Optimization of cell disruption methods for efficient recovery of bioactive metabolites via NMR of three freshwater microalgae (chlorophyta)
Abstract
This study demonstrates the use of NMR techniques coupled with chemometric analysis as a high throughput data mining method to identify and examine the efficiency of different disruption techniques tested on microalgae (Chlorella variabilis, Scenedesmus regularis and Ankistrodesmus gracilis). The yield and chemical diversity from the disruptions together with the effects of pre-oven and pre-freeze drying prior to disruption techniques were discussed. HCl extraction showed the highest recovery of oil compounds from the disrupted microalgae (up to 90%). In contrast, NMR analysis showed the highest intensity of bioactive metabolites obtained for homogenized extracts pre-treated with freeze-drying, indicating that homogenizing is a more favorable approach to recover bioactive substances from the disrupted microalgae. The results show the potential of NMR as a useful metabolic fingerprinting tool for assessing compound diversity in complex microalgae extracts.
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Ma et al. optimized a microalgae cell disruption technique using nuclear magnetic resonance (NMR) coupled with chemometrics.
“Ma et al. [108] optimized a microalgae cell disruption technique using nuclear magnetic resonance (NMR) coupled with chemometrics.”
From Factors Affecting Microalgae Production for Biofuels and the Potentials of Chemometric Methods in Assessing and Optimizing Productivity (2019) · cites this paper as [108]
Recent studies in microalgae employ extraction strategies that involve the selection of improved formula for solvents, as well as other technologies like supercritical fluid extraction and electrical disruption, which do not use toxic solvents.
“Recent studies in microalgae employ extraction strategies that involve the selection of improved formula for solvents, as well as other technologies like supercritical fluid extraction and electrical disruption, which do not use toxic solvents [108].”
From Factors Affecting Microalgae Production for Biofuels and the Potentials of Chemometric Methods in Assessing and Optimizing Productivity (2019) · cites this paper as [108]
In Ma et al.'s study, identification of metabolites from a high-complexity microalgae extract was achieved.
“The identification of metabolites from a high complexity of microalgae extract was achieved in this study.”
From Factors Affecting Microalgae Production for Biofuels and the Potentials of Chemometric Methods in Assessing and Optimizing Productivity (2019) · cites this paper as [108]
In Ma et al.'s study, PCA and PLSDA revealed the effect of pre-treatment.
“Furthermore, the PCA and partial list squares discriminant analysis (PLSDA) revealed the effect of pre-treatment.”
From Factors Affecting Microalgae Production for Biofuels and the Potentials of Chemometric Methods in Assessing and Optimizing Productivity (2019) · cites this paper as [108]
Cites
Brennan, L., & Owende, P. (2010) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2009.10.009 · Cited by 4,894 · see citing works
Beckonert, O. P., Keun, H. C., Ebbels, T. M. D., Bundy, J. G., Holmes, E. C., Lindon, J. C., & Nicholson, J. K. (2007) · Nature Protocols · doi:10.1038/nprot.2007.376 · Cited by 2,112 · see citing works
Trygg, J., Holmes, E. C., & Lundstedt, T. (2006) · Journal of Proteome Research · doi:10.1021/pr060594q · Cited by 1,276 · see citing works
Commercial potential for Haematococcus microalgae as a natural source of astaxanthin
Lorenz, R. T., & Cysewski, G. R. (2000) · Trends in biotechnology · doi:10.1016/s0167-7799(00)01433-5 · Cited by 1,190 · see citing works
Extraction of oil from microalgae for biodiesel production: A review
Halim, R., Danquah, M. K., & Webley, P. A. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2012.01.001 · Cited by 1,043 · see citing works
Metabolites from algae with economical impact
Cardozo, K. H. M., Guaratini, T., Barros, M. P., Falcão, V. D. R., Tonon, Â. P., Lopes, N. P., Campos, S. C. G., Torres, M. A., Souza, A. D. O., Colepicolo, P., et al. (2006) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2006.05.007 · Cited by 960 · see citing works
Fleurence, J. (1999) · Trends in Food Science & Technology · doi:10.1016/s0924-2244(99)00015-1 · Cited by 933 · see citing works
Gil-Chávez, J., Villa-Rodríguez, J. A., Ayala-Zavala, J. F., Heredia, J. B., Sepulveda, D. R., Yahia, E. M., & González-Aguilar, G. A. (2013) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12005 · Cited by 658 · see citing works
Martins, A., Vieira, H., Gaspar, H., & Santos, S. (2014) · Marine Drugs · doi:10.3390/md12021066 · Cited by 576 · see citing works
Developments in oil extraction from microalgae
Mercer, P., & Armenta, R. E. (2011) · European Journal of Lipid Science and Technology · doi:10.1002/ejlt.201000455 · Cited by 532 · see citing works
Aqueous extraction of proteins from microalgae: Effect of different cell disruption methods
Safi, C., Ursu, A.-V., Laroche, C., Zebib, B., Merah, O., Pontalier, P.-Y., & Vaca‐García, C. (2014) · Algal Research · doi:10.1016/j.algal.2013.12.004 · Cited by 394 · see citing works
Selective extraction from microalgae Nannochloropsis sp. using different methods of cell disruption
Grimi, N., Dubois, A., Marchal, L., Jubeau, S., Lebovka, N., & Vorobiev, E. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.12.011 · Cited by 314 · see citing works
Araújo, G. S., de Matos, L. J. B. L., Fernandes, J. O., Cartaxo, S. J. M., Gonçalves, L. R. B., Fernandes, F. A. N., & Farias, W. R. L. (2012) · Ultrasonics Sonochemistry · doi:10.1016/j.ultsonch.2012.07.027 · Cited by 293 · see citing works
Li, Y., Ghasemi Naghdi, F., Garg, S., Adarme-Vega, T., Thurecht, K. J., Ghafor, W., Tannock, S., & Schenk, P. M. (2014) · Microbial Cell Factories · doi:10.1186/1475-2859-13-14 · Cited by 261 · see citing works
Factors affecting cellular lipid extraction from marine microalgae
Balasubramanian, R. K., Doan, Y. T.-T., & Obbard, J. P. (2012) · Chemical Engineering Journal · doi:10.1016/j.cej.2012.11.063 · Cited by 173 · see citing works
Microalgae in the postgenomic era: a blooming reservoir for new natural products
Sasso, S., Pohnert, G., Lohr, M., Mittag, M., & Hertweck, C. (2011) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2011.00304.x · Cited by 171 · see citing works
An investigation of ultrasound effect on microalgal cell integrity and lipid extraction efficiency
Keris-Sen, U. D., Sen, U., Soydemir, G., & Gurol, M. D. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.11.018 · Cited by 139 · see citing works
Cheng, J., Sun, J., Huang, Y. Y., Feng, J., Zhou, J., & Cen, K. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.09.126 · Cited by 105 · see citing works
Lophocladines, Bioactive Alkaloids from the Red Alga Lophocladia sp.
