Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-06-11T16:36:55.801Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  15 June 2020

Nahla Bouzidi Open the ORCID record for Nahla Bouzidi [Opens in a new window] ,
Fatma Zili ,
Federico García-Maroto ,
Diego López Alonso  and
Hatem Ben Ouada
Nahla Bouzidi*
Affiliation:
Laboratory of Blue Biotechnology and Aquatic Bioproducts (B3Aqua), National Institute of Marine Sciences and Technology, BP 59, 5000Monastir, Tunisia
Fatma Zili
Affiliation:
Laboratory of Blue Biotechnology and Aquatic Bioproducts (B3Aqua), National Institute of Marine Sciences and Technology, BP 59, 5000Monastir, Tunisia
Federico García-Maroto
Affiliation:
Department of Chemistry and Physics, University of Almeria, 04120Almería, Spain
Diego López Alonso
Affiliation:
Department of Biology and Geology, University of Almería, 04120Almería, Spain
Hatem Ben Ouada
Affiliation:
Laboratory of Blue Biotechnology and Aquatic Bioproducts (B3Aqua), National Institute of Marine Sciences and Technology, BP 59, 5000Monastir, Tunisia
*
Author for correspondence: Nahla Bouzidi, E-mail: bouzidi.nehla@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

A thermo-tolerant diatom species has been isolated from Tunisian hot spring water (40°C). The isolated diatom has been molecularly identified and classified into the genus Halamphora. The growth kinetics, lipid content and distribution of fatty acids were assessed at 20 and 30°C temperature levels and constant irradiance in controlled batch cultures (11 days). Halamphora sp. showed better growth (μ = 0.53 day−1) and a higher lipid yield (25% of the dry weight) at a higher temperature (30°C). Under the two temperatures tested, the highest lipid and fatty acid contents were mainly reached during the stationary growth phase. The fatty acid profile showed a significant content of two essential fatty acids, eicosapentaenoic acid (EPA, 20:5n-3) and arachidonic acid (AA, 20:4n-6), reaching ~15% and ~21% of the total fatty acids, respectively, at 20°C and 30°C. The distribution of the different components of the fatty acids showed that EPA and AA were mainly located in the neutral lipid fraction in the stationary phase.

