Investigation of the photosynthetic response of Chlorella vulgaris to light changes in a torus-shape photobioreactor.

Light response Microalgae Photoacclimation Photoprotection Photosynthesis

Journal

Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612

Informations de publication

Date de publication:
Dec 2021
Historique:
received: 22 04 2021
accepted: 05 10 2021
revised: 14 09 2021
pubmed: 2 11 2021
medline: 17 11 2021
entrez: 1 11 2021
Statut: ppublish

Résumé

An efficient use of light is essential to achieve good performances in microalgae cultivation systems. This can be challenging particularly under solar conditions where light is highly dynamic (e.g., day/night cycles, rapid changes in wind and weather conditions). Microalgae display different mechanisms to optimize light use efficiency. In the short term, when high light is encountered, several processes of photoprotection can be involved to avoid cell damages (e.g., xanthophyll cycle). In the long term, when cells are exposed to a different light intensity, pigment content changes, i.e., photoacclimation. The purpose of this study is to investigate the photosynthetic response of Chlorella vulgaris cultures grown in closed lab-scale, torus-shape photobioreactor under well-controlled light conditions, namely, constant and dynamic light transitions. Experiments were conducted in continuous mode with detailed characterization of the light attenuation conditions for each condition, as represented by the mean rate of photon absorption (MRPA), so as to characterize the time responses of the photosynthetic cells toward light changes. This enables to observe short-term and long-term responses with their own characteristic times. The mechanisms involved were found to be different between increasing and decreasing light transitions. Furthermore the MRPA was found a valuable parameter to relate the effect of light to biological responses (i.e., pigment changes) under constant light and dynamic light conditions.Key points• MRPA proved valuable to relate C. vulgaris responses to light changes.• A linear evolution was found between pigment content and MRPA in continuous light.• A rising PFD step induced fast protection and acclimation mechanisms.

Identifiants

pubmed: 34724082
doi: 10.1007/s00253-021-11636-w
pii: 10.1007/s00253-021-11636-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8689-8701

