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Diverse thermal responses of the growth, photosynthesis, lipid and fatty acids in the terrestrial oil-producing microalga Vischeria sp. WL1

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Abstract

Temperature is a common and effective environmental driver employed for promoting lipid accumulation in microalgae, while the thermal reaction norms associated with total lipid, fatty acid, photosynthesis and growth are little known. Here, we investigated the thermal responses of growth rate, photosynthetic parameters, lipid accumulation, and fatty acid composition at a wide range of temperatures (9, 13, 17, 21, 25, 28, 30, 31, 32, and 32.3 ℃) in a terrestrial high-oil-production microalga Vischeria sp. WL1 on days 4 and 8. We identified the thermal reaction norm of growth rate for Vischeria sp. WL1 with the optimal temperature of 30.5 ± 0.3 and 27.9 ± 0.6 ℃ at day 4 and 8, respectively. The percentage of oil content increased with decreasing cultivation temperature on both days 4 and 8. We found that several photosynthetic parameters (Chl a content, Fv/Fm, PIabs, φE0, and ψ0) showed similar thermal reaction norms as that of the growth rate. While, the thermal responses of fatty acids exhibit remarkable diversity, and only linoleic (C18:2), linolenic (C18:3), and arachidonic (C20:4) show comparable thermal reaction norms as that of the growth rate. Our study reveals the consistent/intricate physiological and lipidic adaptations to temperature fluctuations, providing insights for optimizing oil yield and targeted fatty acid production via temperature manipulation.

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References

  • Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240

    Google Scholar 

  • Barati B, Gan SY, Lim PE, Beardall J, Phang SM (2019) Green algal molecular responses to temperature stress. Acta Physiol Plantarum 41:26

    Google Scholar 

  • Barkia I, Saari N, Manning SR (2019) Microalgae for high-value products towards human health and nutrition. Mar Drugs 17:304

    Google Scholar 

  • Barton S, Jenkins J, Buckling A, Schaum CE, Smirnoff N, Raven JA, Yvon-Durocher G, Ezenwa V (2020) Evolutionary temperature compensation of carbon fixation in marine phytoplankton. Ecol Lett 23:722–733

    PubMed  PubMed Central  Google Scholar 

  • Boelen P, Dijk R, Damsté JSS, Rijpstra WIC, Buma AG (2013) On the potential application of polar and temperate marine microalgae for EPA and DHA production. AMB Express 3:26

    PubMed  PubMed Central  Google Scholar 

  • Cao J, Yuan H, Li B, Yang J (2014) Significance evaluation of the effects of environmental factors on the lipid accumulation of Chlorella minutissima UTEX 2341 under low-nutrition heterotrophic condition. Bioresour Technol 152:177–184

    CAS  PubMed  Google Scholar 

  • Chaisutyakorn P, Praiboon J, Kaewsurelikhit C (2017) The effect of temperature on growth and lipid and fatty acid composition on marine micaroalgae used for biodiesel production. J Appl Phycol 30:37–45

    Google Scholar 

  • Chamizo S, Belnap J, Eldridge D, J., Cantón Y, Malam Issa O, (2016) The role of biocrusts in arid land hydrology. In: Weber B, Büdel B, Belnap J (eds) Biological Soil Crusts: An Organizing Principle in Drylands. Springer, Cham, pp 321–346

    Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Biotech Adv 25:294–306

    CAS  Google Scholar 

  • Converti A, Casazza AA, Ortiz EY, Perego P, Del Borghi M (2009) Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Process 48:1146–1151

    CAS  Google Scholar 

  • Courchesne NM, Parisien A, Wang B, Lan CQ (2009) Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotech 141:31–41

    CAS  Google Scholar 

  • Deng W, Sun J, Chang ZG, Gou NN, Wu WY, Luo XL, Zhou JS, Yu HB, Ji H (2020) Energy response and fatty acid metabolism in Onychostoma macrolepis exposed to low-temperature stress. J Thermal Biol 94:102725

    CAS  Google Scholar 

  • Deshmukh S, Kumar R, Bala K (2019) Microalgae biodiesel: A review on oil extraction, fatty acid composition, properties and effect on engine performance and emissions. Fuel Process Technol 191:232–247

    CAS  Google Scholar 

  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotech 19:235–240

    CAS  PubMed  Google Scholar 

  • Fakhry EM, Maghraby DME (2015) Lipid accumulation in response to nitrogen limitation and variation of temperature in Nannochloropsis salina. Bot Stud 56:2–8

    Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    CAS  PubMed  ADS  Google Scholar 

  • He Q, Yang H, Hu C (2018) Effects of temperature and its combination with high light intensity on lipid production of Monoraphidium dybowskii Y2 from semi-arid desert areas. Bioresour Technol 265:407–414

    CAS  PubMed  Google Scholar 

  • Helamieh M, Gebhardt A, Reich M, Kuhn F, Kerner M, Kummerer K (2021) Growth and fatty acid composition of Acutodesmus obliquus under different light spectra and temperatures. Lipids 56:485–498

