Cell disruption of microalgae: advances and perspectives

Nunes, André Luiz Figueiredo; Lima, Viviane Sobreira; Miranda Júnior, José Roberto; Resende, Monique Ellen Torres; Silva, César Augusto Sodré da; Martins, Márcio Arêdes; Coimbra, Jane Selia dos Reis

doi:10.1590/0103-8478cr20220330

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Food technology • Cienc. Rural 54 (5) • May 2024 • https://doi.org/10.1590/0103-8478cr20220330 copy

Cell disruption of microalgae: advances and perspectives

Rompimento celular de microalgas: avanços e perspectivas

Authorship SCIMAGO INSTITUTIONS RANKINGS

RESUMO:

As microalgas são organismos cuja biomassa possui biomoléculas abundantes como carboidratos, lipídeos, proteínas, pigmentos, vitaminas, minerais e compostos antioxidantes, com inúmeras aplicações industriais com destaque para os segmentos de alimentos, nutricional, farmacológico, cosmético e de energia, na produção de biocombustíveis. Entretanto, o acesso de forma integra a essas biomoléculas pode ser dificultado pela rigidez estrutural de sua parede celular, sendo necessário a aplicação de um pré-tratamento que promova a lise celular. As diferentes técnicas de ruptura celular aplicáveis à biomassa microalgal descritas na literatura podem ser de natureza mecânica, com destaque para as técnicas de moagem em moinho de bolas e homogeneização à alta pressão (HAP) ou não mecânica (química, térmica e enzimática), cada uma com vantagens e desvantagens. Assim, o objetivo da presente revisão narrativa é descrever o uso de diferentes métodos para o rompimento de células de microalgas, com suas vantagens, desvantagens e seus desafios.

Palavras-chave:
homogeneização; moagem; enzimas; métodos químicos; métodos mecânicos e não mecânicos

Authorship

André Luiz Figueiredo Nunes

Departamento de Tecnologia de Alimentos, Universidade Federal de Viçosa (UFV), Campus Universitário, 36570-900, Viçosa, MG, Brasil..Universidade Federal de Viçosa (UFV)BrazilViçosa, MG, BrazilDepartamento de Tecnologia de Alimentos, Universidade Federal de Viçosa (UFV), Campus Universitário, 36570-900, Viçosa, MG, Brasil..

https://orcid.org/0000-0002-9918-3171

Viviane Sobreira Lima

https://orcid.org/0009-0005-4962-5305

José Roberto Miranda Júnior

https://orcid.org/0009-0003-0255-3602

Monique Ellen Torres Resende

Departamento de Farmácia, Universidade Federal de Juiz de Fora (UFJF), Governador Valadares, MG, Brasil.Universidade Federal de Juiz de Fora (UFJF)BrazilGovernador Valadares, MG, BrazilDepartamento de Farmácia, Universidade Federal de Juiz de Fora (UFJF), Governador Valadares, MG, Brasil.

https://orcid.org/0000-0002-4540-475X

César Augusto Sodré da Silva

https://orcid.org/0000-0002-7302-7058

Márcio Arêdes Martins

Departamento de Engenharia Agrícola, Universidade Federal de Viçosa (UFV), Viçosa, MG, Brasil.Universidade Federal de Viçosa (UFV)BrazilViçosa, MG, BrazilDepartamento de Engenharia Agrícola, Universidade Federal de Viçosa (UFV), Viçosa, MG, Brasil.

https://orcid.org/0000-0001-5705-9431

Jane Selia dos Reis Coimbra ^*E-mail: jcoimbra@ufv.br. *Corresponding author

https://orcid.org/0000-0002-5998-189X

E-mail: jcoimbra@ufv.br. ^*Corresponding author

Editor: Rudi Weiblen (0000-0002-1737-9817)

DECLARATION OF CONFLICT OF INTEREST

The authors declare no conflicts of interest and do not have any financial or personal association with institutions, teams, or individuals who could improperly affect the paper.

AUTHORS’ CONTRIBUTIONS

The authors contributed equally to the manuscript.

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (1)
Tables (3)

Thumbnail

Figure 1
Cell disruption methods.

Thumbnail

Table 1
Chemical composition of different microalgal species.