Keywords

Arachidonic aciddiatomseicosapentaenoic acidfast growthHalamphoralipidsthermophile
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 4 , June 2020 , pp. 529 - 536
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alonso, DL, Belarbi, EH, Rodríguez-Ruiz, J, Segura, CI and Giménez, A (1998) Acyl lipids of three microalgae. Phytochemistry 47, 1473–1481.10.1016/S0031-9422(97)01080-7CrossRefGoogle Scholar
Alonso, DL, Belarbi, EH, Fernández-Sevilla, JM, Rodríguez-Ruiz, J and Grima, EM (2000) Acyl lipid composition variation related to culture age and nitrogen concentration in continuous culture of the microalga Phaeodactylum tricornutum. Phytochemistry 54, 461–471.10.1016/S0031-9422(00)00084-4CrossRefGoogle ScholarPubMed
Anderson, NJ (2000) Minireview: diatoms, temperature and climatic change. European Journal of Phycology 35, 307–314.Google Scholar
Bigogno, C, Khozin-Goldberg, I, Boussiba, S, Vonshak, A and Cohen, Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60, 497–503.10.1016/S0031-9422(02)00100-0CrossRefGoogle ScholarPubMed
Bruder, K and Medlin, LK (2007) Molecular assessment of phylogenetic relationships in selected species/genera in the naviculoid diatoms (Bacillariophyta). I. The genus Placoneis. Nova Hedwigia 85, 331–352.10.1127/0029-5035/2007/0085-0331CrossRefGoogle Scholar
Chen, YC (2012) The biomass and total lipid content and composition of twelve species of marine diatoms cultured under various environments. Food Chemistry 131, 211–219.10.1016/j.foodchem.2011.08.062CrossRefGoogle Scholar
Chtourou, H, Dahmen, I, Jebali, A, Karray, F, Hassairi, I, Abdelkafi, S, Ayadi, H, Sayadi, S and Dhouib, A (2015 a) Characterization of Amphora sp., a newly isolated diatom wild strain, potentially usable for biodiesel production. Bioprocess and Biosystems Engineering 38, 1381–1392.10.1007/s00449-015-1379-6CrossRefGoogle ScholarPubMed
Chtourou, H, Dahmen, I, Karray, F, Sayadi, S and Dhouib, A (2015 b) Biodiesel production of Amphora sp. and Navicula sp. by different cell disruption and lipid extraction methods. Journal of Biobased Materials and Bioenergy 9, 588–595.10.1166/jbmb.2015.1563CrossRefGoogle Scholar
Chuecas, L and Riley, JP (1969) Component fatty acids of the total lipids of some marine phytoplankton. Journal of the Marine Biological Association of the United Kingdom 49, 97–l16.10.1017/S0025315400046439CrossRefGoogle Scholar
Covarrubias, Y, Cantoral-Uriza, EA, Casas-Flores, JS and Garcia-Meza, JV (2016) Thermophile mats of microalgae growing on the woody structure of a cooling tower of a thermoelectric power plant in Central Mexico. Revista Mexicana de Biodiversidad 87, 277–287.10.1016/j.rmb.2016.04.001CrossRefGoogle Scholar
Dahmen-Ben Moussa, I, Athmouni, K, Chtourou, H, Ayadi, H, Sayadi, S and Dhouib, A (2018 a) Phycoremediation potential, physiological, and biochemical response of Amphora subtropica and Dunaliella sp. to nickel pollution. Journal of Applied Phycology 30, 931–941.CrossRefGoogle Scholar
Dahmen-Ben Moussa, I, Chtourou, H, Rezgui, F, Sayadi, S and Dhouib, A (2018 b) Salinity stress increases lipid, secondary metabolites and enzyme activity in Amphora subtropica and Dunaliella sp. for biodiesel production. Bioresource Technology 218, 816–825.10.1016/j.biortech.2016.07.022CrossRefGoogle Scholar
Eland, LE, Davenport, R and Mota, CR (2012) Evaluation of DNA extraction methods for freshwater eukaryotic microalgae. Water Research 46, 5355–5364.10.1016/j.watres.2012.07.023CrossRefGoogle ScholarPubMed
Elser, JJ, Sterner, RW, Gorokhova, E, Fagan, WF, Markow, TA, Cotner, JB, Harrison, JF, Hobbie, SE, Odell, GM and Weider, LW (2000) Biological stoichiometry from genes to ecosystems. Ecology Letters 3, 540–550.10.1046/j.1461-0248.2000.00185.xCrossRefGoogle Scholar
Fernández, FG, Pérez, JA, Sevilla, JM, Camacho, FG and Grima, EM (2000) Modeling of eicosapentaenoic acid (EPA) production from Phaeodactylum tricornutum cultures in tubular photobioreactors. Effects of dilution rate, tube diameter, and solar irradiance. Biotechnology and Bioengineering 68, 173–183.10.1002/(SICI)1097-0290(20000420)68:2<173::AID-BIT6>3.0.CO;2-C3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Ghozzi, K, Zemzem, M, Ben Dhiab, R, Challouf, R, Yahia, A, Omrane, H and Ben Ouada, H (2013) Screening of thermophilic microalgae and cyanobacteria from Tunisian geothermal sources. Journal of Arid Environments 97, 14–17.CrossRefGoogle Scholar
Guillard, RLR (2005) Purification methods for microalgae. In Andersen, RA (ed.), Algal Culturing Techniques. Amsterdam: Elsevier Academic Press, pp. 117–132.Google Scholar
Jiang, Y, Laverty, KS, Brown, J, Nunez, M, Brown, L, Chagoya, J, Burow, M and Quigg, A (2014) Effects of fluctuating temperature and silicate supply on the growth, biochemical composition and lipid accumulation of Nitzschia sp. Bioresource Technology 154, 336–344.10.1016/j.biortech.2013.12.068CrossRefGoogle ScholarPubMed
Khozin-Goldberg, I, Iskandarov, U and Cohen, Z (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Applied Microbiology and Biotechnology 91, 905–915.10.1007/s00253-011-3441-xCrossRefGoogle ScholarPubMed
Lebeau, T and Robert, JM (2003) Diatom cultivation and biotechnologically relevant products. Part I: Cultivation at various scales. Applied Microbiology and Biotechnology 60, 612–623.CrossRefGoogle ScholarPubMed