    CAS  PubMed  Google Scholar 

  • Hoffmann M, Marxen K, Schulz R, Vanselow KH (2010) TFA and EPA productivities of Nannochloropsis salina influenced by temperature and nitrate stimuli in turbidostatic controlled experiments. Mar Drugs 8:2526–2545

    CAS  PubMed  Google Scholar 

  • Hu Q (2013) Environmental effects on cell composition. In: Richmond A, Hu Q (eds) Handbook of Microalgal Culture. Applied Phycology and Biotechnology. Wiley-Blackwell, Oxford, pp 114–122

    Google Scholar 

  • Ivanova JG, Kabaivanova LV, Petkov GD (2015) Temperature and irradiance effects on Rhodella reticulata growth and biochemical characteristics. Russ J Plant Physiol 62:647–652

    CAS  Google Scholar 

  • Kremer CT, Fey SB, Arellano AA, Vasseur DA (2018) Gradual plasticity alters population dynamics in variable environments: thermal acclimation in the green alga Chlamydomonas reinhartdii. Proc R Soc B 285:20171942

    PubMed  PubMed Central  Google Scholar 

  • Krimech A, Helamieh M, Wulf M, Krohn I, Riebesell U, Cherifi O, Mandi L, Kerner M (2022) Differences in adaptation to light and temperature extremes of Chlorella sorokiniana strains isolated from a wastewater lagoon. Bioresour Technol 350:126931

    CAS  PubMed  Google Scholar 

  • Lepori-Bui M, Paight C, Eberhard E, Mertz CM, Moeller HV (2022) Evidence for evolutionary adaptation of mixotrophic nanoflagellates to warmer temperatures. Global Change Biol 28:7094–7107

    CAS  Google Scholar 

  • Li X, Hu HY, Zhang YP (2011) Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresource Technol 102:3098–3102

    CAS  Google Scholar 

  • Li Y, Horsman M, Wu N, Lan CQ, Dubois-Calero N (2008) Biofuels from microalgae. Biotechnol Progr 24:815–820

    CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–382

    CAS  Google Scholar 

  • Listmann L, LeRoch M, Schlüter L, Thomas MK, Reusch TBH (2016) Swift thermal reaction norm evolution in a key marine phytoplankton species. Evol Appl 9:1156–1164

    PubMed  PubMed Central  Google Scholar 

  • Ma C, Wen H, Xing D, Pei X, Zhu J, Ren N, Liu B (2017) Molasses wastewater treatment and lipid production at low temperature conditions by a microalgal mutant Scenedesmus sp. Z-4. Biotechnol Biofuels 10:111

    Google Scholar 

  • Mortensen SH, Borsheim KY, Rainuzzo JR, 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 and Ecol 122:173–185

    CAS  Google Scholar 

  • O’Donnell DR, Du ZY, Litchman E (2019) Experimental evolution of phytoplankton fatty acid thermal reaction norms. Evol Appl 12:1201–1211

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donnell DR, Hamman CR, Johnson EC, Kremer CT, Klausmeier CA, Litchman E (2018) Rapid thermal adaptation in a marine diatom reveals constraints and trade-offs. Glob Chang Biol 24:4554–4565

    PubMed  ADS  Google Scholar 

  • Pasquet V, Ulmann L, Mimouni V, Guihéneuf F, Jacquette B, Morant-Manceau A, Tremblin G (2014) Fatty acids profile and temperature in the cultured marine diatom Odontella aurita. J Appl Phycol 26:2265–2271

    CAS  Google Scholar 

  • Ranglova K, Lakatos GE, Manoel JAC, Grivalsky T, Masojidek J (2019) Rapid screening test to estimate temperature optima for microalgae growth using photosynthesis activity measurements. Folia Microbiol 64:615–625

    CAS  Google Scholar 

  • Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461

    CAS  Google Scholar 

  • Renaud SM, Thinh L, 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 211:195–214

    CAS  Google Scholar 

  • Renaud SM, Zhou HC, Parry DL, Thinh L, 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, Nizschia paleacea, and commercial species Isochrysis sp. (clone T.ISO). J Appl Phycol 7:595–602

    CAS  Google Scholar 

  • Satchithanandam S, Fritsche J, Rader JI (2002) Gas chromatographic analysis of infant formulas for total fatty acids, including trans fatty acids. J AOAC Int 85:86–94

    CAS  PubMed  Google Scholar 

  • Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G (2018) Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun 9:1719

    PubMed  PubMed Central  ADS  Google Scholar 

  • She Y, Gao X, Jing X, Wang J, Dong Y, Cui J, Xue H, Li Z, Zhu D (2022) Effects of nitrogen source and NaCl stress on oil production in Vischeria sp. WL1 (Eustigmatophyceae) isolated from dryland biological soil crusts in China. J Appl Phycol 34:1281–1291

