[en] Achieving enhanced lipid yield without compromising biomass is a central challenge for sustainable algal biofuel production. While temperature, nutrients, and light can induce lipid accumulation, they often reduce overall fitness, offsetting net gains. By contrast, hydrodynamic cues remain underexplored, particularly in the context of motile algae and their physiological response in terms of fitness and lipid production. Here, we investigate
Heterosigma akashiwo
, a well-known motile phytoplankton species, exposed to controlled hydrodynamic cues at two physiological stages: immediately after inoculation (lag phase) and during the mid-exponential growth phase. We quantify intracellular lipid accumulation, growth kinetics, and photophysiology, and compare these parameters between two different strains of
H. akashiwo
. Early induction of hydrodynamic cues (during the lag phase) increased average cytoplasmic lipid accumulation by nearly 300% at the single-cell level, without adverse effects on fitness and biomass production. Growth rate accelerated while photophysiological performance was preserved. In contrast, delayed induction (exponential phase) yielded only marginal lipid enhancement and reduced biomass and photosynthetic efficiency. At the strain level, these trends were consistent, while we note strain-specific differences in the extent of the response. These results identify the onset timing of hydrodynamic cues as a tunable parameter to enhance lipogenesis while preserving physiological fitness, suggesting a simple and potentially scalable route to improve lipid production using motile microalgae.
KAKAVAND, Narges ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Physics and Materials Science > Team Anupam SENGUPTA
SENGUPTA, Anupam ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Physics and Materials Science (DPHYMS)
External co-authors :
no
Language :
English
Title :
Tuning lipid accumulation and fitness of motile algae via hydrodynamic cues
FNR11572821 - MBRACE - Biophysics Of Microbial Adaptation To Fluctuations In The Environment, 2017 (15/05/2018-14/11/2024) - Anupam Sengupta FNR13719464 - TOPOFLUME - Topological Fluid Mechanics: Decoding Emergent Dynamics In Anisotropic Fluids And Living Systems, 2019 (01/09/2020-31/08/2023) - Anupam Sengupta FNR14063202 - ACTIVE - Active Phenomena Across Scales In Biological Systems, 2020 (01/11/2020-30/04/2027) - Massimiliano Esposito
Université Du Luxembourg FNR - Fonds National de la Recherche
Funding text :
The authors declare that financial support was received for the research and/or publication of this article. This work was supported by the Luxembourg National Research Fund (FNR) through the PRIDE Doctoral Training Unit ACTIVE (PRIDE19/14063202/ACTIVE); the FNR ATTRACT Investigator Grant A17/MS/11572821/MBRACE (to AS); the FNR CORE Grant C19/MS/13719464/TOPOFLUME/Sengupta (to AS); and the Institute for Advanced Studies, University of Luxembourg, AUDACITY Grant IAS-20/CAMEOS. Additional support was provided by the University of Luxembourg.
Abu-Ghosh S. Fixler D. Dubinsky Z. Iluz D. (2016). Flashing light in microalgae biotechnology. Bioresour. Technology 203, 357–363. 10.1016/j.biortech.2015.12.05726747205
Allaf M. M. Trick C. G. (2024). Influence of multi‐stressor combinations of pCO2, temperature, and salinity on the toxicity of heterosigma Akashiwo (raphidophyceae), a fish‐killing flagellate. J. Phycol. 60, 1001–1020. 10.1111/jpy.1348138995628
Atikij T. Syaputri Y. Iwahashi H. Praneenararat T. Sirisattha S. Kageyama H. et al. (2019). Enhanced lipid production and molecular dynamics under salinity stress in green microalga Chlamydomonas reinhardtii (137c). Mar. Drugs 17, 484. 10.3390/md1708048431434347
Bianco C. M. Stewart J. J. Miller K. R. Fitzgerald C. Coyne K. J. (2016). Light intensity impacts the production of biofuel intermediates in heterosigma akashiwo growing on simulated flue gas containing carbon dioxide and nitric oxide. Bioresour. Technology 219, 246–251. 10.1016/j.biortech.2016.07.11927494106
Bigelow Laboratory for Ocean Sciences, National Center for Marine Algae and Microbiota (NCMA) (2025a). Heterosigma akashiwo ccmp3107 — strain page.
