological and ecological analysis of algae. Appl Spectrosc Rev. 2009;44:335–61. https://doi.org/10.1080/05704920902907440.

    Article  CAS  Google Scholar 

  45. Heraud P, Stojkovic S, Beardall J, McNaughton D, Wood BR. Intercolonial variability in macromolecular composition in P-starved and P-replete Scenedesmus populations revealed by infrared microspectroscopy. J Phycol. 2008;44:1335–9. https://doi.org/10.1111/j.1529-8817.2008.00564.x.

    Article  CAS  PubMed  Google Scholar 

  46. Suman TY, Radhika Rajasree SR, Kirubagaran R. Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol Environ Saf. 2015;113:23–30. https://doi.org/10.1016/j.ecoenv.2014.11.015.

    Article  CAS  PubMed  Google Scholar 

  47. Déniel M, Errien N, Daniel P, Caruso A, Lagarde F. Current methods to monitor microalgae-nanoparticle interaction and associated effects. Aquat Toxicol. 2019;217:105311. https://doi.org/10.1016/j.aquatox.2019.105311.

    Article  PubMed  Google Scholar 

  48. Zhang C, Wang J, Tan L, Chen X. Toxic effects of microplastic on marine microalgae Skeletonema costatum: interactions between microplastic and algae. Aquat Toxicol. 2016;178:158–64. https://doi.org/10.1016/j.aquatox.2016.07.020.

    Article  CAS  PubMed  Google Scholar 

  49. Mao Y, Ai H, Chen Y, Zhang Z, Zeng P, Kang L, et al. Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere. 2018;208:59–68. https://doi.org/10.1016/j.chemosphere.2018.05.170.

    Article  CAS  PubMed  Google Scholar 

  50. Wang Z-H, Nie X-P, Yue W-J, Li X. Physiological responses of three marine microalgae exposed to cypermethrin. Int J Clin Exp Med. 2016;9:14247–53. https://doi.org/10.1002/tox.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Frédéric Amiard for their technical assistance during infrared measurement. Acknowledgements to plateforme “Spectroscopy” and plateforme “Matière Molle” of Institut Molécules et Matériaux du Mans of Le Mans University for their technical support.

Funding

This work was supported financially by Conseil départemental de la Sarthe, Le Mans Métropole and ANR CESA (ANR-15-CE34-0006-02, NANOPLASTICS project).

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  1. Le Mans Université, IMMM UMR-CNRS 6283, Avenue Olivier Messiaen, 72085, Le Mans Cedex 9, France

    Maureen Déniel, Fabienne Lagarde & Nicolas Errien

  2. Laboratoire Mer, Molécules, Santé, EA 2160, Avenue Olivier Messiaen, 72085, Le Mans Cedex 9, France

    Aurore Caruso

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Déniel, M., Lagarde, F., Caruso, A. et al. Infrared spectroscopy as a tool to monitor interactions between nanoplastics and microalgae. Anal Bioanal Chem 412, 4413–4422 (2020). https://doi.org/10.1007/s00216-020-02683-9

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