Abstract
The photosynthetic efficiency (PE) and potential of Phaeodactylum tricornutum for CO2 mitigation in industrial tubular photobioreactors (PBRs) of different volumes were evaluated. A preliminary assay was performed at lab-scale to optimize the salt concentration of the culture medium. Interestingly, salinity did not affect the growth of P. tricornutum at concentrations of 2.5, 5, 10, and 20 g L−1. Higher volumetric productivities were achieved in the 2.5-m3 tubular PBR (0.235 g L−1 day−1), followed by 35- and 10-m3 PBRs. Maximum areal productivities corresponded to 48.5, 45.0, and 12.8 g m−2 day−1 for the 35-, 10-, and 2.5-m3 PBRs, respectively. PE was thus higher in the 35- and 10-m3 PBRs (2.21 and 2.08%, respectively). The 10- and 35-m3 PBR showed CO2 mitigation efficiencies of 60 and 41%, respectively, of the CO2 introduced into the PBR, corresponding to 2.3 and 2.5 g of fixed CO2 per g of biomass. Overall, cultivation of P. tricornutum couples high PE and areal productivity when the industrial PBRs were used, particularly PBRs of larger volumes. This improved PE performance with larger PBR volumes strongly suggests that large-scale cultivation of this diatom holds great potential for industrial CO2 mitigation.
Similar content being viewed by others
References
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, de Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, la Roche J, Lindquist E, Lommer M, Martin–Jézéquel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Secq MPO–L, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, van de Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244
Buono S, Colucci A, Angelini A, Langellotti AL, Massa M, Martello A, Fogliano V, Dibenedetto A (2016) Productivity and biochemical composition of Tetradesmus obliquus and Phaeodactylum tricornutum: effects of different cultivation approaches. J Appl Phycol 28:3179–3192
Callejón-Ferre AJ, Velázquez-Martí B, López-Martínez JA, Manzano-Agugliaro F (2011) Greenhouse crop residues: energy potential and models for the prediction of their higher heating value. Renew Sust Energ Rev 15:948–955
Cornet JF (2010) Calculation of optimal design and ideal productivities of volumetrically lightened photobioreactors using the constructal approach. Chem Eng Sci 65:985–998
De Martino A, Meichenin A, Shi J, Pan K, Bowler C (2007) Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J Phycol 43:992–1009
De Martino A, Bartual A, Willis A, Meichenin A, Villazán B, Maheswari U, Bowler C (2011) Physiological and molecular evidence that environmental changes elicit morphological interconversion in the model diatom Phaeodactylum tricornutum. Protist 162:462–481
Dragone G, Fernandes B, Vicente AA, Teixeira JA (2010) Third generation biofuels from microalgae. In: Mendez-Vilas A (ed) Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, 1st edn. Formatex Research Center, Badajoz, pp 1355–1366
Fernández FGA, Hall DO, Guerrero EC, Rao KK, Grima EM (2003) Outdoor production of Phaeodactylum tricornutum biomass in a helical reactor. J Biotechnol 103:137–152
García MCC, Sevilla JMF, Fernández FGA, Grima EM, Camacho FG (2000) Mixotrophic growth of Phaeodactylum tricornutum on glycerol: growth rate and fatty acid profile. J Appl Phycol 12:239–248
Granum E, Kirkvold S, Myklestad SM (2002) Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar Ecol Prog Ser 242:83–94
Grognard F, Akhmetzhanov AR, Bernard O (2014) Automatica optimal strategies for biomass productivity maximization in a photobioreactor using natural light. Autom 50:359–368
Gügi B, Le Costaouec T, Burel C, Lerouge P, Helbert W, Bardor M (2015) Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms. Mar Drugs 13:5993–6018
Hamilton ML, Warwick J, Terry A, Allen ML, Napier A, Sayanova O (2015) Towards the industrial production of Omega-3 long chain polyunsaturated fatty acids from a genetically modified diatom Phaeodactylum tricornutum. PLoS One 10:e0144054
Hamilton ML, Powers S, Napier JA, Sayanova O (2016) Heterotrophic production of omega-3 long-chain polyunsaturated fatty acids by trophically converted marine diatom Phaeodactylum tricornutum. Mar Drugs 14:53
Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S (2010) Biofuels from algae: challenges and potential. Biofuels 1:763–784
Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R (2012) The place of diatoms in the biofuels industry. Biofuels 3:221–240
Kumar K, Dasgupta CN, Nayak B, Lindblad P, Das D (2011) Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol 102:4945–4953
Laws EA, Bidigare RR, Popp BN (1997) Effect of growth rate and CO2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol Oceanogr 42:1552–1560
Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396
Liang Y, Sun M, Tian C, Cao C, Li Z (2014) Effects of salinity stress on the growth and chlorophyll fluorescence of Phaeodactylum tricornutum and Chaetoceros gracilis (Bacillariophyceae). Bot Mar 57:469–476
Liu L, Pohnert G, Wei D (2016) Extracellular metabolites from industrial microalgae and their biotechnological potential. Mar Drugs 14:191
Marinho YF, Brito LO, Campos CVS, Severi W, Andrade HA, Galvez AO (2017) Effect of the addition of Chaetoceros calcitrans, Navicula sp. and Phaeodactylum tricornutum (diatoms) on phytoplankton composition and growth of Litopenaeus vannamei (Boone) postlarvae reared in a biofloc system. Aquac Res 48:4155–4164
Mata TM, Melo AC, Simões M, Caetano NS (2012) Parametric study of a brewery effluent treatment by microalgae Scenedesmus obliquus. Bioresour Technol 107:151–158
Morais KCC, Vargas JVC, Mariano AB, Ordonez JC, Kava V (2016) Sustainable energy via biodiesel production from autotrophic and mixotrophic growth of the microalga Phaeodactylum tricornutum in compact photobioreactors. SusTech
Myint MT, Ghassemi A, Nirmalakhandan N (2013) A generic stoichiometric equation for microalgae – microorganism nexus by using clarified domestic wastewater as growth medium. Desalin Water Treat 51:6632–6640
Nunez M, Quigg A (2016) Changes in growth and composition of the marine microalgae Phaeodactylum tricornutum and Nannochloropsis salina in response to changing sodium bicarbonate concentrations. J Appl Phycol 28:2123–2138
Pereira H, Barreira L, Mozes A, Florindo C, Polo C, Duarte CV, Custódio L, Varela J (2011) Microplate-based high throughput screening procedure for the isolation of lipid-rich marine microalgae. Biotechnol Biofuels 4:61
Pereira H, Polo C, Rešek E, Engelen A (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935
Pereira H, Gangadhar KN, Schulze PSC, Santos T, Sousa CB, Schueler LM, Custódio L, Malcata FX, Gouveia L, Varela JCS, Barreira L (2016) Isolation of a euryhaline microalgal strain, Tetraselmis sp. CTP4, as a robust feedstock for biodiesel production. Sci Rep 6:35663
Pereira H, Páramo J, Silva J, Marques A, Barros A, Maurício D, Santos T, Schulze P, Barros R, Gouveia L, Barreira L, Varela J (2018) Scale-up and large-scale production of Tetraselmis sp. CTP4 (Chlorophyta) for CO2 mitigation: from an agar plate to 100-m3 industrial photobioreactors. Sci Rep 8:5112
Pérez-lópez P, González-garcía S, Allewaert C, Verween A, Murray P, Feijoo G, Teresa M (2014) Environmental evaluation of eicosapentaenoic acid production by Phaeodactylum tricornutum. Sci Total Environ 466:991–1002
Pires JCM, Alvim-Ferraz MCM, Martins FG, Simões M (2012) Carbon dioxide capture from flue gases using microalgae: engineering aspects and biorefinery concept. Renew Sust Energ Rev 16:3043–3053
Prestegard SK, Knutsen G, Herfindal L (2014) Adenosine content and growth in the diatom Phaeodactylum tricornutum (Bacillariophyceae): effect of salinity, light, temperature and nitrate. Diatom Res 29:37–41
Prestegard SK, Erga SR, Steinrücken P, Mjøs SA (2015) Specific metabolites in a Phaeodactylum tricornutum strain isolated from western Norwegian Fjord water. Mar Drugs 14:9
Rebolloso-Fuentes MM, Navarro-Pérez A, García-Camacho F, Ramos-Miras JJ, Guil-Guerrero JL (2001) Biomass nutrient profiles of the microalga Nannochloropsis. J Agric Food Chem 49:2966–2972
Reis A, Gouveia L, Veloso V, Fernandes HL, Empis JA, Novais JM (1996) Eicosapentaenoic acid-rich biomass production by the microalga Phaeodactylum tricornutum in a continuous-flow reactor. Bioresour Technol 55:83–88
Remmers IM, Martens DE, Wijffels RH, Lamers PP (2017) Dynamics of triacylglycerol and EPA production in Phaeodactylum tricornutum under nitrogen starvation at different light intensities. PLoS One 12:e0175630