Thumbnail

Table 2
Mechanical techniques of microalgae cell disruption.

Thumbnail

Table 3
Non-mechanical rupture techniques.

Figure 1 Cell disruption methods.

Table 1 Chemical composition of different microalgal species.

Species	--------------------Composition (% dry matter)--------------------			References
	Proteins	Lipids	Carbohydrates
Chlorella vulgaris	51-58	14-22	12-17	MARTINS et al. (2010MARTINS, A. et al. Microalgae for biodiesel production and other applications: a review. Renewable Sustainable Energy Reviews, v.14, n.1, p.217-232, 2010. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S1364032109001646 >. Accessed: Apr. 08, 2022. doi: 10.1016/j.rser.2009.07.020. https://www.sciencedirect.com/science/ar... )
Chlorella pyrenoidosa	57	2	26	GOUVEIA et al. (2008GOUVEIA, L. et al. Microalgae in novel food product. In: KONSTANTINOS, N.; PAPADOPOULOS, P. P. Food Chemistry Research Developments. New York: Nova Science Publishers Inc., 2008. Chap.2, p.1-37.)
Dunaliela salina	57	6	32	GOUVEIA et al. (2008GOUVEIA, L. et al. Microalgae in novel food product. In: KONSTANTINOS, N.; PAPADOPOULOS, P. P. Food Chemistry Research Developments. New York: Nova Science Publishers Inc., 2008. Chap.2, p.1-37.)
Euglena gracilis	39-61	22-38	14-18	BRUTON (2009BRUTON, T. A review of the potential of marine algae as a source of biofuel in Ireland. Dublin: Sustainable Energy Ireland, 2009. 88p. (Technical Report). Available from: <Available from: http://cdn.technologynetworks.com/TN/Resources/PDF/algae%20report%2004%202009.pdf >. Accessed: Jul. 06, 2022. http://cdn.technologynetworks.com/TN/Res... ) GOUVEIA et al. (2008GOUVEIA, L. et al. Microalgae in novel food product. In: KONSTANTINOS, N.; PAPADOPOULOS, P. P. Food Chemistry Research Developments. New York: Nova Science Publishers Inc., 2008. Chap.2, p.1-37.)
Haematococcus pluvialis	10.2	40.7	33.6	BATISTA et al. (2013BATISTA, A. P. et al. Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Research, v.2, n.2, p.164-173, 2013. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S2211926413000210 >. Accessed: Jul. 06, 2022. doi: 10.1016/j.algal.2013.01.004. https://www.sciencedirect.com/science/ar... )
Porphyridium cruentum	28-39	9-14	40-57	BRUTON (2009BRUTON, T. A review of the potential of marine algae as a source of biofuel in Ireland. Dublin: Sustainable Energy Ireland, 2009. 88p. (Technical Report). Available from: <Available from: http://cdn.technologynetworks.com/TN/Resources/PDF/algae%20report%2004%202009.pdf >. Accessed: Jul. 06, 2022. http://cdn.technologynetworks.com/TN/Res... ) GOUVEIA et al. (2008GOUVEIA, L. et al. Microalgae in novel food product. In: KONSTANTINOS, N.; PAPADOPOULOS, P. P. Food Chemistry Research Developments. New York: Nova Science Publishers Inc., 2008. Chap.2, p.1-37.)
Scenedesmus obliquus	50-56	12-14	10-17	SPOLAORE et al. (2006SPOLAORE, P. et al. Commercial applications of microalgae. Journal of Bioscience and Bioengineering, v.101, n.2, p.87-96, 2006. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S1389172306705497 >. Accessed: Apr. 07, 2022. doi: 10.1263/jbb.101.87. https://www.sciencedirect.com/science/ar... ) CAI et al. (2013CAI, T. et al. Nutrient recovery from wastewater streams by microalgae: status and prospects. Renewable and Sustainable Energy Reviews, v.19, p.360-369, 2013. Available from: <https://www.sciencedirect.com/science/article/pii/S1364032112006429>. Accessed: Apr. 10, 2022. doi: 10.1016/j.rser.2012.11.030. https://doi.org/10.1016/j.rser.2012.11.0... )
Scenedesmus dimorphus	8-18	16-40	21-52	BRUTON (2009BRUTON, T. A review of the potential of marine algae as a source of biofuel in Ireland. Dublin: Sustainable Energy Ireland, 2009. 88p. (Technical Report). Available from: <Available from: http://cdn.technologynetworks.com/TN/Resources/PDF/algae%20report%2004%202009.pdf >. Accessed: Jul. 06, 2022. http://cdn.technologynetworks.com/TN/Res... ) GOUVEIA et al. (2008GOUVEIA, L. et al. Microalgae in novel food product. In: KONSTANTINOS, N.; PAPADOPOULOS, P. P. Food Chemistry Research Developments. New York: Nova Science Publishers Inc., 2008. Chap.2, p.1-37.)
Scenedesmus quadricauda	47	1-9	21-52	BRUTON (2009BRUTON, T. A review of the potential of marine algae as a source of biofuel in Ireland. Dublin: Sustainable Energy Ireland, 2009. 88p. (Technical Report). Available from: <Available from: http://cdn.technologynetworks.com/TN/Resources/PDF/algae%20report%2004%202009.pdf >. Accessed: Jul. 06, 2022. http://cdn.technologynetworks.com/TN/Res... )

