A strategic approach to apply bacterial substances for increasing metabolite productions of Euglena gracilis in the bioreactor.
Euglena gracilis
Extracellular polymeric substances
Fed-batch fermentation
Harvesting
Paramylon
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
18
01
2021
accepted:
11
06
2021
revised:
20
05
2021
pubmed:
27
6
2021
medline:
21
7
2021
entrez:
26
6
2021
Statut:
ppublish
Résumé
Bacterial extracellular polymeric substances (EPS) are promising materials that have a role in enhancing growth, metabolite production, and harvesting efficiency. However, the validity of the EPS effectiveness in scale-up cultivation of microalgae is still unknown. Therefore, in order to verify whether the bacterial metabolites work in the scale-up fermentation of microalgae, we conducted a bioreactor fermentation following the addition of bacterial EPS derived from the marine bacterium, Pseudoalteromonas sp., to Euglena gracilis. Various culture strategies (i.e., batch, glucose fed-batch, and glucose and EPS fed-batch) were conducted to maximize metabolite production of E. gracilis in scale-up cultivation. Consequently, biomass and paramylon concentrations in the continuous glucose and EPS-treated culture were enhanced by 3.0-fold and 4.2-fold (36.1 ± 1.4 g L
Identifiants
pubmed: 34173846
doi: 10.1007/s00253-021-11412-w
pii: 10.1007/s00253-021-11412-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5395-5406Subventions
Organisme : Korea Institute of Marine Science and Technology
ID : 20170488
Organisme : National Research Foundation of Korea
ID : NRF-2019R1A2C2087449
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Alba MA, Sánchez RR, Pérez NJR, Navarrete JS, Paz RF, Montoya-Estrada A, Gómez JJH (2008) Comparative study of the antimutagenic properties of vitamins C and E against mutation induced by norfloxacin. BMC Pharmacol 8(1):2
pubmed: 18267022
pmcid: 2276188
doi: 10.1186/1471-2210-8-2
Barrow C, Shahidi F (2007) Marine nutraceuticals and functional foods. CRC Press
Buetow DE (1968) The biology of Euglena.
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306
pubmed: 17350212
doi: 10.1016/j.biotechadv.2007.02.001
pmcid: 17350212
Clarke A, Stone B (1960) Structure of the paramylon from Euglena gracilis. Biochim Biophys Acta 44:161–163
pubmed: 13693876
doi: 10.1016/0006-3002(60)91534-1
pmcid: 13693876
Decho AW (1990) Microbial exopolymer secretions in ocean environments: their role (s) in food webs and marine processes. Oceanogr Mar Biol Annu Rev 28(7):73–153
Decho AW, Gutierrez T (2017) Microbial extracellular polymeric substances (EPSs) in ocean systems. Front Microbiol 8:922
pubmed: 28603518
pmcid: 5445292
doi: 10.3389/fmicb.2017.00922
Fuggi A, Di Martino RV, Vona V, Rigano C (1981) Nitrate and ammonium assimilation in algal cell-suspensions and related pH variations in the external medium, monitored by electrodes. Plant Sci Lett 23(2):129–138
doi: 10.1016/0304-4211(81)90002-X
Furuhashi T, Ogawa T, Nakai R, Nakazawa M, Okazawa A, Padermschoke A, Nishio K, Hirai MY, Arita M, Ohta D (2015) Wax ester and lipophilic compound profiling of Euglena gracilis by gas chromatography-mass spectrometry: toward understanding of wax ester fermentation under hypoxia. Metabolomics 11(1):175–183
