Enhanced astaxanthin production by oxidative stress using methyl viologen as a reactive oxygen species (ROS) reagent in green microalgae Coelastrum sp.

https://doi.org/10.22146/ijbiotech.54092

Ameerah Tharek(1), Shaza Eva Mohamad(2*), Koji Iwamoto(3), Iwane Suzuki(4), Hirofumi Hara(5), Rozzeta Dolah(6), Shinji Yoshizaki(7), Haryati Jamaluddin(8), Madihah Md Salleh(9), Adibah Yahya(10)

(1) Malaysia Japan International Institute of Technology (MJIIT), Department of Chemical and Environmental Engineering (CHEE), Universiti Teknologi Malaysia, Jalan Sultan Yahya Petra, 54100, Kuala Lumpur
(2) Malaysia Japan International Institute of Technology (MJIIT), Department of Chemical and Environmental Engineering (CHEE), Universiti Teknologi Malaysia, Jalan Sultan Yahya Petra, 54100, Kuala Lumpur
(3) Malaysia Japan International Institute of Technology (MJIIT), Department of Chemical and Environmental Engineering (CHEE), Universiti Teknologi Malaysia, Jalan Sultan Yahya Petra, 54100, Kuala Lumpur
(4) Graduate School of Life and Environmental Sciences, 1-1-1 Tennodai, University of Tsukuba, Tsukuba, 305-8572
(5) Malaysia Japan International Institute of Technology (MJIIT), Department of Chemical and Environmental Engineering (CHEE), Universiti Teknologi Malaysia, Jalan Sultan Yahya Petra, 54100, Kuala Lumpur
(6) 1Malaysia Japan International Institute of Technology (MJIIT), Department of Chemical and Environmental Engineering (CHEE), Universiti Teknologi Malaysia, Jalan Sultan Yahya Petra, 54100, Kuala Lumpur
(7) Tokyo City University, Faculty of Environmental Studies, 3-3-1 Ushikubo nishi Tsuzuki-ku, Yokohama, Kanagawa 224-8551
(8) Faculty of Science, Department of Biosciences, Universiti Teknologi Malaysia, 81310, UTM Johor Bahru
(9) Faculty of Science, Department of Biosciences, Universiti Teknologi Malaysia, 81310, UTM Johor Bahru
(10) Faculty of Science, Department of Biosciences, Universiti Teknologi Malaysia, 81310, UTM Johor Bahru
(*) Corresponding Author

Abstract


Microalgae are known to be a potential resource of high-value metabolites that can be used in the growing field of biotechnology. These metabolites constitute valuable compounds with a wide range of applications that strongly enhance a bio-based economy. Among these metabolites, astaxanthin is considered the most important secondary metabolite, having superior antioxidant properties. For commercial feasibility, microalgae with enhanced astaxanthin production need to be developed. In this study, the tropical green microalgae strain, Coelastrum sp., isolated from the environment in Malaysia, was incubated with methyl viologen, a reactive oxygen species (ROS) reagent that generates superoxide anion radicals (O2-) as an enhancer to improve the accumulation of astaxanthin. The effect of different concentrations of methyl viologen on astaxanthin accumulation was investigated. The results suggested that the supplementation of methyl viologen at low concentration (0.001 mM) was successfully used as a ROS reagent in facilitating and thereby increasing the production of astaxanthin in Coelastrum sp. at a rate 1.3 times higher than in the control.

Keywords


Astaxanthin; Coelastrum sp.; methyl viologen; reactive oxygen species

Full Text:

PDF


References

Ambati RR, Moi PS, Ravi S, Aswathanarayana RG. 2014. Astaxanthin: Sources, extraction,  stabil­ity, biological activities and its commercial appli­ cations ­ A review. Mar Drugs 12(1):128–152. doi:10.3390/md12010128.

Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal trans­duction. Annu Rev of Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701.

Asada K. 1994. Production and action of active oxy­  gen species in photosynthetic tissues. In:  C Foyer,  P Mullineaux, editors, Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton, Ann: CRC Press. p. 77–104. doi:10.1201/9781351070454­.