Table 2 Mechanical techniques of microalgae cell disruption.

Rupture techniques	Species	Operating conditions	References
High-pressure homogenization	Chlorella vulgaris, Chlorella sorokiniana, Phaeodactylum tricornutum, Nannochloropsis	10% w v^-1 biomass 180 MPa, 22 °C	GROSSMANN et al., 2019
	Chlorella sorokiniana, Phaeodactylum tricornutum	5% w w^-1 oil/biomass 1000 bar, 3 passes	EBERT et al., 2019
	Chlorella vulgaris	10% w v^-1 biomass 150 MPa, 9 passes	DAI et al., 2020DAI, L. et al. Emulsifying properties of acid-hydrolyzed insoluble protein fraction from Chlorella protothecoides: Formation and storage stability of emulsions. Food Hydrocolloid, v.108, e105954, 2020. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0268005X19330413 >. Accessed: May, 10, 2021. doi: 10.1016/j.foodhyd.2020.105954. https://www.sciencedirect.com/science/ar...
HPH^* and alkaline treatment	Chlorella vulgaris	1.3% w v^-1 biomass 1.5 bar, 25 °C	URSU et al., 2014URSU, A. V. et al. Extraction, fractionation and functional properties of proteins from the microalgae Chlorella vulgaris. Bioresource Technology, v.157, p.134-139, 2014. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0960852414000960 >. Accessed: Oct. 19, 2021. doi: 10.1016/j.biortech.2014.01.071. https://www.sciencedirect.com/science/ar...
Grinding (ball mill)	Tetraselmis sp.	Flow rate: 1.5 L min^-1 30 min, 20 °C	SCHWENZFEIER et al., 2011SCHWENZFEIER, A. et al. Isolation and characterization of soluble protein from the green microalgae Tetraselmis sp. Bioresource Technology, v.102, n.19, p.9121-9127, 2011. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/21831634/ >. Accessed: Oct. 25, 2021. doi: 10.1016/j.biortech.2011.07.046. https://pubmed.ncbi.nlm.nih.gov/21831634...
	Parachlorella kessleri	Flow rate: 200 mL min^-1 20 °C	RIVERA et al., 2018
	Nannochloropsis oculate Porphyridium cruemtum	Flow rate: 48 to 200 mL min^-1, 8 m s^-1rotation speed, 0.375 - 2.15 mm ball diameter, 20 °C	MONTALESCOT et al., 2015MONTALESCOT, V. et al. Optimization of bead milling parameters for the cell disruption of microalgae: process modeling and application to Porphyridium Cruentum and Nannochloropsis Oculata. Bioresource Technology, v.196, p.339-346, 2015. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0960852415010378 >. Accessed: Sep. 18, 2021. doi: 10.1016/j.biortech.2015.07.075. https://www.sciencedirect.com/science/ar...
Sonication	Chlorella vulgaris	20% amplitude, 200 W, 5 pulses s^-1: on and off, 15 min	SANKARAN et al., 2018SANKARAN, R. et al. Extraction of proteins from microalgae using integrated method of sugaring-out assisted liquid biphasic flotation (LBF) and ultrasound. Ultrasonics Sonochemistry, v.48, p.231-239, 2018. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S1350417718300944 >. Accessed: Feb. 21, 2022. doi: 10.1016/j.ultsonch.2018.06.002. https://www.sciencedirect.com/science/ar...
Sonication	Scenedesmus obliquus	60% amplitude 20 KHz, 2 min	SILVA et al., 2021
Microwave	Scenedesmus obliquus	400 W, 10 min warm-up 0.25 h extraction	ZHOU et al., 2019
Microwave	Scnedesmus quadricauda	600 W, 8 min warm-up 3.5 h extraction	ONUMAEGBU et al., 2019
Hydrodynamic cavitation	Chlorella pyrenoidosa	1% w v^-1 solids, 80% amplitude, 90 min cavitation	WAGHMARE et al., 2019WAGHMARE, A. et al. Hydrodynamic cavitation for energy efficient and scalable process of microalgae cell disruption. Algal Research, v.40, e101496, 2019. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S2211926418306490 >. Accessed: Apr. 07, 2022. doi: 10.1016/j.algal.2019.101496. https://www.sciencedirect.com/science/ar...
Pulsed electric field	Haematococcus pluvialis	10 to 80 pulses 5 min, 1 Hz	MARTÍNEZ et al., 2019MARTÍNEZ, J. M. et al. Use of pulsed electric field permeabilization to extract astaxanthin from the nordic microalgae Haematococcus pluvialis. Bioresource Technology, v.289, p.e121694, 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31254897/ >. Accessed: Dec. 16, 2021. doi: 10.1016/j.biortech.2019.121694. https://pubmed.ncbi.nlm.nih.gov/31254897...
Thermal (Autoclaves)	Synechocystis PCC 6803	Autoclave: 15 min 121 °C (miminal)	SHENG. et al., 2012SHENG, J. et al. Disruption of Synechocystis PCC 6803 for lipid extraction. Water Science and Technology, v.65, p.567-73, 2012. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/22258690/ >. Accessed: Apr. 07, 2022. doi: 10.2166/wst.2012.879. https://pubmed.ncbi.nlm.nih.gov/22258690...

