Effects of temperature, irradiance, and pH on the growth and biochemical composition of Haslea ostrearia batch-cultured in an airlift plan-photobioreactor.

Airlift plan-photobioreactor Biochemical composition Growth conditions Haslea ostrearia

Journal

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

Informations de publication

Date de publication:
Aug 2022
Historique:
received: 14 04 2021
accepted: 28 06 2022
revised: 26 05 2022
pubmed: 18 7 2022
medline: 30 7 2022
entrez: 17 7 2022
Statut: ppublish

Résumé

Haslea ostrearia is a pennate diatom that produces marennine, a water-soluble blue pigment responsible for the greening phenomenon and the increase of organoleptic quality of oysters. Apart from the oyster industry, there is a growing interest in the mass cultivation of this diatom due to the biological activities of marennine. To gain knowledge about the feasibility to upscale production of this diatom, in particular, in the context of global warming, the effects of different temperatures (20, 25, and 30 °C), irradiances (100, 200, and 300 μmol photons m

Identifiants

pubmed: 35842874
doi: 10.1007/s00253-022-12055-1
pii: 10.1007/s00253-022-12055-1
doi:

Substances chimiques

Fatty Acids 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5233-5247

Subventions

Organisme : Horizon 2020 Research and Innovation Program GHaNA (The Genus Haslea, New marine resources for blue biotechnology and Aquaculture)
ID : No 734708/GHANA/H2020-MSCA-RISE- 2016