Chokshi K, Pancha I, Ghosh A, Mishra S. 2017. Oxida­tive stress­induced bioprospecting of microalgae. In: M Kumar, P Ralph, editors, Systems Biology of Ma­ rine Ecosystems. Cham: Springer International Publishing. p. 251–276. doi:10.1007/978­3­319­62094­.

Clarens AF, Resurreccion EP, White MA, Colosi LM. 2010. Environmental life cycle comparison of algae to other bioenergy feedstocks. Environ Sci Technol 44(5):1813–1819. doi:10.1021/es902838n.

Dragoş N, Bercea V, Bica A, Drugǎ B, Nicoarǎ A, Coman C. 2010. Astaxanthin production from a new strain of Haematococcus pluvialis grown in batch culture. Ann Romanian Soc Cell Biol. 15(2):353–361.

Fraser PD, Bramley PM. 2004. The biosynthesis and nutri­tional uses of carotenoids. Prog Lipid Res. 43(3):228– 265. doi:10.1016/j.plipres.2003.10.002.

Guerin M, Huntley ME, Olaizola M. 2003. Haemato­ coccus astaxanthin: Applications for human health and nutrition. Trends Biotechnol. 21(5):210–216. doi:10.1016/S0167­7799(03)00078­7.

Hong ME, Hwang SK, Chang WS, Kim BW, Lee J, Sim SJ. 2015. Enhanced autotrophic astaxanthin pro­ duction from Haematococcus pluvialis under high temperature via heat stress­driven Haber–Weiss reaction. Appl Microbiol Biotechnol. 99(12):5203–5215. doi:10.1007/s00253­015­6440­5.

Hu J, Nagarajan D, Zhang Q, Chang JS, Lee DJ. 2018. Heterotrophic cultivation of microalgae for pigment production: A review. Biotechnol Adv. 36(1):54–67. doi:10.1016/j.biotechadv.2017.09.009.

Ip  PF,  Chen  F.  2005.  Employment of reactive oxygen species to enhance astaxanthin  forma­tion in Chlorella zofingiensis in heterotrophic culture. Process Biochem. 40(11):3491–3496. doi:10.1016/j.procbio.2005.02.014.

Kilian O, Benemann CS, Niyogi KK, Vick B. 2011. High­efficiency homologous recombination in the oil­producing alga Nannochloropsis sp. Proc Natl Acad Sci U.S.A 108(52):21265–21269. doi:10.1073/pnas.1105861108.

Kobayashi M. 2003. Astaxanthin biosynthesis enhanced by reactive oxygen species in the green alga Haema­ tococcus pluvialis. Biotechnol Bioprocess Eng. 8(6):322–330. doi:10.1007/BF02949275.

Kobayashi M, Hirai N, Kurimura Y, Ohigashi H, Tsuji Y. 1997. Abscisic acid­dependent algal morpho­ genesis in the unicellular green alga Haematococ­cus pluvialis. Plant Growth Regul. 22(2):79–85. doi:10.1023/A:1005862809711.

Kobayashi M, Kakizono  T,  Nagai  S.  1993.  En­hanced carotenoid biosynthesis by oxidative stress in acetate­induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl Environ Microbiol. 59(3):867–873. doi:10.1128/aem.59.3.867­873.1993.

Lafarga T, Clemente I, Garcia­Vaquero M. 2020. Carotenoids from microalgae. In: C Galanakis, editor,    Carotenoids: Properties, Processing and Applications. Academic Press. p. 149–187. doi:10.1016/B978­0­12­817067­0.00005­1.

Lee YK, Soh CW. 1991. Accumulation of Astax­anthin in Haematococcus Lacustris (Chlorophyta). J Phycol. 27(5):575–577. doi:10.1111/j.0022­ 3646.1991.00575.x.

Li  Y,  Sommerfeld  M,  Chen  F,  Hu  Q.  2010.   Effect of photon flux densities on regulation of caroteno­ genesis and cell viability of Haematococcus pluvi­alis (Chlorophyceae). J Appl Phycol. 22(3):253–263. doi:10.1007/s10811­009­9453­6.