^*HPH: High-pressure homogenization.

Table 3 Non-mechanical rupture techniques.

-------Rupture techniques-------		Species	Operational conditions	References
Chemical	Acid	Scenedesmus sp. Chlorella sp. Ankistrosdemus sp. Micromonas sp. Chlamydomonas sp.	0 to 1.5 M H₂S0₄ 40 to 120 min hydrolysis 23 to 90 °C	CASTRO et al., 2015CASTRO, A. Y. et al. Optimization of wastewater microalgae saccharification using dilute acid hydrolysis for acetone, butanol, and ethanol fermentation. Applied Energy, v.140, n.15, p.14-19, 2015. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0306261914012148 >. Accessed: Sep. 18, 2021. doi: 10.1016/j.apenergy.2014.11.045. https://www.sciencedirect.com/science/ar...
		Spirulina plantesis	0.5 to 5.5 M H₂S0₄ 30 to 120 min hydrolysis 25 to 100 °C	DUONGBIA et al., 2019DUONGBIA, N. et al. Acidic hydrolysis performance and hydrolyzed lipid characterizations of wet Spirulina platensis. Biomass Conversion and Biorefinery, v.9, p.305-319, 2019. Available from: <Available from: https://link.springer.com/article/10.1007/s13399-018-0350-6 >. Accessed: Mar. 30, 2022. doi: 10.1007/s13399-018-0350-6. https://link.springer.com/article/10.100...
		Haematococcus pluvialis	0.5 to 4.5 M HCL 3.2 to 16.8 min hydrolysis 56 to 84 °C	VECHIO et al., 2021VECHIO, H. et al. A new approach on astaxanthin extraction via acid hydrolysis of wet Haematococcus pluvialis biomass. Journal of Applied Phycology, v.33, n.5, p.2957-2966, 2021. Available from: <Available from: https://link.springer.com/article/10.1007/s10811-021-02495-z >. Accessed: Apr. 10, 2022. doi: 10.1007/s10811-021-02495-z. https://link.springer.com/article/10.100...
	Alkaline	Chlorococcum infusionum	0.75% w v^-1 NaOH 30 min hydrolysis; 120 °C	HARUN et al., 2011HARUN, R. et al. . Exploring alkaline pretreatment of microalgal biomass for bioethanol production. Applied Energy, v.88, n.10, p.3464-3467, 2011. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S1364032109002664 >. Accessed: Apr. 03, 2022. doi: 10.1016/j.apenergy.2010.10.048. https://www.sciencedirect.com/science/ar...
	Surfactant	Nannochloropsis sp.	Surfactant concentration: 60 to 500 mg L^-1 Reaction time: 1 to 6 h 25 to 50 °C	WU et al., 2017WU, C. et al. Surfactants assist in lipid extraction from wet Nannochloropsis sp. Bioresource Technology , v.243, p.793-799, 2017. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S0960852417310969?via%3Dihub >. Accessed: Apr. 02, 2022. doi: 10.1016/j.biort ech.2017.07.010. https://www.sciencedirect.com/science/ar...