doi: 10.1007/s11306-014-0687-1
Gan H, Enomoto Y, Kabe T, Ishii D, Hikima T, Takata M, Iwata T (2017) Synthesis, properties and molecular conformation of paramylon ester derivatives. Polym Degrad Stab 145:142–149
doi: 10.1016/j.polymdegradstab.2017.05.011
Gissibl A, Sun A, Care A, Nevalainen H, Sunna A (2019) Bioproducts from Euglena gracilis: synthesis and applications. Front Bioengin Biotech 7:108
doi: 10.3389/fbioe.2019.00108
Green AG (2004) From alpha to omega—producing essential fatty acids in plants. Nat Biotechnol 22(6):680–682
pubmed: 15175687
doi: 10.1038/nbt0604-680
pmcid: 15175687
Grimm P, Risse JM, Cholewa D, Müller JM, Beshay U, Friehs K, Flaschel E (2015) Applicability of Euglena gracilis for biorefineries demonstrated by the production of α-tocopherol and paramylon followed by anaerobic digestion. J Biotechnol 215:72–79
pubmed: 25910451
doi: 10.1016/j.jbiotec.2015.04.004
pmcid: 25910451
Hasan MT, Sun A, Mirzaei M, Te’o J, Hobba G, Sunna A, Nevalainen H (2017) A comprehensive assessment of the biosynthetic pathways of ascorbate, α-tocopherol and free amino acids in Euglena gracilis var. saccharophila. Algal Res 27:140–151
doi: 10.1016/j.algal.2017.08.029
Hassler CS, Schoemann V, Nichols CM, Butler EC, Boyd PW (2011) Saccharides enhance iron bioavailability to Southern Ocean phytoplankton. Proc Natl Acad Sci 108(3):1076–1081
pubmed: 21169217
doi: 10.1073/pnas.1010963108
pmcid: 21169217
Inui H, Miyatake K, Nakano Y, Kitaoka S (1982) Wax ester fermentation in Euglena gracilis. FEBS Lett 150(1):89–93
doi: 10.1016/0014-5793(82)81310-0
Inui H, Ishikawa T, Tamoi M (2017) Wax ester fermentation and its application for biofuel production. In: Schwartzbach SD, Shigeoka S (eds) Euglena: biochemistry, cell and molecular biology. Springer International Publishing, Cham, pp 269–283
doi: 10.1007/978-3-319-54910-1_13
Inwongwan S, Kruger NJ, Ratcliffe RG, O’Neill EC (2019) Euglena central metabolic pathways and their subcellular locations. Metabolites 9(6):115
pmcid: 6630311
doi: 10.3390/metabo9060115
pubmed: 6630311
Israilides C, Smith A, Harthill J, Barnett C, Bambalov G, Scanlon B (1998) Pullulan content of the ethanol precipitate from fermented agro-industrial wastes. Appl Microbiol Biotechnol 49(5):613–617
doi: 10.1007/s002530051222
Ivušić F, Šantek B (2015) Optimization of complex medium composition for heterotrophic cultivation of Euglena gracilis and paramylon production. Bioprocess Biosyst Eng 38(6):1103–1112
pubmed: 25601569
doi: 10.1007/s00449-015-1353-3
pmcid: 25601569
Jacob-Lopes E, Mérida LR, Queiroz MI, Zepka LQ (2015) Microalgal biorefineries. Jacob-Lopes and Queiroz (ed) Biomass production and uses Rijeka: InTech:81-106
Jeon MS, Oh J-J, Kim JY, Han S-I, Sim SJ, Choi Y-E (2019) Enhancement of growth and paramylon production of Euglena gracilis by co-cultivation with Pseudoalteromonas sp. MEBiC 03485. Bioresour Technol 288:121513
pubmed: 31146078
doi: 10.1016/j.biortech.2019.121513
pmcid: 31146078
Khatiwada B, Kautto L, Sunna A, Sun A, Nevalainen H (2019) Nuclear transformation of the versatile microalga Euglena gracilis. Algal Res 37:178–185
doi: 10.1016/j.algal.2018.11.022
Kim JY, Oh J-J, Jeon MS, Kim G-H, Choi Y-E (2019) Improvement of Euglena gracilis paramylon production through a cocultivation strategy with the indole-3-acetic acid-producing bacterium Vibrio natriegens. App Environ Biotech 85(19):e01548–e01519