Bigelow Laboratory for Ocean Sciences, National Center for Marine Algae and Microbiota (NCMA) (2025b). Heterosigma akashiwo ccmp452 — strain page.
Brahma S. Nath B. Basumatary B. Das B. Saikia P. Patir K. et al. (2022). Biodiesel production from mixed oils: a sustainable approach towards industrial biofuel production. Chem. Eng. J. Adv. 10, 100284. 10.1016/j.ceja.2022.100284
Carrara F. Sengupta A. Behrendt L. Vardi A. Stocker R. (2021). Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence. Proc. Natl. Acad. Sci. U. S. A., 118. e2005944118. 10.1073/pnas.200594411833495340
Chen M. Chen Y. Zhang Q. (2021). A review of energy consumption in the acquisition of bio-feedstock for microalgae biofuel production. Sustainability 13, 8873. 10.3390/su13168873
Chiarini A. Quadrio M. (2021). The light/dark cycle of microalgae in a thin-layer photobioreactor. J. Appl. Phycol. 33, 183–195. 10.1007/s10811-020-02310-1
Chin G. J. W. L. Andrew A. R. Abdul-Sani E. R. Yong W. T. L. Misson M. Anton A. (2023). The effects of light intensity and nitrogen concentration to enhance lipid production in four tropical microalgae. Biocatal. Agric. Biotechnol. 48, 102660. 10.1016/j.bcab.2023.102660
Cho M. K. Shin H. S. (2016). Mechanotransduction-induced lipid production system with high robustness and controllability for microalgae. Sci. Rep. 6, 32860. 10.1038/srep3286027609701
Choi O. K. Lee J. W. (2022). Co2-triggered switchable solvent for lipid extraction from microalgal biomass. Sci. Total Environ. 819, 153084. 10.1016/j.scitotenv.2022.15308435038530
Chowdury K. H. Nahar N. Deb U. K. (2020). The growth factors involved in microalgae cultivation for biofuel production: a review. Comput. Water, Energy, Environ. Eng. 9, 185–215. 10.4236/cweee.2020.94012
de la Rosa A. M. González-Cardoso M. Á. del Carmen Cerón-García M. López-Rosales L. Gallardo-Rodríguez J. J. Seoane S. et al. (2023). Bioactives overproduction through operational strategies in the ichthyotoxic microalga heterosigma akashiwo culture. Toxins 15, 349. 10.3390/toxins1505034937235383
Ding N. Li C. Wang T. Guo M. Mohsin A. Zhang S. (2021). Evaluation of an enclosed air-lift photobioreactor (alpbr) for biomass and lipid biosynthesis of microalgal cells grown under fluid-induced shear stress. Biotechnol. & Biotechnol. Equip. 35, 139–149. 10.1080/13102818.2020.1856717
Fernández F. A. Camacho F. G. Chisti Y. (1999). “Photobioreactors: light regime, mass transfer, and scaleup,”Prog. Industrial Microbiology 35. 231–247. 10.1016/s0079-6352(99)80118-0
Fuentes-Grünewald C. Garcés E. Alacid E. Sampedro N. Rossi S. Camp J. (2012). Improvement of lipid production in the marine strains Alexandrium minutum and heterosigma akashiwo by utilizing abiotic parameters. J. Industrial Microbiol. Biotechnol. 39, 207–216. 10.1007/s10295-011-1016-621766212
Fuentes-Grünewald C. Garcés E. Alacid E. Rossi S. Camp J. (2013). Biomass and lipid production of dinoflagellates and raphidophytes in indoor and outdoor photobioreactors. Mar. Biotechnol. 15, 37–47. 10.1007/s10126-012-9450-722544375
Gallardo Rodríguez J. J. Sánchez Mirón A. García Camacho F. Cerón García M. C. Belarbi E. H. Chisti Y. et al. (2009). Causes of shear sensitivity of the toxic dinoflagellate protoceratium reticulatum. Biotechnol. Prog. 25, 792–800. 10.1002/btpr.16119399843
