Astaxanthin Production by Newly Isolated Rhodosporidium toruloides: Optimization of Medium Compositions by Response Surface Methodology
Astaxanthin is a valuable carotenoid pigment, which has been extensively used in various industries. In this study, Rhodosporidium toruloides was first used as a new microbial source for producing natural astaxanthin. Various carbon, nitrogen, and mineral sources were evaluated for their effect on astaxanthin production of R. toruloides. Response surface methodology (RSM) was then used to optimize the medium compositions for maximizing the astaxanthin concentration. Among the examined nutrients, glucose, peptone, and KH2PO4 were the most efficient carbon, nitrogen, and mineral source for astaxanthin production, respectively. Through RSM, a maximum astaxanthin concentration of 927.11 µg l-1 was obtained by using Hansen broth containing 83.74 g l-1 glucose, 20.01 g l-1 peptone, and 6.19 g l-1 KH2PO4. This study suggested that R. toruloides is a promising candidate to produce natural astaxanthin.
An GH, Bielich J, Auerbach R, Johnson EA (1991). Isolation and characterization of carotenoid hyperproducing mutants of yeast by flow cytometry and cell sorting. Nature Biotechnology 9:70-73.
Batghare AH, Singh N, Moholkar VS (2018). Investigations in ultrasound-induced enhancement of astaxanthin production by wild strain Phaffia rhodozyma MTCC 7536. Bioresource Technology 254:166-173.
Chen JH, Liu L, Wei D (2017). Enhanced production of astaxanthin by Chromochloris zofingiensis in a microplate-based culture system under high light irradiation. Bioresource Technology 245:518-529.
Choi YE, Yun YS, Park JM (2002). Evaluation of factors promoting astaxanthin production by a unicellular green alga, Haematococcus pluvialis, with fractional factorial design. Biotechnology Progress 18:1170-1175.
Christian D, Zhang J, Sawdon AJ, Peng CA (2018). Enhanced astaxanthin accumulation in Haematococcus pluvialis using high carbon dioxide concentration and light illumination. Bioresource Technology 256:548-551.
Dermiki M, Bourquin AL, Jauregi P (2010). Separation of astaxanthin from cells of Phaffia rhodozyma using colloidal gas aphrons in a flotation column. Biotechnology Progress 26:477-487.
Dias C, Silva C, Freitas C, Reis A, Da Silva TL (2016). Effect of medium pH on Rhodosporidium toruloides NCYC 921 carotenoid and lipid production evaluated by flow cytometry. Applied Biochemistry and Biotechnology 179:776-787.
Díaz T, Fillet S, Campoy S, Vázquez R, Viña J, Murillo J, Adrio JL (2018). Combining evolutionary and metabolic engineering in Rhodosporidium toruloides for lipid production with non-detoxified wheat straw hydrolysates. Applied Microbiology and Biotechnology 102:3287-3300.
Dom?nguez-Bocanegra A, Legarreta IG, Jeronimo FM, Campocosio AT (2004). Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis. Bioresource Technology 92:209-214.
Domínguez-Bocanegra A, Ponce-Noyola T, Torres-Muñoz J (2007). Astaxanthin production by Phaffia rhodozyma and Haematococcus pluvialis: a comparative study. Applied Microbiology and Biotechnology 75:783-791.
Fang TJ, Cheng YS (1993). Improvement of astaxanthin production by Phaffia rhodozyma through mutation and optimization of culture conditions. Journal of Fermentation and Bioengineering 75:466-469.
Fang TJ, Wang JM (2002). Extractability of astaxanthin in a mixed culture of a carotenoid over-producing mutant of Xanthophyllomyces dendrorhous and Bacillus circulans in two-stage batch fermentation. Process Biochemistry 37:1235-1245.
Freitas C, Nobre B, Gouveia L, Roseiro J, Reis A, da Silva TL (2014a). New at-line flow cytometric protocols for determining carotenoid content and cell viability during Rhodosporidium toruloides NCYC 921 batch growth. Process Biochemistry 49:554-562.
Freitas C, Parreira TM, Roseiro J, Reis A, da Silva TL (2014b). Selecting low-cost carbon sources for carotenoid and lipid production by the pink yeast Rhodosporidium toruloides NCYC 921 using flow cytometry. Bioresource Technology 158:355-359.
González-García Y, Rábago-Panduro LM, French T, Camacho-Córdova DI, Gutiérrez-González P, Córdova J (2017). High lipids accumulation in Rhodosporidium toruloides by applying single and multiple nutrients limitation in a simple chemically defined medium. Annals of Microbiology 67:519-527.
Guyomarc’h F, Binet A, Dufossé L (2000). Production of carotenoids by Brevibacterium linens: variation among strains, kinetic aspects and HPLC profiles. Journal of Industrial Microbiology and Biotechnology 24:64-70.
Ide T, Hoya M, Tanaka T, Harayama S (2012). Enhanced production of astaxanthin in Paracoccus sp. strain N-81106 by using random mutagenesis and genetic engineering. Biochemical Engineering Journal 65:37-43.
Ip PF, Chen F (2005). Production of astaxanthin by the green microalga Chlorella zofingiensis in the dark. Process Biochemistry 40:733-738.
Ip PF, Wong KH, Chen F (2004). Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochemistry 39:1761-1766.
Kelley CE, Harmon AW (1972). Method of determining carotenoid contents of Alaska pink shrimp and representative values for several shrimp products. Fishery Bulletin 70:11-17.
Kiperstok AC, Sebestyén P, Podola B, Melkonian M (2017). Biofilm cultivation of Haematococcus pluvialis enables a highly productive one-phase process for astaxanthin production using high light intensities. Algal Research 21:213-222.