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Andersen RA (2005) Algal culturing techniques. Elsevier
Barbarino E, Lourenço SO (2005) An evaluation of methods for extraction and quantification of protein from marine macro-and microalgae. J Appl Phycol 17(5):447–460
doi: 10.1007/s10811-005-1641-4
Barbosa MJ, Hoogakker J, Wijffels RH (2003) Optimisation of cultivation parameters in photobioreactors for microalgae cultivation using the A-stat technique. Biomol Eng 20(4–6):115–123
pubmed: 12919788 doi: 10.1016/S1389-0344(03)00033-9
Barra L, Chandrasekaran R, Corato F, Brunet C (2014) The challenge of ecophysiological biodiversity for biotechnological applications of marine microalgae. Mar Drugs 12(3):1641–1675
pubmed: 24663117 pmcid: 3967230 doi: 10.3390/md12031641
Benavente-Valdés JR, Aguilar C, Contreras-Esquivel JC, Méndez-Zavala A, Montañez J (2016) Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10:117–125
doi: 10.1016/j.btre.2016.04.001
Blanchemain A, Grizeau D (1996) Eicosapentaenoic acid content of Skeletonema costatum as a function of growth and irradiance; relation with chlorophyll a content and photosynthetic capacity. J Exp Mar Biol Ecol 196(1–2):177–188
doi: 10.1016/0022-0981(95)00129-8
Bouzidi N, Zili F, García-Maroto F, Alonso DL, Ouada HB (2020) Impact of temperature and growth phases on lipid composition and fatty acid profile of a thermophilic Bacillariophyta strain related to the genus Halamphora from north-eastern Tunisia. J Mar Biol Assoc UK 100(4):529–536
doi: 10.1017/S002531542000048X
Chen CY, Durbin EG (1994) Effects of pH on the growth and carbon uptake of marine phytoplankton. Mar Ecol-Prog Ser 109:83–83
doi: 10.3354/meps109083
Chentir I, Doumandji A, Ammar J, Zili F, Jridi M, Markou G, Ouada HB (2018) Induced change in Arthrospira sp.(Spirulina) intracellular and extracellular metabolites using multifactor stress combination approach. J Appl Phycol 30(3):1563–1574
doi: 10.1007/s10811-017-1348-3
Davidovich O, Davidovich N, Mouget J-L (2018) The effect of temperature on vegetative growth and sexual reproduction of two diatoms from the genus Haslea Simonsen. Russ J Mar Biol 44(1):8–13
doi: 10.1134/S1063074018010030
de Castro AS, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246(1–4):405–412
Falaise C, James A, Travers M-A, Zanella M, Badawi M, Mouget J-L (2019) Complex relationships between the blue pigment marennine and marine bacteria of the genus Vibrio. Mar Drugs 17(3):160
pmcid: 6471480 doi: 10.3390/md17030160
Folch J, Lees M, Stanley GS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509
pubmed: 13428781 doi: 10.1016/S0021-9258(18)64849-5
Gastineau R, Pouvreau J-B, Hellio C, Morançais M, Jl F, Gaudin P, Bourgougnon N, Mouget J-L (2012) Biological activities of purified marennine, the blue pigment responsible for the greening of oysters. J Agric Food Chem 60(14):3599–3605
pubmed: 22423636 doi: 10.1021/jf205004x
Gastineau R, Turcotte F, Pouvreau J-B, Morançais M, Fleurence J, Windarto E, Prasetiya FS, Arsad S, Jaouen P, Babin M (2014) Marennine, promising blue pigments from a widespread Haslea diatom species complex. Mar Drugs 12(6):3161–3189
pubmed: 24879542 pmcid: 4071570 doi: 10.3390/md12063161
George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus–a potential strain for bio-fuel production. Bioresour Technol 171:367–374
pubmed: 25218209 doi: 10.1016/j.biortech.2014.08.086
Groth-Nard C (1994) Les lipides des diatomees: exemple d'haslea ostrearia (simonsen), responsable du verdissement des huitres
Guihéneuf F, Mimouni V, Ulmann L, Tremblin G (2008) Environmental factors affecting growth and omega 3 fatty acid composition in Skeletonema costatum. The influences of irradiance and carbon source: Communication presented at the 25ème Congrès Annuel de l’Association des Diatomistes de Langue Francaise (ADLaF), Caen, 25–28 September 2006. Diatom Res 23(1):93–103
doi: 10.1080/0269249X.2008.9705739
Guihéneuf F, Stengel DB (2017) Interactive effects of light and temperature on pigments and n-3 LC-PUFA-enriched oil accumulation in batch-cultivated Pavlova lutheri using high-bicarbonate supply. Algal Res 23:113–125
doi: 10.1016/j.algal.2017.02.002
Guillard RRL (1973) Division rates. In: Stein JR (ed) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, London, pp 289–311
Janssen M, Bathke L, Marquardt J, Krumbein WE, Rhiel E (2001) Changes in the photosynthetic apparatus of diatoms in response to low and high light intensities. Int Microbiol 4(1):27–33
pubmed: 11770817 doi: 10.1007/s101230100005
Jeffrey SW, Humphrey G (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167(2):191–194
doi: 10.1016/S0015-3796(17)30778-3
Jiang H, Gao K (2004) Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (bacillariophyceae) 1. J Phycol 40(4):651–654
doi: 10.1111/j.1529-8817.2004.03112.x
Khalil ZI, Asker MM, El-Sayed S, Kobbia IA (2010) Effect of pH on growth and biochemical responses of Dunaliella bardawil and Chlorella ellipsoidea. World J Microbiol Biotechnol 26(7):1225–1231
pubmed: 24026927 doi: 10.1007/s11274-009-0292-z
Lebeau T, Gaudin P, Junter G-A, Mignot L, Robert J-M (2000) Continuous marennin production by agar-entrapped Haslea ostrearia using a tubular photobioreactor with internal illumination. Appl Microbiol Biotechnol 54(5):634–640