Gallardo-Rodríguez J. Astuya-Villalón A. Avello V. Llanos-Rivera A. Krock B. Agurto-Muñoz C. et al. (2020). Production of extracts with anaesthetic activity from the culture of heterosigma akashiwo in pilot-scale photobioreactors. Algal Res. 45, 101760. 10.1016/j.algal.2019.101760
Gao B. Hong J. Chen J. Zhang H. Hu R. Zhang C. (2023). The growth, lipid accumulation and adaptation mechanism in response to variation of temperature and nitrogen supply in psychrotrophic filamentous microalga xanthonema hormidioides (xanthophyceae). Biotechnol. Biofuels Bioprod. 16, 12. 10.1186/s13068-022-02249-036658609
García Camacho F. Contreras Gómez A. Mazzuca Sobczuk T. Molina Grima E. (2000). Effects of mechanical and hydrodynamic stress in agitated, sparged cultures of porphyridium cruentum. Process Biochem. 35, 1045–1050. 10.1016/s0032-9592(00)00138-2
Ghoshal A. Dhar J. Grossart H.-P. Sengupta A. (2024). Phytoplankton tune local ph to actively modulate circadian swimming behavior. biorXiv. 10.1101/2023.07.24.550407
Guillard R. R. L. (1975). “Culture of phytoplankton for feeding marine invertebrates,” in Culture of marine invertebrate animals, 29–60.
Harvey E. L. Menden-Deuer S. Rynearson T. A. (2015). Persistent intra-specific variation in genetic and behavioral traits in the raphidophyte, heterosigma akashiwo. Front. Microbiol. 6, 1277. 10.3389/fmicb.2015.0127726635748
Healey E. M. Flood S. Bock P. K. Fulweiler R. W. York J. K. Coyne K. J. (2023). Effects of nitrate and ammonium on assimilation of nitric oxide by heterosigma akashiwo. Photosynth. Res. 13, 621. 10.1038/s41598-023-27692-336635297
Hennige S. J. Coyne K. J. MacIntyre H. Liefer J. Warner M. E. (2013). The photobiology of heterosigma akashiwo. photoacclimation, diurnal periodicity, and its ability to rapidly exploit exposure to high light. J. Phycol. 49, 349–360. 10.1111/jpy.1204327008521
Hoang A. T. Sirohi R. Pandey A. Nizetic S. Lam S. S. Chen W.-H. et al. (2023). Biofuel production from microalgae: challenges and chances. Photochem. Rev. 22, 1089–1126. 10.1007/s11101-022-09819-y
Hosseinia A. Jazini M. Mahdieh M. Karimi K. (2020). Efficient superantioxidant and biofuel production from microalga haematococcus pluvialis via a biorefinery approach. Bioresour. Technol. 306, 123100. 10.1016/j.biortech.2020.12310032192960
Huang Q. Jiang F. Wang L. Yang C. (2017). Design of photobioreactors for mass cultivation of photosynthetic organisms. Engineering 3, 318–329. 10.1016/j.eng.2017.03.020
Jan H. A. Osman A. I. Al-Fatesh A. S. Almutairi G. Surina I. Al-Otaibi R. L. et al. (2023). Biodiesel production from sisymbrium irio as a potential novel biomass waste feedstock using homemade titania catalyst. Sci. Rep. 13, 11282. 10.1038/s41598-023-38408-y37438448
Jaouen P. Vandanjon L. Quéméneur F. (1999). The shear stress of microalgal cell suspensions (tetraselmis suecica) in tangential flow filtration systems: the role of pumps. Bioresour. Technology 68, 149–154. 10.1016/s0960-8524(98)00144-8
