Abstract
High temperatures (30–36 °C) inhibited astaxanthin accumulation in Haematococcus pluvialis under photoautotrophic conditions. The depression of carotenogenesis was primarily attributed to excess intracellular less reactive oxygen species (LROS; O2 − and H2O2) levels generated under high temperature conditions. Here, we show that the heat stress-driven inefficient astaxanthin production was improved by accelerating the iron-catalyzed Haber–Weiss reaction to convert LROS into more reactive oxygen species (MROS; O2 and OH·), thereby facilitating lipid peroxidation. As a result, during 18 days of photoautotrophic induction, the astaxanthin concentration of cells cultured in high temperatures in the presence of iron (450 μM) was dramatically increased by 75 % (30 °C) and 133 % (36 °C) compared to that of cells exposed to heat stress alone. The heat stress-driven Haber–Weiss reaction will be useful for economically producing astaxanthin by reducing energy cost and enhancing photoautotrophic astaxanthin production, particularly outdoors utilizing natural solar radiation including heat and light for photo-induction of H. pluvialis.
Similar content being viewed by others
References
Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:382–388
Augusto O, Miyamoto S (2011) Oxygen radicals and related species. In: Pantopoulos K, Schipper HM (eds) Principles of free radical biomedicine, vol. 1. Nova Science, New York, pp 19–42
Ben-Amotz A, Avron M (1983) On the factors which determine massive β-carotene accumulation in the halotolerant alga Dunaliella bardawil. Plant Physiol 72:593–597
Bielski BHJ, Richter HW (1977) Study of superoxide radical chemistry by stopped-flow radiolysis and radiation-induced oxygen-consumption. J Am Chem Soc 99:3019–3023
Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117
Bubrick P (1991) Production of astaxanthin from Haematococcus. Bioresour Technol 38:237–239
Dominguez-Bocanegra AR, Legarreta IG, Jeronimo FM, Campocosio AT (2004) Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis. Bioresour Technol 92:209–214
Fábregas J, Domínguez A, Maseda A, Otero A (2003) Interactions between irradiance and nutrient availability during astaxanthin accumulation and degradation in Haematococcus pluvialis. Appl Microbiol Biotechnol 61:545–551
Giannelli L, Yamada H, Katsuda T, Yamaji H (2014) Effects of temperature on the astaxanthin productivity and light harvesting characteristics of the green alga Haematococcus pluvialis. J Biosci Bioeng. doi:10.1016/j.jbiosc.2014.09.002
Gilmore AM, Yamamoto HY (1991) Zeaxanthin formation and energy dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol 96:635–643
González PM, Piloni NE, Puntarulo S (2012) Iron overload and lipid peroxidation in biological systems. In: Catala A (ed) Lipid peroxidation, vol. 1. InTech, Rijeka, pp 89–108
Grünewald K, Hirschberg J, Hagen C (2001) Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. J Biol Chem 276(8):6023–6029
Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21:210–216
Han D, Wang J, Sommerfeld M, Hu Q (2012) Susceptibility and protective mechanisms of motile and non motile cells of Haematococcus pluvialis (Chlorophyceae) to photooxidative stress. J Phycol 48:693–705
Harker M, Tsavalos AJ, Young AJ (1996) Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresour Technol 55:207–214
Hashimoto H, Kurra-Hotta M, Katoh S (1989) Changes in protein content and in the structure and number of chloroplasts during leaf senescence in rice seedlings. Plant Cell Physiol 30(5):707–715
Hong M-E, Choi SP, Park YI, Kim YK, Chang WS, Kim BW, Sim SJ (2012) Astaxanthin production by a highly photosensitive Haematococcus mutant. Process Biochem 47:1972–1979
Huang JC, Wang Y, Sandmann G, Chen F (2006) Isolation and characterization of a carotenoid oxygenase gene from Chlorella zofingiensis (Chlorophyta). Appl Microbiol Biotechnol 71:473–479
Jiang Y, Huang B (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52(355):341–349
Kaewpintong K, Shotipruk A, Powtongsook S, Pavasant P (2007) Photoautotrophic high-density cultivation of vegetative cells of Haematococcus pluvialis in airlift bioreactor. Bioresour Technol 98:288–295
Kang CD, Lee JS, Park TH, Sim SJ (2005) Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biotechnol 68:237–241
Kang CD, Lee JS, Park TH, Sim SJ (2007) Complementary limiting factors of astaxanthin synthesis during photoautotrophic induction of Haematococcus pluvialis: C/N ratio and light intensity. Appl Microbiol Biotechnol 74:987–994
Kehrer JP (2000) The Haber–Weiss reaction and mechanisms of toxicity. Toxicol 149:43–50
Kobayashi M, Kakizono T, Nagai S (1993) Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl Environ Microbiol 59:867–873