Robbins A (2016) How to understand the results of the climate change summit: conference of Parties21 (COP21) Paris 2015. J Public Health Policy 37:129–132
Rodolfi L, Biondi N, Guccione A, Bassi N, D'Ottavio M, Arganaraz G, Tredici MR (2017) Oil and eicosapentaenoic acid production by the diatom Phaeodactylum tricornutum cultivated outdoors in Green Wall Panel (GWP®) reactors. Biotechnol Bioeng 104:2204–2210
Ryckebosch E, Bruneel C, Termote-Verhalle R, Goiris K, Muylaert K, Foubert I (2014) Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil. Food Chem 160:393–400
Santos MM, Moreno-Garrido I, Gonçalves F, Soares AMV, Ribeiro R (2002) An in situ bioassay for estuarine environments using the microalga Phaeodactylum tricornutum. Environ Toxicol Chem 21:567–574
Sayre R (2010) Microalgae: the potential for carbon capture. BioScience 60:722–727
Slegers PM, Van Beveren PJM, Wijffels RH, Van Straten G, Van Boxtel AJB (2013) Scenario analysis of large scale algae production in tubular photobioreactors. Appl Energy 105:395–406
Sobczuk TM, Camacho FG, Rubio FC, Fernández FCA, Grima EM (2000) Carbon dioxide uptake efficiency by outdoor microalgal cultures in tubular airlift photobioreactors. Biotechnol Bioeng 67:465–475
Steinrücken P, Prestegard SK, De Vree JH, Storesund JE, Pree B, Mjøs SA, Erga SR (2018) Comparing EPA production and fatty acid profiles of three Phaeodactylum tricornutum strains under western Norwegian climate conditions. Algal Res 30:11–22
Swanson D, Block R, Mousa SA (2012) Omega-3 fatty acids EPA and DHA: health benefits throughout life. Adv Nutr 3:1–7
Thaulow N, Sahu S (2004) Mechanism of concrete deterioration due to salt crystallization. Mater Charact 53:123–127
Thornton DCO (2014) Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 49:20–46
Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Gałuszka A, Cearreta A, Edgeworth M, Ellis EC, Ellis M, Jeandel C, Leinfelder R, McNeill JR, Richter D, Steffen W, Syvitski J, Vidas D, Wagreich M, Williams M, Zhisheng A, Grinevald J, Odada E, Oreskes N, Wolfe AP (2016) The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351:137–148
Wen ZY, Chen F (2003) Heterotrophic production of eicosapentaenoic acid by microalgae. Biotechnol Adv 21:273–294
Yan N, Fan C, Chen Y, Hu Z (2016) The potential for microalgae as bioreactors to produce pharmaceuticals. Int J Mol Sci 17:E962
Yongmanitchai W, Ward OP (1991) Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Appl Environ Microbiol 57:419–425
Zhao P, Gu W, Wu S, Huang A, He L, Xie X, Gao S, Zhang B, Niu J, Lin AP, Wang G (2014) Silicon enhances the growth of Phaeodactylum tricornutum Bohlin under under green light and low temperature. Sci Rep 4:3958
Funding
The present work was funded by the Portuguese national budget P2020 in the scope of the project no. 023310 – ALGACO2: “Cultivo industrial de microalgas como tecnologia verde para captura de CO2 atmosférico” and CCMAR/Multi/04326/2013 grant of the Foundation for Science and Technology (FCT). H.P. (SFRH/BD/105541/2014) was funded by a PhD grant from FCT.
Author information
Authors and Affiliations
Contributions
PQ conceived, designed, and performed the experiments, interpreted the data with statistical expertise, prepared the figures/tables, and wrote the manuscript; MT, JTS, AM, and TS collected and assembled the data, prepared figures/tables, and drafted the manuscript; HP and JV designed the experiences, analyzed and interpreted the data, and critically revised the manuscript; MS and JLS designed the experiences, analyzed and interpreted the data, obtaining of funding or logistic support, and critically revised the manuscript. All authors have read the manuscript and approved this submission.
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Quelhas, P.M., Trovão, M., Silva, J.T. et al. Industrial production of Phaeodactylum tricornutum for CO2 mitigation: biomass productivity and photosynthetic efficiency using photobioreactors of different volumes. J Appl Phycol 31, 2187–2196 (2019). https://doi.org/10.1007/s10811-019-1750-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-019-1750-0