Ji N. Wang J. Huang W. Huang J. Cai Y. Sun S. et al. (2024). Transcriptome analysis of the harmful alga heterosigma akashiwo under a 24-hour light-dark cycle. Harmful Algae 133, 102601. 10.1016/j.hal.2024.10260138485440
Khan M. I. Shin J. H. Kim J. D. (2018). The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb. Cell Factories 17, 36. 10.1186/s12934-018-0879-x29506528
Kwok A. C. M. Chan W. S. Wong J. T. Y. (2023). Dinoflagellate amphiesmal dynamics: cell wall deposition with ecdysis and cellular growth. Mar. Drugs 21, 70. 10.3390/md2102007036827111
Lin Z. Chen B. Zhao L. (2020). Fluorescence-based bioassays with dose–response curve and relative potency in measuring algicidal virulence of bacillus sp. b1 exudates against heterosigma akashiwo. Sci. Total Environ. 724, 137691. 10.1016/j.scitotenv.2020.13769132247969
Lou Y. Liu Y. Li N. Liu Y. Wang G. Zhao X. et al. (2020). The influence of carbon limitation on growth of heterosigma akashiwo: a case study in fatty acids composition. Sci. Total Environ. 706, 135700. 10.1016/j.scitotenv.2019.13570031818562
Lum W. M. Lim H. C. Lau W. L. S. Law I. K. Teng S. T. Benico G. et al. (2022). Description of two new species chattonella tenuiplastida sp. Nov. and chattonella malayana sp. Nov. (raphidophyceae) from south China sea, with a report of wild fish mortality. Harmful Algae 118, 102322. 10.1016/j.hal.2022.10232236195418
Maltsev Y. Krivova Z. Maltseva S. Maltseva K. Gorshkova E. Kulikovskiy M. (2021a). Lipid accumulation by coelastrella multistriata (scenedesmaceae, sphaeropleales) during nitrogen and phosphorus starvation. Sci. Rep. 11, 19818. 10.1038/s41598-021-99376-934615938
Maltsev Y. Maltseva K. Kulikovskiy M. Maltseva S. (2021b). Influence of light conditions on microalgae growth and content of lipids, carotenoids, and fatty acid composition. Biology 10, 1060. 10.3390/biology1010106034681157
Margalef R. (1978). Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol. Acta 1 (1).
Martinez Carvajal G. D. Taidi B. Jarrahi M. (2024). Towards a low energy, stirless photobioreactor using photosynthetic motile microalgae. Algal Res. 77, 103350. 10.1016/j.algal.2023.103350
Mat Aron N. S. Khoo K. S. Chew K. W. Show P. L. Chen W.-H. Nguyen T. H. P. (2020). Sustainability of the four generations of biofuels – a review. Int. J. Energy Res. 2020, 1–17. 10.1002/er.5557
Mehdizadeh Allaf M. Trick C. G. (2023). Insights into cellular localization and environmental influences on the toxicity of marine fish-killing flagellate, heterosigma akashiwo. Int. J. Mol. Sci. 24, 10333. 10.3390/ijms24121033337373479
Min S. K. Yoon G. H. Joo J. H. Sim S. J. Shin H. S. (2014). Mechanosensitive physiology of chlamydomonas reinhardtii under direct membrane distortion. Sci. Reports 4, 4675. 10.1038/srep0467524728350
Morales-Sánchez D. Schulze P. S. C. Kiron V. Wijffels R. H. (2020). Temperature-dependent lipid accumulation in the polar marine microalga chlamydomonas malina rcc2488. Front. Plant Sci. 11, 619064. 10.3389/fpls.2020.61906433424911
Nagappan S. Devendran S. Tsai P.-C. Dahms H.-U. Ponnusamy V. K. (2019). Potential of two-stage cultivation in microalgae biofuel production. Fuel 252, 339–349. 10.1016/j.fuel.2019.04.138