Gross, H., Goeger, D. E., Hills, P., Mooberry, S. L., Ballantine, D. L., Murray, T. F., Valeriote, F. A., & Gerwick, W. H. (2006) · Journal of Natural Products · doi:10.1021/np050519e · Cited by 101 · see citing works
San, T., Chen, J. W., Giap, S. G. E., Ahmad, A., & Loh, S. H. (2011) · Bioresource Technology · doi:10.1016/j.biortech.2011.09.042 · Cited by 91 · see citing works
Antti, H., Ebbels, T. M. D., Keun, H. C., et al. (2004) · Chemometrics and Intelligent Laboratory Systems · doi:10.1016/j.chemolab.2003.11.013 · Cited by 77 · see citing works
1H NMR-based metabonomics for the diagnosis of inborn errors of metabolism in urine
Constantinou, M. A., Papakonstantinou, E., Spraul, M., Sevastiadou, S., Costalos, C., Koupparis, M. Α., Shulpis, K., Tsantili‐Kakoulidou, A., & Mikros, E. (2005) · Analytica Chimica Acta · doi:10.1016/j.aca.2005.03.059 · Cited by 75 · see citing works
Harvesting and extraction technology contributions to algae biofuels economic viability
Richardson, J. W., Johnson, M. D., Lacey, R. E., Oyler, J., & Capareda, S. C. (2014) · Algal Research · doi:10.1016/j.algal.2014.05.007 · Cited by 70 · see citing works
Selection and optimisation of a method for efficient metabolites extraction from microalgae
Serive, B., Kaas, R., Bérard, J., Pasquet, V., Picot, L., & Cadoret, J. (2012) · Bioresource Technology · doi:10.1016/j.biortech.2012.07.105 · Cited by 59 · see citing works
Central metabolic processes of marine macrophytic algae revealed from NMR based metabolome analysis
Gupta, V., Thakur, R. S., Reddy, C. R. K., et al. (2013) · RSC Advances · doi:10.1039/c3ra23017a · Cited by 55 · see citing works
Analyses of photoprotective compounds in red algae from the Brazilian coast
Cardozo, K. H. M., Marques, L. G., Carvalho, V. M., Carignan, M. O., Pinto, E., Marinho‐Soriano, E., & Colepicolo, P. (2011) · Revista Brasileira de Farmacognosia · doi:10.1590/s0102-695x2011005000047 · Cited by 49 · see citing works
Aquatic Microalgae As Potential Sources Of Uv-Screening Compounds
Dionisio‐Sese, M. L. (2010) · The Philippine journal of science · Cited by 24 · see citing works
Algal Bioactive Diversities Against Pathogenic MicrobesPreprint
Parsaeimehr, A. (2013) · SSRN Electronic Journal · Cited by 7 · see citing works
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Musa, M., Ayoko, G. A., Ward, A., Rösch, C., Brown, R. J., & Rainey, T. J. (2019) · Cells · doi:10.3390/cells8080851 · Cited by 97 · see citing works
- Authors
- Ma, N. L., Teh, K. Y., Lam, S. S., Kaben, A. M., & Cha, T. S.
- Affiliations
- Universiti Malaysia Terengganu (MY)
- Venue
- Bioresource Technology
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 190
- Pages
- 536-542
- ISSN
- 0960-8524 (ISSN-L)
- OpenAlex
- W2063366506
- Cited by
- 19
- References
- 28
- Citations by year
- 2026: 2 · 2025: 3 · 2023: 1 · 2021: 2 · 2020: 5 · 2019: 3 · 2017: 2 · 2016: 1
- FWCI
- 0.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bioresource Technology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Universiti Malaysia Terengganu (59264)
- Ministry of Higher Education, Malaysia
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Seaweed-derived Bioactive Compounds
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- cell disruption, microalgae, Chlorella variabilis, bioactive metabolites, NMR metabolomics, homogenization, sonication, HCl extraction, freeze-drying, metabolic fingerprinting, chemometrics
- MeSH terms
- Chlorophyta, Biological Factors, Cell Fractionation, Freezing, Hydrochloric Acid, Magnetic Resonance Spectroscopy, Sonication
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