pubmed: 11131387 doi: 10.1007/s002530000380
Lebeau T, Gaudin P, Moan R, Robert J-M (2002) A new photobioreactor for continuous marennin production with a marine diatom: influence of the light intensity and the immobilised-cell matrix (alginate beads or agar layer). Appl Microbiol Biotechnol 59(2):153–159
pubmed: 12111140
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
pubmed: 14907713 doi: 10.1016/S0021-9258(19)52451-6
Nantes Lucchetti A (2014) Modélisation et conception d'un système de culture de microalgues. Paris, ENMP
Merchuk J, Gluz M (1999) Bioreactors, airlift reactors In: Flickinger, M C & Drew, S W (Eds) Encyclopedia of Bioprocess technology: Fermentation, Biocatalysis and Bioseparation John Wiley & Sons, Inc, 1–5
Moheimani NR, Borowitzka MA (2011) Increased CO2 and the effect of pH on growth and calcification of Pleurochrysis carterae and Emiliania huxleyi (Haptophyta) in semicontinuous cultures. Appl Microbiol Biotechnol 90(4):1399–1407
pubmed: 21369804 doi: 10.1007/s00253-011-3174-x
Mortensen SH, Børsheim KY, Rainuzzo J, Knutsen G (1988) Fatty acid and elemental composition of the marine diatom Chaetoceros gracilis Schütt. Effects of silicate deprivation, temperature and light intensity. J Exp Mar Biol Ecol 122(2):173–185
doi: 10.1016/0022-0981(88)90183-9
Mouget J-L, Rosa P, Tremblin G (2004) Acclimation of Haslea ostrearia to light of different spectral qualities–confirmation of chromatic adaptation in diatoms. J Photochem Photobiol b: Biol 75(1–2):1–11
doi: 10.1016/j.jphotobiol.2004.04.002
Mouget J-L, Rosa P, Vachoux C, Tremblin G (2005) Enhancement of marennine production by blue light in the diatom Haslea ostrearia. J Appl Phycol 17(5):437–445
doi: 10.1007/s10811-005-0561-7
Mouget J-L, Tremblin G, Morant-Manceau A, Morançais M, Robert J-M (1999) Long-term photoacclimation of Haslea ostrearia (Bacillariophyta): effect of irradiance on growth rates, pigment content and photosynthesis. Eur J Phycol 34(2):109–115
doi: 10.1080/09670269910001736162
Pouvreau J-B, Morançais M, Fleury F, Rosa P, Thion L, Cahingt B, Zal F, Fleurence J, Pondaven P (2006) Preliminary characterisation of the blue-green pigment “marennine” from the marine tychopelagic diatom Haslea ostrearia (Gaillon/Bory) Simonsen. J Appl Phycol 18(6):757–767
doi: 10.1007/s10811-006-9087-x
Prasetiya FS, Safitri I, Widowati I, Cognie B, Decottignies P, Gastineau R, Morançais M, Windarto E, Tremblay R, Mouget J-L (2016) Does allelopathy affect co-culturing Haslea ostrearia with other microalgae relevant to aquaculture? J Appl Phycol 28(4):2241–2254
doi: 10.1007/s10811-015-0779-y
Prelle LR, Graiff A, Gründling-Pfaff S, Sommer V, Kuriyama K, Karsten U (2019) Photosynthesis and respiration of Baltic Sea benthic diatoms to changing environmental conditions and growth responses of selected species as affected by an adjacent peatland (Hütelmoor) Frontiers in Microbiology 10:1500
Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Cultures and collections of algae proceedings of US-Japan Conference, Hakone, September 1966, Japan Society of Plant Physiology
Pruvost J, Van Vooren G, Cogne G, Legrand J (2009) Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Bioresour Technol 100(23):5988–5995
pubmed: 19560349 doi: 10.1016/j.biortech.2009.06.004
Pruvost J, Van Vooren G, Le Gouic B, Couzinet-Mossion A, Legrand J (2011) Systematic investigation of biomass and lipid productivity by microalgae in photobioreactors for biodiesel application. Bioresour Technol 102(1):150–158
pubmed: 20675127 doi: 10.1016/j.biortech.2010.06.153
Rech M (2004) Effets de l'éclairement visible et ultraviolet sur la croissance et la photosynthèse de microalgues: incidences sur l'écophysiologie du phytoplancton des claires ostréicoles. Le Mans
Rech M, Morant-Manceau A, Tremblin G (2008) Carbon fixation and carbonic anhydrase activity in Haslea ostrearia (Bacillariophyceae) in relation to growth irradiance. Photosynthetica 46(1):56–62
doi: 10.1007/s11099-008-0011-2
Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211(1–4):195–214
doi: 10.1016/S0044-8486(01)00875-4
Renaud SM, Zhou H, Parry DL, Thinh L-V, Woo K (1995) Effect of temperature on the growth, total lipid content and fatty acid composition of recently isolated tropical microalgae Isochrysis sp., Nitzschia closterium, Nitzschia paleacea, and commercial species Isochrysis sp.(clone T. ISO). J Appl Phycol 7(6):595–602
doi: 10.1007/BF00003948
Ritchie R (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(1):115–126
doi: 10.1007/s11099-008-0019-7
Robert J-M (1983) Fertilité des claires ostréicoles et verdissement: utilisation de l’azote par les diatomées dominantes. Nantes
Robert J-M, Morançais M, Pradier E, Mouget J-L, Tremblin G (2002) Extraction and quantitative analysis of the blue-green pigment “marennine” synthesized by the diatom Haslea ostrearia. J Appl Phycol 14(4):299–305
doi: 10.1023/A:1021184532581
Rossignol N, Jaouen P, Robert J-M, Quéméneur F (2000a) Production of exocellular pigment by the marine diatom Haslea ostrearia Simonsen in a photobioreactor equipped with immersed ultrafiltration membranes. Bioresour Technol 73(2):197–200
doi: 10.1016/S0960-8524(99)00171-6