Ngatcha A. D. P. Muhammad G. Lv Y. Xiong W. Zhao A. Xu J. et al. (2022). Microalgae biomass pre-treatment with deep eutectic solvent to optimize lipid isolation in biodiesel production. Biomass Convers. Biorefinery 12, S133–S143. 10.1007/s13399-021-02236-9
Nzayisenga J. C. Farge X. Groll S. L. Sellstedt A. (2020). Effects of light intensity on growth and lipid production in microalgae grown in wastewater. Biotechnol. Biofuels 13, 4. 10.1186/s13068-019-1646-x31921352
Pancha I. Chokshi K. Ghosh T. Paliwal C. Maurya R. Mishra S. (2015). Bicarbonate supplementation enhanced biofuel production potential as well as nutritional stress mitigation in the microalgae scenedesmus sp. ccnm 1077. Bioresour. Technol. 193, 315–323. 10.1016/j.biortech.2015.06.10726142998
Patel A. Gami B. Patel P. Patel B. (2023). Biodiesel production from microalgae dunaliella tertiolecta: a study on economic feasibility on large-scale cultivation systems. Biomass Convers. Biorefinery 13, 1071–1085. 10.1007/s13399-020-01191-1
Peng L. Fu D. Chu H. Wang Z. Qi H. (2020). Biofuel production from microalgae: a review. Environ. Chem. Lett. 18, 285–297. 10.1007/s10311-019-00939-0
Reyimu Z. Özçimen D. (2017). Batch cultivation of marine microalgae nannochloropsis oculata and tetraselmis suecica in treated municipal wastewater toward bioethanol production. J. Clean. Prod. 150, 40–46. 10.1016/j.jclepro.2017.02.189
Roháček K. (2002). Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40, 13–29. 10.1023/a:1020125719386
Saccardo A. Bezzo F. Sforza E. (2022). Microalgae growth in ultra-thin steady-state continuous photobioreactors: assessing self-shading effects. Front. Bioeng. Biotechnol. 10, 977429. 10.3389/fbioe.2022.97742936032730
Salama E.-S. Abou-Shanab R. A. Kim J. R. Lee S. Kim S.-H. Oh S.-E. et al. (2014). The effects of salinity on the growth and biochemical properties of chlamydomonas mexicana gu732420 cultivated in municipal wastewater. Environ. Technol. 35, 1491–1498. 10.1080/09593330.2013.87135024701948
Sánchez-Bayo A. López-Chicharro D. Morales V. Espada J. J. Puyol D. Martínez F. et al. (2020). Biodiesel and biogas production from isochrysis galbana using dry and wet lipid extraction: a biorefinery approach. Renew. Energy 146, 188–195. 10.1016/j.renene.2019.06.148
Saroussi S. Sanz-Luque E. Kim R. G. Grossman A. R. (2017). Nutrient scavenging and energy management: acclimation responses in nitrogen and sulfur deprived chlamydomonas. Curr. Opinion Plant Biol. 39, 114–122. 10.1016/j.pbi.2017.06.00228692856
Sato T. Yamada D. Hirabayashi S. (2010). Development of virtual photobioreactor for microalgae culture considering turbulent flow and flashing light effect. Energy Convers. Manag. 51, 1196–1201. 10.1016/j.enconman.2009.12.030
Schreiber U. Klughammer C. Kolbowski J. (2012). Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color pam chlorophyll fluorometer. Photosynth. Research 113, 127–144. 10.1007/s11120-012-9758-122729479
Sengupta A. (2023). Planktonic active matter. arXiv. 10.48550/arXiv.2301.09550
Sengupta A. Carrara F. Stocker R. (2017). Phytoplankton can actively diversify their migration strategy in response to turbulent cues. Nature 543, 555–558. 10.1038/nature2141528297706