		Chlorella sorokiniana sp.	Surfactant concentration: 288.37 to 647 g mol^-1 Surface charge: -49.9 to 61.5 mV ^*CMC: 0.2 to 14.4 mM	TAGHAVIJELOUDAR et al., 2021TAGHAVIJELOUDAR, M. et al. Simultaneous harvesting and extracellular polymeric substances extrusion of microalgae using surfactant: Promoting surfactant-assisted flocculation through pH adjustment. Bioresource Technology, v.319, e124224, 2021. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S096085242031498X >. Accessed: Apr. 07, 2022. doi: 10.1016/j.biortech.2020.124224. https://www.sciencedirect.com/science/ar...
Biological	Enzymatic	Chlorella pyrenoidosa	10% w v^-1 biomass ^** Cellulase: 200 U g^-1 200 mL mixture	ZHANG et al., 2020ZHANG, J. et al. Utilization of enzymatic cell disruption hydrolysate ofChlorella pyrenoidosaas potential carbon source in algae mixotrophic cultivation. Algal Research, v.45, e101730, 2020. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S2211926419302723 >. Accessed: Apr. 05, 2022. doi: 10.1016/j.algal.2019.101730. https://www.sciencedirect.com/science/ar...
		Schizochytrium sp.	1:10 ratio of biomass:hemicellulase Reaction time: 48 h; 55 °C	HAC ISA et al., 2021HAC ISA, M. C. et al. Effect of different cell disruption methods on lipid yield of Schizochytrium sp. Journal of the American Oil Chemists` Society, v.99, n.2, p.129-139, 2021. Available from: <Available from: https://www.authorea.com/users/420143/articles/526520-effect-of-different-cell-disruption-methods-on-lipid-yield-of-schizochytrium-sp >. Accessed: Apr. 09, 2022. doi: 10.1002/aocs.12551. https://www.authorea.com/users/420143/ar...
	Enzymatic	Chlorella vulgaris	1.5·10^-4 to 2·10^-1 mg mL^-1 enzyme poll Reaction time: 24 h; 37 °C	CANELLI et al., 2021CANELLI, G. et al. Tailored enzymatic treatment of Chlorella vulgaris cell wall leads to effective disruption while preserving oxidative stability. LWT, Food Science and Technology, v.143, e111157, 2021. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S0023643821003108 >. Accessed: Dec. 17, 2021. doi: 10.1016/j.lwt.2021.111157. https://www.sciencedirect.com/science/ar...
---------Osmotic shock--------		Chaetoceros muelleri	1:5, biomass:water ratio	GONZÁLES-GONZÁLES et al., 2021GONZÁLES-GONZÁLES, L. M. et al. Osmotic shock pretreatment of Chaetoceros muelleri wet biomass enhanced solvent-free lipid extraction and biogas production. Algal Research, v.54, e10217, 2021. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S2211926420310456 >. Accessed: Apr. 05, 2022. doi: 10.1016/j.algal.2020.102177. https://www.sciencedirect.com/science/ar...

* Critical micelle concentration; ^**Amount to catalyze the transformation of 1 µmol of substrate per minute.

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[1] E-mail: jcoimbra@ufv.br. ^*Corresponding author