Rossignol N, Lebeau T, Jaouen P, Robert J (2000b) Comparison of two membrane–photobioreactors, with free or immobilized cells, for the production of pigments by a marine diatom. Bioprocess Eng 23(5):495–501
doi: 10.1007/s004499900186
Rousch JM, Bingham SE, Sommerfeld MR (2003) Changes in fatty acid profiles of thermo-intolerant and thermo-tolerant marine diatoms during temperature stress. J Exp Mar Biol Ecol 295(2):145–156
doi: 10.1016/S0022-0981(03)00293-4
Scholz B (2014) Purification and culture characteristics of 36 benthic marine diatoms isolated from the Solthörn tidal flat (Southern North Sea). J Phycol 50(4):685–697
pubmed: 26988452 doi: 10.1111/jpy.12193
Simonsen R (1974) The diatom plankton of the Indian Ocean Expedition of R/V Meteor 1964–5, “Meteor” Forschungsergebnisse. Reihe d: Biologie 19:1–107
Spilling K, Brynjólfsdóttir Á, Enss D, Rischer H, Svavarsson HG (2013) The effect of high pH on structural lipids in diatoms. J Appl Phycol 25(5):1435–1439
doi: 10.1007/s10811-012-9971-5
Stonik V, Stonik I (2015) Low-molecular-weight metabolites from diatoms: structures, biological roles and biosynthesis. Mar Drugs 13(6):3672–3709
pubmed: 26065408 pmcid: 4483651 doi: 10.3390/md13063672
Strickland JDH, Parsons TR (1972) Spectrophotometric determination of chlorophylls and total carotenoids. In: Stevenson JC (ed) A practical handbook of seawater analysis, 2nd edn. Fisheries research board, Ottawa CANADA, pp 189–190
Sukenik A, Zmora O, Carmeli Y (1993) Biochemical quality of marine unicellular algae with special emphasis on lipid composition II Nannochloropsis sp. Aquaculture 117(3–4):313–326
doi: 10.1016/0044-8486(93)90328-V
Sun H, Zhao W, Mao X, Li Y, Wu T, Chen F (2018) High-value biomass from microalgae production platforms: strategies and progress based on carbon metabolism and energy conversion. Biotechnol Biofuels 11(1):227
pubmed: 30151055 pmcid: 6100726 doi: 10.1186/s13068-018-1225-6
Suzuki Y, Takahashi M (1995) Growth responses of several diatom species isolated from various environments to temperature. J Phycol 31(6):880–888
doi: 10.1111/j.0022-3646.1995.00880.x
Taraldsvik M, Myklestad SM (2000) The effect of pH on growth rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. Eur J Phycol 35(2):189–194
doi: 10.1080/09670260010001735781
Thompson PA, Mx Guo, Harrison PJ, Whyte JN (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28(4):488–497
doi: 10.1111/j.0022-3646.1992.00488.x
Thompson PA, Harrison PJ, Whyte JN (1990) Influence of irradiance on the fatty acid composition of phytoplankton. J Phycol 26(2):278–288
doi: 10.1111/j.0022-3646.1990.00278.x
Turcotte F, Mouget J-L, Genard B, Lemarchand K, Deschênes J-S, Tremblay R (2016) Prophylactic effect of Haslea ostrearia culture supernatant containing the pigment marennine to stabilize bivalve hatchery production. Aquat Living Resour 29(4):401
doi: 10.1051/alr/2016032
Turpin V, Robert JM, Goulletquer P, Massé G, Rosa P (2001) Oyster greening by outdoor mass culture of the diatom Haslea ostrearia Simonsen in enriched seawater. Aquacult Res 32(10):801–809
doi: 10.1046/j.1365-2109.2001.00615.x
Van Wagenen J, Miller TW, Hobbs S, Hook P, Crowe B, Huesemann M (2012) Effects of light and temperature on fatty acid production in Nannochloropsis salina. Energies 5(3):731–740
doi: 10.3390/en5030731
Vandanjon L, Jaouen P, Rossignol N, Quéméneur F, Robert J-M (1999) Concentration and desalting by membrane processes of a natural pigment produced by the marine diatom Haslea ostrearia Simonsen Progress in Industrial Microbiology. vol 35. Elsevier, pp 393–402
Vega-Catalan FJ (1990) A method for conforming the pH dependence of the Michaelis parameters of nonallosteric enzymes to four kinetic schemes. Comput Biomed Res 23(5):447–454
pubmed: 2225789 doi: 10.1016/0010-4809(90)90033-9
Wacker A, Piepho M, Harwood JL, Guschina IA, Arts MT (2016) Light-induced changes in fatty acid profiles of specific lipid classes in several freshwater phytoplankton species. Front Plant Sci 7:264
pubmed: 27014290 pmcid: 4792871 doi: 10.3389/fpls.2016.00264
Wah NB, Ahmad ALB, Chieh DCJ, Hwai ATS (2015) Changes in lipid profiles of a tropical benthic diatom in different cultivation temperature. Asian J Appl Sci Eng 4(2):91–101
Xuan RN, Mouget J, Turpin V, Jaouen P, Pruvost J (2021) Optimization of the growth and marennine production by the diatom Haslea ostrearia in photobioreactor. Algal Res 55:102251
doi: 10.1016/j.algal.2021.102251
Xuan RN, Safitri I, Mouget J, Pruvost J, Turpin V, Jaouen P (2020) Design of an artificial culture medium to optimize Haslea ostrearia biomass and marennine production. Algal Res 45:101653
doi: 10.1016/j.algal.2019.101653
Yongmanitchai W, Ward OP (1991) Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Appl Environ Microbiol 57(2):419–425
pubmed: 2014989 pmcid: 182726 doi: 10.1128/aem.57.2.419-425.1991
Young JN, Goldman JA, Kranz SA, Tortell PD, Morel FM (2015) Slow carboxylation of Rubisco constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol 205(1):172–181
pubmed: 25283055 doi: 10.1111/nph.13021
Zhang D, Wen S, Wu X, Cong W (2018) Effect of culture condition on the growth, biochemical composition and EPA production of alkaliphilic Nitzschia plea isolated in the Southeast of China. Bioprocess Biosystems Eng 41(6):831–839
doi: 10.1007/s00449-018-1917-0