    CAS  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-bazire G (1971) Purification and properties of unicellular blue-green algae (Order Chroococcales). Bact Rev 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sushchik NN, Kalacheva GS, Zhila NO (2003) A temperature dependence of the intra- and extracellular fatty-acid composition of green algae and cyanobacterium. Russ J Plant Physiol 50:374–380

    CAS  Google Scholar 

  • Svenning JB, Dalheim L, Eilertsen HC, Vasskog T (2019) Temperature dependent growth rate, lipid content and fatty acid composition of the marine cold-water diatom Porosira glacialis. Algal Res 37:11–16

    Google Scholar 

  • Tan KWM, Lee YK (2016) The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth. Biotechnol Biofuels 9:255

    PubMed  PubMed Central  Google Scholar 

  • Teoh M-L, Chu W-L, Marchant H, Phang S-M (2004) Influence of culture temperature on the growth, biochemical composition and fatty acid profiles of six Antarctic microalgae. J Appl Phycol 16:421–430

    CAS  Google Scholar 

  • Thomas MK, Kremer CT, Klausmeier CA, Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–1088

    CAS  PubMed  ADS  Google Scholar 

  • Thomas MK, Litchman E (2015) Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia 763:357–369

    Google Scholar 

  • Thompson PA, Guo MX, Harrison PJ (1992) Effects of variation in temperature. I. On the biochemical composition of eight species of marine phytoplankton. J Phycol 28:481–488

    CAS  Google Scholar 

  • Thompson PA, Guo MX, Harrison PJ, Whyte JNC (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497

    CAS  Google Scholar 

  • Toseland A, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, Lenton TM, Valentin K, Pearson GA, Moulton V, Mock T (2013) The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Climate Change 3:979–984

    CAS  ADS  Google Scholar 

  • Wang Y, He B, Sun Z, Chen Y-F (2016) Chemically enhanced lipid production from microalgae under low sub-optimal temperature. Algal Res 16:20–27

    Google Scholar 

  • Weber B, Tamm A, Maier S, Rodríguez-Caballero E (2018) Biological soil crusts of the Succulent Karoo: a review. Afr J Range Forage Sci 35:335–350

    Google Scholar 

  • Xu J, Li T, Li CL, Zhu SN, Wang ZM, Zeng EY (2020) Lipid accumulation and eicosapentaenoic acid distribution in response to nitrogen limitation in microalga Eustigmatos vischeri JHsu-01 (Eustigmatophyceae). Algal Res 48:101910

    Google Scholar 

  • Xue Z, Wan F, Yu W, Liu J, Zhang Z, Kou X (2018) Edible oil production from microalgae: A review. Eur J Lipid Sci Technol 120:1700428

    Google Scholar 

  • Yuan X, Gao X, Zheng T, Wang J, Dong Y, Xue H (2023) Carbon nanomaterial-treated cell cultures of Nostoc flagelliforme produce exopolysaccharides with ameliorative physio-chemical properties. Int J Biol Macromol 227:726–735

    CAS  PubMed  Google Scholar 

  • Zhong HY, Bedgood DR, Bishop AG, Prenzler PD, Robards K (2007) Endogenous biophenol, fatty acid and volatile profiles of selected oils. Food Chem 100:1544–1551

    CAS  Google Scholar 

  • Zhu CJ, Lee YK, Chao TM (1997) Effects of temperature and growth phase on lipid and biochemical composition of Isochrysis galbana TK1. J Appl Phycol 9:451–457

    CAS  Google Scholar 

Download references

Funding

This research was supported by the Key Research and Development Program of Shaanxi Province (No. 2022NY-194) and the Shaanxi Province Qin Chuangyuan “Scientist+Engineer” Team Construction Project (No. 2023KXJ-206).

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Authors and Affiliations

  1. School of Food and Biological Engineering, Shaanxi University of Science & Technology, Xi’an, 710021, Shaanxi, China

    Daxi Wang, Xiang Gao, Xiaojiao Wang, Xiaolong Yuan, Xinhong Guo & Zhengke Li

  2. College of Environmental and Resource Sciences, Fujian Key Laboratory of Pollution Control and Resource Recycling, Fujian Normal University, Fujian, Fuzhou, 350007, China

    Yong Zhang

  3. Hubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi, 435002, Hubei, China

    Kui Xu

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  1. Daxi Wang
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  4. Xiaolong Yuan
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  5. Xinhong Guo
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Contributions

ZL and XG designed research. DW, XW, XY, XG performed the experiments. DW and ZL wrote the manuscript. All authors contributed to the corrections of this manuscript.

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Correspondence to Xiang Gao or Zhengke Li.

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Wang, D., Gao, X., Wang, X. et al. Diverse thermal responses of the growth, photosynthesis, lipid and fatty acids in the terrestrial oil-producing microalga Vischeria sp. WL1. J Appl Phycol 36, 29–39 (2024). https://doi.org/10.1007/s10811-023-03152-3

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