Liang, Y, Mai, K and Sun, S (2005) Differences in growth, total lipid content and fatty acid composition among 60 clones of Cylindrotheca fusiformis. Journal of Applied Phycology 17, 61–65.CrossRefGoogle Scholar
Lim, DKY, Garg, S, Timmins, M, Zhang, ESB, Thomas-Hall, SR, Schuhmann, H, Li, Y and Schenk, PM (2012) Isolation and evaluation of oil-producing microalgae from subtropical coastal and brackish waters. PLoS ONE 7, e40751.10.1371/journal.pone.0040751CrossRefGoogle ScholarPubMed
Mannino, AM (2007) Diatoms from thermal-sulphur waters of “Fiume Caldo” (North-western Sicily). Cryptogamie Algologie 28, 385–396.Google Scholar
Martín, LA, Popovich, CA, Martinez, AM, Damiani, MC and Leonardi, PI (2016) Oil assessment of Halamphora coffeaeformis diatom growing in a hybrid two-stage system for biodiesel production. Renewable Energy 92, 127–135.10.1016/j.renene.2016.01.078CrossRefGoogle Scholar
Mezhoud, N, Zili, F, Bouzidi, N, Helaoui, F, Ammar, J and Ben Ouada, H (2014) The effects of temperature and light intensity on growth, reproduction and EPS synthesis of a thermophilic strain related to the genus Graesiella. Bioprocess and Biosystems Engineering 37, 2271–2280.10.1007/s00449-014-1204-7CrossRefGoogle ScholarPubMed
Moheimani, NR, Borowitzka, MA, Isdepsky, A and Fon Sing, S (2013) Standard methods for measuring growth of algae and their composition. In Borowitzka, MA and Moheimani, NR (eds), Algae for Biofuels and Energy. Dordrecht: Springer, pp. 265–284.10.1007/978-94-007-5479-9_16CrossRefGoogle Scholar
Moll, KM, Gardner, RD, Eustance, EO, Gerlach, R and Peyton, BM (2014) Combining multiple nutrient stresses and bicarbonate addition to promote lipid accumulation in the diatom RGd-1. Algal Research 5, 7–15.CrossRefGoogle Scholar
Napolitano, GE, Ackman, RG and Ratnayake, WMN (1990) Fatty acid composition of three cultured algal species (Isochrysis galbana, Chaetoceros gracilis and Chaetoceros calcitrans) used as food for bivalve larvae. Journal of the World Aquaculture Society 21, 122–130.CrossRefGoogle Scholar
Oliveira, M, Monteiro, M, Robbs, P and Leite, S (1999) Growth and chemical composition of Spirulina maxima and Spirulina platensis biomass at different temperatures. Aquaculture International 7, 261–275.CrossRefGoogle Scholar
Pulz, O and Gross, W (2004) Valuable products from biotechnology of microalgae. Applied Microbiology and Biotechnology 65, 635–648.10.1007/s00253-004-1647-xCrossRefGoogle ScholarPubMed
Renaud, SM, Zhou, HC, Parry, DL, Thinh, L and Woo, KC (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). Journal of Applied Phycology 7, 595–602.10.1007/BF00003948CrossRefGoogle Scholar
Richmond, A (1986) Cell response to environmental factors. In Richmond, A (ed.), Handbook of Microalgal Mass Cultures. Boca Raton, FL: CRC Press, pp. 69–101.Google Scholar
Rodríguez-Ruiz, J, Belarbi, EH, Sánchez, JLG and Alonso, DL (1998) Rapid simultaneous lipid extraction and transesterification for fatty acid analyses. Biotechnology Techniques 12, 689–691.CrossRefGoogle Scholar
Rousch, JM, Bingham, SE and Sommerfeld, MR (2003) Changes in fatty acid profiles of thermo-intolerant and thermo-tolerant marine diatoms during temperature stress. Journal of Experimental Marine Biology and Ecology 295, 145–156.10.1016/S0022-0981(03)00293-4CrossRefGoogle Scholar
Seckbach, J (2007) Algae and Cyanobacteria in Extreme Environments, vol. 11. Dordrecht: Springer Science and Business Media.10.1007/978-1-4020-6112-7CrossRefGoogle Scholar
Stepanek, JG and Kociolek, JP (2014) Molecular phylogeny of Amphora sensu lato (Bacillariophyta): an investigation into the monophyly and classification of the amphoroid diatoms. Protist 165, 177–195.10.1016/j.protis.2014.02.002CrossRefGoogle ScholarPubMed
Stepanek, JG, Fields, FJ and Kociolek, JP (2016) A comparison of lipid content metrics using six species from the genus Halamphora (Bacillariophyta). Biofuels 7269, 1–8.Google Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.10.1093/molbev/msr121CrossRefGoogle Scholar
Thompson, PA, Guo, MX, Harrison, PJ and Whyte, JNC (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. Journal of Phycology 28, 488–497.CrossRefGoogle Scholar
Wah, NB, Latif, A, Ahmad, B, Chan, D, Chieh, J, Tan, A and Hwai, S (2015) Changes in lipid profiles of a tropical benthic diatom in different cultivation temperature. Asian Journal of Applied Science and Engineering 4, 2305–2915.Google Scholar
Wainman, BC and Smith, REH (2003) Can physicochemical factors predict lipid content in phytoplankton? Freshwater Biology 38, 571–579.10.1046/j.1365-2427.1997.00228.xCrossRefGoogle Scholar
Walne, PR (1974) Culture of Bivalve Molluscs: 50 Years’ Experience at Conwy. West Byfleet: Fishing News.Google Scholar
Yongmanitchai, W and Ward, P (1991) Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Applied and Environmental Microbiology 57, 419–425.10.1128/AEM.57.2.419-425.1991CrossRefGoogle ScholarPubMed
Zhu, CJ and Lee, YK (1997) Determination of biomass dry weight of marine microalgae. Journal of Applied Phycology 9, 189–194.10.1023/A:1007914806640CrossRefGoogle Scholar
Supplementary material: Image

Bouzidi et al. Supplementary Materials

Bouzidi et al. Supplementary Materials

Download Bouzidi et al. Supplementary Materials(Image)
Image 393 KB