Auteurs

Rebiha Adjout (R)

Laboratoire d'Aquaculture Et de Bioremédiation (AQUABIOR), Université Oran, 1 Ahmed Ben Bella, B.P 1524 El M'Naouer, 31000, Oran, Algérie. adjout.rebiha@edu.univ-oran1.dz.

Jean-Luc Mouget (JL)

Mer Molécules Santé (MMS EA 2160), Le Mans Université, Ave O. Messiaen, 72085, Le Mans, France.

Jeremy Pruvost (J)

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

Imene Chentir (I)

Laboratoire d'Alimentation, Transformation, Contrôle et Valorisation des Agroressources, Ecole Supérieure Des Sciences de L'Aliment Et Des Industries Agroalimentaires, Ave Ahmed Hamidouche, Route Beaulieu El Harrach, 16200, Algérie.

Celine Loiseau (C)

Mer Molécules Santé (MMS EA 2160), Département Génie Biologique, Le Mans Université, Institut Universitaire de Technologie de Laval, 52 rue des Docteurs Calmette et Guérin, BP 2045, 53020, Laval, France.

Mohammed Bey Baba Hamed (MB)

Laboratoire d'Aquaculture Et de Bioremédiation (AQUABIOR), Université Oran, 1 Ahmed Ben Bella, B.P 1524 El M'Naouer, 31000, Oran, Algérie.

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