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Acien G, Fernandez-Sevilla JM, Molina-Grima E (2013) Photobioreactors for the production of microalgae. Reviews in Environ Sci and Bio/Technol 12. https://doi.org/10.1007/s11157-012-9307-6
Allen J, Forsberg J (2001) Allen, J. F. & Forsberg, J. Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326. https://doi.org/10.1016/S1360-1385(01)02010-6
doi: 10.1016/S1360-1385(01)02010-6 pubmed: 11435171
Andersen RA (2005) Algal culturing techniques - 1st edition. https://www.elsevier.com/books/algal-culturing-techniques/andersen/978-0-12-088426-1 . Accessed 14 Feb 2019
Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355:1419–1431
doi: 10.1098/rstb.2000.0703
Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci U S A 79:4352–4356
doi: 10.1073/pnas.79.14.4352
Bonnanfant M, Jesus B, Pruvost J, Mouget J-L, Campbell DA (2019) Photosynthetic electron transport transients in Chlorella vulgaris under fluctuating light. Algal Res 44:101713. https://doi.org/10.1016/j.algal.2019.101713
doi: 10.1016/j.algal.2019.101713
Brunet C, Johnsen G, Lavaud J, Roy S (2011) Pigments and photoacclimation processes. In: Phytoplankton pigments: characterization, chemotaxonomy and applications in oceanography
Crofts AR, Wraight CA (1983) The electrochemical domain of photosynthesis. Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics 726:149–185. https://doi.org/10.1016/0304-4173(83)90004-6
Degrenne B, Pruvost J, Christophe G, Cornet JF, Cogne G, Legrand J (2010) Investigation of the combined effects of acetate and photobioreactor illuminated fraction in the induction of anoxia for hydrogen production by Chlamydomonas reinhardtii. Int J Hydrogen Energy 35:10741–10749. https://doi.org/10.1016/j.ijhydene.2010.02.067
doi: 10.1016/j.ijhydene.2010.02.067
Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Microb Ecolog 56:163–176. https://doi.org/10.3354/ame01345
doi: 10.3354/ame01345
Goldschmidt-Clermont M, Bassi R (2015) Sharing light between two photosystems: mechanism of state transitions. Curr Opin Plant Biol 25:71–78. https://doi.org/10.1016/j.pbi.2015.04.009
doi: 10.1016/j.pbi.2015.04.009 pubmed: 26002067
Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004
doi: 10.1016/j.jplph.2014.03.004 pubmed: 24854581
Heinz Walz GmbH (2001) Instruction manual for PAM-CONTROL
Ifrim GA, Titica M, Cogne G, Boillereaux L, Legrand J, Caraman S (2014) Dynamic pH model for autotrophic growth of microalgae in photobioreactor: a tool for monitoring and control purposes. AIChE J 60:585–599. https://doi.org/10.1002/aic.14290
doi: 10.1002/aic.14290
Kandilian R, Pruvost J, Artu A, Lemasson C, Legrand J, Pilon L (2016) Comparison of experimentally and theoretically determined radiation characteristics of photosynthetic microorganisms. J Quant Spectrosc Radiat Transfer 175:30–45. https://doi.org/10.1016/j.jqsrt.2016.01.031
doi: 10.1016/j.jqsrt.2016.01.031
Kargul J, Barber J (2008) Photosynthetic acclimation: structural reorganisation of light harvesting antenna – role of redox-dependent phosphorylation of major and minor chlorophyll a/b binding proteins. FEBS J 275:1056–1068. https://doi.org/10.1111/j.1742-4658.2008.06262.x
doi: 10.1111/j.1742-4658.2008.06262.x pubmed: 18318833
Kazbar A, Cogne G, Urbain B, Marec H, Le-Gouic B, Tallec J, Takache H, Ismail A, Pruvost J (2019a) Effect of dissolved oxygen concentration on microalgal culture in photobioreactors. Algal Research 101. https://doi.org/10.1016/j.algal.2019.101432
Kazbar A, Marec H, Takache H, Ismail A, Pruvost J (2019b) Effect of design dark fraction on the loss of biomass productivities in photobioreactors. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-019-02217-3
doi: 10.1007/s00449-019-02217-3 pubmed: 31541313
Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application Notes 1:27–35
Kok B (1956) On the inhibition of photosynthesis by intense light. Biochimica Biophysica Acta 21:234–244. https://doi.org/10.1016/0006-3002(56)90003-8
doi: 10.1016/0006-3002(56)90003-8
Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665. https://doi.org/10.4319/lo.1993.38.8.1646
doi: 10.4319/lo.1993.38.8.1646
Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Func Plant Sci Biotech 1:267–287
Le Borgne F (2011) Développement d’un photobioréacteur solaire intensifié en vue de la production à grande échelle de biomasse microalgale. Thesis, Nantes
Le Gouic B, Marec H, Pruvost J, Cornet J-F (2021) Investigation of growth limitation by CO
Malapascua JRF, Jerez CG, Sergejevová M, Figueroa FL, Masojídek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Bio 22:123–140. https://doi.org/10.3354/ab00597
doi: 10.3354/ab00597
Malapascua JRF, Ranglova K, Masojidek J (2018) Photosynthesis and growth kinetics of Chlorella vulgaris R-117 cultured in an internally LED‑illuminated photobioreactor. Photosynthetica. https://doi.org/10.32615/ps.2019.031
Muller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
doi: 10.1104/pp.125.4.1558
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16. https://doi.org/10.1093/aob/mcq059
doi: 10.1093/aob/mcq059 pubmed: 20338950 pmcid: 2889791