Kim S, Lee D, Lim D, Lim S, Park S, Kang C, Yu J, Lee T (2020) Paramylon production from heterotrophic cultivation of Euglena gracilis in two different industrial byproducts: corn steep liquor and brewer’s spent grain. Algal Res 47:101826
doi: 10.1016/j.algal.2020.101826
Kottuparambil S, Thankamony RL, Agusti S (2019) Euglena as a potential natural source of value-added metabolites. A review. Algal Res 37:154–159
doi: 10.1016/j.algal.2018.11.024
Krajčovič J, Vesteg M, Schwartzbach SD (2015) Euglenoid flagellates: a multifaceted biotechnology platform. J Biotechnol 202:135–145
pubmed: 25527385
doi: 10.1016/j.jbiotec.2014.11.035
pmcid: 25527385
Lee J, Cho D-H, Ramanan R, Kim B-H, Oh H-M, Kim H-S (2013) Microalgae-associated bacteria play a key role in the flocculation of Chlorella vulgaris. Bioresour Technol 131:195–201
pubmed: 23347927
doi: 10.1016/j.biortech.2012.11.130
pmcid: 23347927
Murphree CA, Dums JT, Jain SK, Zhao C, Young DY, Khoshnoodi N, Tikunov A, Macdonald J, Pilot G, Sederoff H (2017) Amino acids are an ineffective fertilizer for Dunaliella spp. growth. Frontiers in. Plant Sci 8:847
Nakazawa M, Andoh H, Koyama K, Watanabe Y, Nakai T, Ueda M, Sakamoto T, Inui H, Nakano Y, Miyatake K (2015) Alteration of wax ester content and composition in Euglena gracilis with gene silencing of 3-ketoacyl-CoA thiolase isozymes. Lipids 50(5):483–492
pubmed: 25860691
doi: 10.1007/s11745-015-4010-3
pmcid: 25860691
Ndikubwimana T, Zeng X, Liu Y, Chang J-S, Lu Y (2014) Harvesting of microalgae Desmodesmus sp. F51 by bioflocculation with bacterial bioflocculant. Algal Res 6:186–193
doi: 10.1016/j.algal.2014.09.004
Ogawa T, Tamoi M, Kimura A, Mine A, Sakuyama H, Yoshida E, Maruta T, Suzuki K, Ishikawa T, Shigeoka S (2015) Enhancement of photosynthetic capacity in Euglena gracilis by expression of cyanobacterial fructose-1, 6-/sedoheptulose-1, 7-bisphosphatase leads to increases in biomass and wax ester production. Biotechnology for Biofuels 8(1):80
pubmed: 26056534
pmcid: 4459067
doi: 10.1186/s13068-015-0264-5
Ogbonna JC, Tomiyamal S, Tanaka H (1998) Heterotrophic cultivation of Euglena gracilis Z for efficient production of α-tocopherol. J Appl Phycol 10(1):67–74
doi: 10.1023/A:1008011201437
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65(6):635–648
pubmed: 15300417
doi: 10.1007/s00253-004-1647-x
pmcid: 15300417
Rahman KM (2020) Food and high value products from microalgae: market opportunities and challenges microalgae biotechnology for food, health and high value products. Springer:3–27
Rodríguez-Zavala J, Ortiz-Cruz M, Mendoza-Hernández G, Moreno-Sánchez R (2010) Increased synthesis of α-tocopherol, paramylon and tyrosine by Euglena gracilis under conditions of high biomass production. J Appl Microbiol 109(6):2160–2172
pubmed: 20854454
doi: 10.1111/j.1365-2672.2010.04848.x
pmcid: 20854454
Russo R, Barsanti L, Evangelista V, Frassanito AM, Longo V, Pucci L, Penno G, Gualtieri P (2017) Euglena gracilis paramylon activates human lymphocytes by upregulating pro-inflammatory factors. Food Science & Nutrition 5(2):205–214
doi: 10.1002/fsn3.383