Lichtenthaler HK. 1987. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods Enzymol. 148(C):350–382. doi:10.1016/0076­ 6879(87)48036­1.

Liu J, Sun Z, Gerken H,  Liu  Z,  Jiang  Y,  Chen  F.  2014. Chlorella zofingiensis as an alternative microalgal producer of astaxanthin: Biology and in­dustrial potential. Mar Drugs 12(6):3487–3515. doi:10.3390/md12063487.

Liu Z, Liu C, Hou Y, Chen S, Xiao D, Zhang J, Chen F. 2013. Isolation and characterization of a  ma­ rine microalga for biofuel production with astax­anthin as a co­product. Energies 6(6):2759–2772. doi:10.3390/en6062759.

Lorenz RT, Cysewski GR. 2000. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol. 18(4):160–167. doi:10.1016/S0167­7799(00)01433­5.

Ma R, Chen F. 2001. Induction of astaxanthin forma­tion in the green microalga Chlorococcum sp. by re­ active oxygen species (ROS) under mixotrophic con­ditions of growth. In: F Chen, Y Jiang, editors, Al­gae and their biotechnological potential. Netherlands: Springer. p. 121–126.

Mittler R. 2002. Oxidative stress,  antioxidants and stress tolerance. Trends Plant Sci. 7(9):405–410. doi:10.1016/S1360­1385(02)02312­9.

Nakano T, Tosa M, Takeuchi M. 1995. Improvement of Biochemical Features in Fish Health by Red Yeast and Synthetic Astaxanthin. J Agric Food Chem. 43(6):1570–1573. doi:10.1021/jf00054a029.

Orosa M, Franqueira D, Cid A, Abalde J. 2001. Carotenoid accumulation in Haematococcus pluvialis in mixotrophic growth. Biotechnol Lett. 23(5):373– 378. doi:10.1023/A:1005624005229.

Rabinowitch HD, Privalle CT, Fridovich I. 1987. Ef­fects of paraquat on the green alga Dunaliella salina: Protection by the mimic of superoxide dismutase, desferal­Mn(IV). Free Radic Biol Med. 3(2):125– 131. doi:10.1016/S0891­5849(87)80007­2.

Raman V, Ravi S. 2011. Effect of salicylic acid and methyl jasmonate on antioxidant systems of Haematococcus pluvialis. Acta Physiol Plant. 33(3):1043– 1049. doi:10.1007/s11738­010­0623­6.

Shaish A, Avron M, Pick U, Ben­Amotz A. 1993. Are active oxygen species involved in induction of β­ carotene in Dunaliella bardawil? Planta 190(3):363– 368. doi:10.1007/BF00196965.

Tharek A, Jamaluddin H, Salleh  M,  Yahya  N,  Kaha  M, Hara H, Iwamoto K, Mohamad S. 2020a. Astaxanthin production by tropical microalgae strains isolated from environment in Malaysia. Asian J Microbiol Biotechnol Environ Sci. 22(1):168–173. doi:10.6084/m9.figshare.12972881.v1.

Tharek A, Yahya A, Salleh MM, Jamaluddin H, Yoshizaki S, Dolah R, Hara H, Iwamoto K, Mohamad SE. 2020b.   Improvement of astaxanthin production in Coelastrum sp. by optimization using taguchi method. Appl Food Biotechnol. 7(4):205–214. doi:10.22037/afb.v7i4.29697.

Úbeda B, Gálvez JÁ, Michel M, Bartual A. 2017. Microalgae cultivation in urban wastewater: Coelastrum cf. pseudomicroporum as a novel carotenoid source and a potential microalgae har­ vesting tool. Bioresource Technol. 228:210–217. doi:10.1016/j.biortech.2016.12.095.

Young AJ. 1991. The photoprotective role of carotenoids in higher plants. Physiol Plant 83(4):702–708. doi:10.1111/j.1399­3054.1991.tb02490.x.



DOI: https://doi.org/10.22146/ijbiotech.54092

Article Metrics

Abstract views : 280 | views : 212

Refbacks

  • There are currently no refbacks.


Copyright (c) 2020 The Author(s)

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.