Ortega-Villasante C, Burén S, Barón-Sola Á, Martínez F, Hernández LE (2016) In vivo ROS and redox potential fluorescent detection in plants: present approaches and future perspectives. Methods 109:92–104. https://doi.org/10.1016/j.ymeth.2016.07.009
doi: 10.1016/j.ymeth.2016.07.009 pubmed: 27424086
Peltier G, Cournac L (2002) Chlororespiration Annual Rev Plant Bio 53:523–550. https://doi.org/10.1146/annurev.arplant.53.100301.135242
doi: 10.1146/annurev.arplant.53.100301.135242
Perkins RG, Kromkamp JC, Serôdio J, Lavaud J, Jesus B, Mouget J-L, Lefebvre S, Forster RM (2010) The application of variable chlorophyll fluorescenceto microphytobenthic biofilms. In: Chlorophyll a fluorescence in aquatic sciences: methods and applications
Pottier L, Pruvost J, Deremetz J, Cornet J-F, Legrand J, Dussap CG (2005) A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torus photobioreactor. Biotechnol Bioeng 91:569–582. https://doi.org/10.1002/bit.20475
doi: 10.1002/bit.20475 pubmed: 16025533
Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395–410. https://doi.org/10.1007/BF00029472
doi: 10.1007/BF00029472 pubmed: 24271480
Pruvost J, Cornet JF (2012) Knowledge models for engineering and optimization of photobioreactors. In: C.Walter CPa (ed) Microalgal biotechnology. De Gruyter GmbH & Co. KG, pp 181–224
Pruvost J, Cornet JF, Le Borgne F, Goetz V, Legrand J (2015) Theoretical investigation of microalgae culture in the light changing conditions of solar photobioreactor production and comparison with cyanobacteria. Algal Res 10:87–99. https://doi.org/10.1016/j.algal.2015.04.005
doi: 10.1016/j.algal.2015.04.005
Pruvost J, Cornet J-F, Legrand J (2008) Hydrodynamics influence on light conversion in photobioreactors: an energetically consistent analysis. Chem Eng Sci 63:3679–3694. https://doi.org/10.1016/j.ces.2008.04.026
doi: 10.1016/j.ces.2008.04.026
Pruvost J, Le Borgne A, Artu A, Legrand J (2017) Development of a thin-film solar photobioreactor with high biomass volumetric productivity (AlgoFilm) based on process intensification principles. Algal Research 21:120–137. https://doi.org/10.1016/j.algal.2016.10.012
doi: 10.1016/j.algal.2016.10.012
Pruvost J, Le Borgne F, Cornet J-F, Legrand J (2016) Chapter five - industrial photobioreactors and scale-up concepts. In: Legrand J (ed) Adv Chem Eng. Academic Press, pp 257–310
Pruvost J, Pottier L, Legrand J (2006) Numerical investigation of hydrodynamic and mixing conditions in a torus photobioreactor. Chem Eng Sci 61:4476–4489. https://doi.org/10.1016/j.ces.2006.02.027
doi: 10.1016/j.ces.2006.02.027
Richmond A (2013) Biological principles of mass cultivation of photoautotrophic microalgae. In: Handbook of microalgal culture. John Wiley & Sons, Ltd, pp 169–204
Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126. https://doi.org/10.1007/s11099-008-0019-7
doi: 10.1007/s11099-008-0019-7
Sharma R (2012) Effects of culture conditions on growth and biochemical profile of Chlorella vulgaris. J Plant Pathol Microbiol 03. https://doi.org/10.4172/2157-7471.1000131
Souliès A, Legrand J, Marec H, Pruvost J, Castelain C, Burghelea T, Cornet J-F (2016) Investigation and modeling of the effects of light spectrum and incident angle on the growth of Chlorella vulgaris in photobioreactors. Biotechnol Prog 32:247–261. https://doi.org/10.1002/btpr.2244
doi: 10.1002/btpr.2244 pubmed: 26871260
Strickland JDH, Parsons TR (1968) A practical handbook of seawater analysis. Fisheries Research Board of Canada
Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardii. Proc Natl Acad Sci U S A 46:83–91
doi: 10.1073/pnas.46.1.83
Takache H, Pruvost J, Cornet J-F (2012) Kinetic modeling of the photosynthetic growth of Chlamydomonas reinhardtii in a photobioreactor. Biotechnol Prog 28:681–692. https://doi.org/10.1002/btpr.1545
doi: 10.1002/btpr.1545 pubmed: 22467331
Takache H, Pruvost J, Marec H (2015) Investigation of light/dark cycles effects on the photosynthetic growth of Chlamydomonas reinhardtii in conditions representative of photobioreactor cultivation. Algal Res 8:192–204. https://doi.org/10.1016/j.algal.2015.02.009
doi: 10.1016/j.algal.2015.02.009
Titica M, Kazbar A, Marec H, Pruvost J, Ifrim george, barbu marian, Caraman S (2018) Simultaneous control of pH and dissolved oxygen in closed photobioreactor. In: 2018 22nd international conference on system theory, control and computing (ICSTCC). IEEE, Sinaia, France, pp 372–378

Auteurs

M Bonnanfant (M)

GEPEA, UMR 6144, Oniris, CNRS, Université de Nantes, 44600, Saint-Nazaire, France.
Mer-Molécules-Santé (MMS), EA 2160, Le Mans Université, Le Mans Cedex 9, France.

H Marec (H)

GEPEA, UMR 6144, Oniris, CNRS, Université de Nantes, 44600, Saint-Nazaire, France.

B Jesus (B)

Mer-Molécules-Santé (MMS), EA2160, Faculté Des Sciences, Université de Nantes, Nantes, France.

J-L Mouget (JL)

Mer-Molécules-Santé (MMS), EA 2160, Le Mans Université, Le Mans Cedex 9, France.

J Pruvost (J)

GEPEA, UMR 6144, Oniris, CNRS, Université de Nantes, 44600, Saint-Nazaire, France. jeremy.pruvost@univ-nantes.fr.

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