Kobayashi M, Kurimura Y, Tsuji Y (1997a) Light-independent astaxanthin production by the green microalga Haematococcus pluvialis under salt stress. Biotechnol Lett 19:507–509
Kobayashi M, Kurimura Y, Kakizono T, Nishio N, Tsuji Y (1997b) Morphological changes in the life cycle of the green alga Haematococcus pluvialis. J Ferment Bioeng 84:94–97
Krieger-Liszkay A, Kós PB, Hideg E (2011) Superoxide anion radicals generated by methyl viologen in photosystem I damage photosystem II. Physiol Plant 142(1):17–25
Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177
Li Y, Sommerfeld M, Chen F, Hu Q (2008) Consumption of oxygen by astaxanthin biosynthesis: a protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae). J Plant Physiol 165:1783–1797
Li Y, Huang J, Sandmann G, Chen F (2009) High-light and sodium chloride stress differentially regulate the biosynthesis of astaxanthin in Chlorella zofingiensis (Chlorophyceae). J Phycol 45:635–641
Li Y, Sommerfeld M, Chen F, Hu Q (2010) Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis (Chlorophyceae). J Appl Phycol 22:253–263
Li J, Zhu D, Niu J, Shen S, Wang G (2011) An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol Adv 29:568–574
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem: F4.3.1-F4.3.8
Lu F, Vonshak A, Boussiba S (1994) Effect of temperature and irradiance on growth of Haematococcus pluvialis (Chlorophyceae). J Phycol 30:829–833
Magalith PZ (1999) Production of ketocarotenoids by microalgae. Appl Microbiol Biotechnol 51:431–438
Mehler AH (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Arch Biochem Biophys 33(1):65–77
Perl-Treves R, Perl A (2002) In: Inzé D, Montagu MV (eds) Oxidative stress in plants, vol. 1. Taylor & Francis, London, pp 1–39
Repetto MG, Ferrarotti NF, Boveris A (2010) The involvement of transition metal ions on iron-dependent lipid peroxidation. Arch Toxicol 84:255–262
Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186
Scherz-Shouval R, Elazar Z (2009) Monitoring starvation-induced reactive oxygen species formation. Method Enzymol 452:119–130
Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant Cell Environ 27(6):725–735
Shoefs B, Rmiki NE, Rachadi J, Lemoine Y (2001) Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett 500:125–128
Sun Z, Cunningham FX, Gantt E (1998) Differential expression of two isopentenyl pyrophosphate isomerases and enhanced carotenoid accumulation in a unicellular Chlorophyte. Proc Natl Acad Sci U S A 95:11482–11488
Takahashi M, Asada K (1982) Dependence of oxygen affinity for Mehler reaction on photochemical activity of chloroplast thylakoids. Plant Cell Physiol 23(8):1457–1461
Tjahjono AE, Hayama Y, Kakizono T, Terada Y, Nishio N, Nagai S (1994) Hyper-accumulation of astaxanthin in a green alga Haematococcus pluvialis at elevated temperatures. Biotechnol Lett 16(2):133–138
Torzillo G, Goksan T, Faraloni C, Kopecky J, Masojidek J (2003) Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage. J Appl Phycol 15:127–136
Veerasamy M, He Y, Huang B (2007) Leaf senescence and protein metabolism in creeping bentgrass exposed to heat stress and treated with cytokinins. J Am Soc Hortic Sci 132(4):467–472
Wan M, Zhang J, Hou D, Fan J, Li Y, Huang J, Wang J (2014) The effect of temperature on cell growth and astaxanthin accumulation of Haematococcus pluvialis during a light–dark cyclic cultivation. Bioresour Technol 167:276–283
Wang Y, Chen T (2008) The biosynthetic pathway of carotenoids in the astaxanthin-producing green alga Chlorella zofingiensis. World J Microbiol Biotechnol 24:2927–2932
Yuan J-P, Chen F (1999) Hydrolysis kinetics of astaxanthin esters and stability of astaxanthin of Haematococcus pluvialis during saponification. J Agric Food Chem 47:31–35
Acknowledgments
This study was supported by the Korea Institute of Energy Technology Evaluation and Planning and Ministry of Trade, Industry and Energy of Korea as a part of the Project of “Process demonstration for bioconversion of CO2 to high-valued biomaterials using microalgae” (20122010200010-11-2-100) in “Energy Efficiency & Resources Technology R&D” project, the National Research Foundation of Korea (NRF) grants (grant no. NRF-2013R1A2A1A01015644/2010-0027955), University-Institute Cooperation Program (2013), and grants (2014M1A8A1049278) from Korea CCS R&D Center of the NRF funded by the Ministry of Science, ICT, and Future Planning of Korea. This study was also supported by the 2012 NLRL (National Leading Research Lab.) Project (2012R1A2A1A01008085).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hong, ME., Hwang, S.K., Chang, W.S. et al. Enhanced autotrophic astaxanthin production from Haematococcus pluvialis under high temperature via heat stress-driven Haber–Weiss reaction. Appl Microbiol Biotechnol 99, 5203–5215 (2015). https://doi.org/10.1007/s00253-015-6440-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6440-5