Sengupta A. Dhar J. Danza F. Ghoshal A. Muller S. Kakavand N. (2022). Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton. Sci. Adv. 8, eabn6005. 10.1126/sciadv.abn600536332020
Sharma P. K. Saharia M. Srivastava R. Kumar S. Sahoo L. (2018). Tailoring microalgae for efficient biofuel production. Front. Mar. Sci. 5, 382. 10.3389/fmars.2018.00382
Shindell D. Smith C. J. (2019). Climate and air-quality benefits of a realistic phase-out of fossil fuels. Nature 573, 408–411. 10.1038/s41586-019-1554-z31534245
Stewart J. J. Bianco C. M. Miller K. R. Coyne K. J. (2015). The marine microalga, Heterosigma akashiwo, converts industrial waste gases into valuable biomass. Front. Energy Res. 3. 10.3389/fenrg.2015.00012
Teh K. Y. Loh S. H. Aziz A. Takahashi K. Mohd Effendy A. W. Cha T. S. (2021). Lipid accumulation patterns and role of different fatty acid types towards mitigating salinity fluctuations in chlorella vulgaris. Sci. Rep. 11, 1–15. 10.1038/s41598-020-79950-333432049
Thangaraj S. Sun J. (2023). Ocean warming and acidification affect the transitional c:n:p ratio and macromolecular accumulation in the harmful raphidophyte heterosigma akashiwo. Commun. Biol. 6, 151. 10.1038/s42003-023-04524-836747020
Thanigaivel S. Priya A. Dutta K. Rajendran S. Vasseghian Y. (2022). Engineering strategies and opportunities of next generation biofuel from microalgae: a perspective review on the potential bioenergy feedstock. Fuel 312, 122827. 10.1016/j.fuel.2021.122827
Thomas W. H. Gibson C. H. (1990). Effects of small-scale turbulence on microalgae. J. Appl. Phycol. 2, 71–77. 10.1007/bf02179771
Vertès A. A. Inui M. Yukawa H. (2006). Implementing biofuels on a global scale. Nat. Biotechnol. 24, 761–764. 10.1038/nbt0706-76116841054
Wang C. Lan C. Q. (2018). Effects of shear stress on microalgae–a review. Biotechnol. Adv. 36, 986–1002. 10.1016/j.biotechadv.2018.03.00129524464
Wang L. Yang T. Pan Y. Shi L. Jin Y. Huang X. (2023). The metabolism of reactive oxygen species and their effects on lipid biosynthesis of microalgae. Int. J. Mol. Sci. 24, 11041. 10.3390/ijms24131104137446218
Yang L. Chen J. Qin S. Zeng M. Jiang Y. Hu L. et al. (2018). Growth and lipid accumulation by different nutrients in the microalga chlamydomonas reinhardtii. Biotechnol. Biofuels 11, 40. 10.1186/s13068-018-1041-z29456627
Yang Y. Ge S. Pan Y. Qian W. Wang S. Zhang J. et al. (2023). Screening of microalgae species and evaluation of algal-lipid stimulation strategies for biodiesel production. Sci. Total Environ. 857, 159281. 10.1016/j.scitotenv.2022.15928136216060
You J. Mallery K. Mashek D. G. Sanders M. Hong J. Hondzo M. J. (2020). Microalgal swimming signatures and neutral lipids production across growth phases. Biotechnol. Bioeng. 117, 970–980. 10.1002/bit.2727131956983
Yuan Y. Zhao T. Gao W. Ye W. Chen Y. Sun D. et al. (2024). Reactive oxygen species derived from nadph oxidase as signaling molecules regulate fatty acids and astaxanthin accumulation in chromochloris zofingiensis. Front. Microbiol. 15, 1387222. 10.3389/fmicb.2024.138722238741732
Zhu Z. Sun J. Fa Y. Liu X. Lindblad P. (2022). Enhancing microalgal lipid accumulation for biofuel production. Front. Microbiol. 13, 1024441. 10.3389/fmicb.2022.102444136299727