Salim S, Bosma R, Vermuë MH, Wijffels RH (2011) Harvesting of microalgae by bio-flocculation. J Appl Phycol 23(5):849–855
pubmed: 21957329
doi: 10.1007/s10811-010-9591-x
Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer’s disease. N Engl J Med 336(17):1216–1222
pubmed: 9110909
doi: 10.1056/NEJM199704243361704
Šantek B, Felski M, Friehs K, Lotz M, Flaschel E (2010) Production of paramylon, a β-1, 3-glucan, by heterotrophic cultivation of Euglena gracilis on potato liquor. Eng Life Sci 10(2):165–170
Šantek B, Friehs K, Lotz M, Flaschel E (2012) Production of paramylon, a β-1, 3-glucan, by heterotrophic growth of Euglena gracilis on potato liquor in fed-batch and repeated-batch mode of cultivation. Eng Life Sci 12(1):89–94
doi: 10.1002/elsc.201100025
Schwarzhans J-P, Cholewa D, Grimm P, Beshay U, Risse J-M, Friehs K, Flaschel E (2015) Dependency of the fatty acid composition of Euglena gracilis on growth phase and culture conditions. J Appl Phycol 27(4):1389–1399. https://doi.org/10.1007/s10811-014-0458-4
doi: 10.1007/s10811-014-0458-4
Suzuki K (2017) Large-scale cultivation of Euglena. Euglena: biochemistry, cell and molecular biology:285–293
Suzuki K, Nakano R, Yamaguchi H, Maruta A, Nakano Y (2013) Function of paramylon from Euglena gracilis as filler. J Soc Pow Tech, Japan 50(10):728–732
doi: 10.4164/sptj.50.728
Takeyama H, Kanamaru A, Yoshino Y, Kakuta H, Kawamura Y, Matsunaga T (1997) Production of antioxidant vitamins, β-carotene, vitamin C, and vitamin E, by two-step culture of Euglena gracilis Z. Biotechnol Bioeng 53(2):185–190
pubmed: 18633963
doi: 10.1002/(SICI)1097-0290(19970120)53:2<185::AID-BIT8>3.0.CO;2-K
pmcid: 18633963
Tani Y, Tsumura H (1989) Screening for tocopherol-producing microorganisms and α-tocopherol production by Euglena gracilis Z. Agric Biol Chem 53(2):305–312
Tossavainen M, Ilyass U, Ollilainen V, Valkonen K, Ojala A, Romantschuk M (2019) Influence of long term nitrogen limitation on lipid, protein and pigment production of Euglena gracilis in photoheterotrophic cultures. PeerJ 7:e6624
pubmed: 30972245
pmcid: 6448558
doi: 10.7717/peerj.6624
Ummalyma SB, Gnansounou E, Sukumaran RK, Sindhu R, Pandey A, Sahoo D (2017) Bioflocculation: an alternative strategy for harvesting of microalgae–an overview. Bioresour Technol 242:227–235
pubmed: 28314665
doi: 10.1016/j.biortech.2017.02.097
pmcid: 28314665
Wang Y, Seppänen-Laakso T, Rischer H, Wiebe MG (2018) Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. PLoS One 13(4)
Watanabe T, Shimada R, Matsuyama A, Yuasa M, Sawamura H, Yoshida E, Suzuki K (2013) Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice. Food Funct 4(11):1685–1690
pubmed: 24104447
doi: 10.1039/c3fo60256g
pmcid: 24104447
Wilburn E, Mahan D, Hill D, Shipp T, Yang H (2008) An evaluation of natural (RRR-α-tocopheryl acetate) and synthetic (all-rac-α-tocopheryl acetate) vitamin E fortification in the diet or drinking water of weanling pigs. J Anim Sci 86(3):584–591
pubmed: 18156353
doi: 10.2527/jas.2007-0377
pmcid: 18156353
Yoshida Y, Saito Y, Jones LS, Shigeri Y (2007) Chemical reactivities and physical effects in comparison between tocopherols and tocotrienols: physiological significance and prospects as antioxidants. J Biosci Bioeng 104(6):439–445
pubmed: 18215628
doi: 10.1263/jbb.104.439
pmcid: 18215628