Li J, Zhu D, Niu J, Shen S, Wang G (2011). An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnology Advances 29:568-574.
Lin X, Gao N, Liu S, Zhang S, Song S, Ji C, Dong X, Su Y, Zhao ZK, Zhu B (2017a). Characterization the carotenoid productions and profiles of three Rhodosporidium toruloides mutants from Agrobacterium tumefaciens-mediated transformation. Yeast 34:335-342.
Lin YJ, Chang JJ, Lin HY, Thia C, Kao YY, Huang CC, Li WH (2017b). Metabolic engineering a yeast to produce astaxanthin. Bioresource Technology 245:899-905.
Liu ZQ, Zhang JF, Zheng YG, Shen YC (2008). Improvement of astaxanthin production by a newly isolated Phaffia rhodozyma mutant with low?energy ion beam implantation. Journal of Applied Microbiology 104:861-872.
Ma R, Thomas-Hall SR, Chua ET, Alsenani F, Eltanahy E, Netzel ME, … Schenk PM (2018). Gene expression profiling of astaxanthin and fatty acid pathways in Haematococcus pluvialis in response to different LED lighting conditions. Bioresource Technology 250:591-602.
Mao X, Wu T, Sun D, Zhang Z, Chen F (2018). Differential responses of the green microalga Chlorella zofingiensis to the starvation of various nutrients for oil and astaxanthin production. Bioresource Technology 249:791-798.
Marques IP, Batista AP, Coelho A, da Silva TL (2018). Co-digestion of Rhodosporidium toruloides biorefinery wastes for biogas production. Process Biochemistry 64:221-227.
Montanti J, Nghiem NP, Johnston DB (2011). Production of astaxanthin from cellulosic biomass sugars by mutants of the yeast Phaffia rhodozyma. Applied Biochemistry and Biotechnology 164:655-665.
Nahidian B, Ghanati F, Shahbazi M, Soltani N (2018). Effect of nutrients on the growth and physiological features of newly isolated Haematococcus pluvialis TMU1. Bioresource Technology 255:229-237.
Nguyen HC, Liang SH, Chen SS, Su CH, Lin JH, Chien CC (2018a). Enzymatic production of biodiesel from insect fat using methyl acetate as an acyl acceptor: optimization by using response surface methodology. Energy Conversion and Management 158:168-175.
Nguyen HC, Su CH, Yu YK, Huong DTM (2018b). Sugarcane bagasse as a novel carbon source for heterotrophic cultivation of oleaginous microalga Schizochytrium sp. Industrial Crops and Products 121:99-105.
Johnson EA, Schroeder SW (1996). Microbial carotenoids. In: Fiechter A (Ed). Advances in biochemical engineering biotechnology. Springer, New York, pp 119-178.
Pan-utai W, Parakulsuksatid P, Phomkaivon N (2017). Effect of inducing agents on growth and astaxanthin production in Haematococcus pluvialis: organic and inorganic. Biocatalysis and Agricultural Biotechnology 12:152-158.
Panis G, Carreon JR (2016). Commercial astaxanthin production derived by green alga Haematococcus pluvialis: a microalgae process model and a techno-economic assessment all through production line. Algal Research 18:175-190.
Parreira TM, Freitas C, Reis A, Roseiro J, da Silva TL (2015). Carbon concentration and oxygen availability affect lipid and carotenoid production by carob pulp syrup?grown Rhodosporidium toruloides NCYC 921. Engineering in Life Sciences 15:815-823.
Ram??rez J, Gutierrez H, Gschaedler A (2001). Optimization of astaxanthin production by Phaffia rhodozyma through factorial design and response surface methodology. Journal of Biotechnology 88:259-268.
Saenge C, Cheirsilp B, Suksaroge TT, Bourtoom T (2011). Potential use of oleaginous red yeast Rhodotorula glutinis for the bioconversion of crude glycerol from biodiesel plant to lipids and carotenoids. Process Biochemistry 46:210-218.
Sajjad W, Ahmad M, Khan S, Ilyas S, Hasan F, Celik C, … Shah AA (2017). Radio-protective and antioxidative activities of astaxanthin from newly isolated radio-resistant bacterium Deinococcus sp. strain WMA-LM9. Annalsof Microbiology 67:443-455.
Sarada R, Tripathi U, Ravishankar G (2002). Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions. Process Biochemistry 37:623-627.
Singh G, Jawed A, Paul D, Bandyopadhyay KK, Kumari A, Haque S (2016). Concomitant production of lipids and carotenoids in Rhodosporidium toruloides under osmotic stress using response surface methodology. Frontiers in Microbiology 7:1686.
Stoklosa RJ, Johnston DB, Nghiem NP (2018). Utilization of sweet sorghum juice for the production of astaxanthin as a biorefinery co-product by Phaffia rhodozyma. ACS Sustainable Chemistry & Engineering 6:3124-3134.
Ukibe K, Hashida K, Yoshida N, Takagi H (2009). Metabolic engineering of Saccharomyces cerevisiae for astaxanthin production and oxidative stress tolerance. Applied and Environmental Microbiology 75:7205-7211.
Xie H, Zhou Y, Hu J, Chen Y, Liang J (2014). Production of astaxanthin by a mutant strain of Phaffia rhodozyma and optimization of culture conditions using response surface methodology. Annals of Microbiology 64:1473-1481.
Yaegashi J, Kirby J, Ito M, Sun J, Dutta T, Mirsiaghi M, … Tanjore D (2017). Rhodosporidium toruloides: a new platform organism for conversion of lignocellulose into terpene biofuels and bioproducts. Biotechnology for Biofuels 10:241.
Yamane Y, Higashida K, Nakashimada Y, Kakizono T, Nishio N (1997). Influence of oxygen and glucose on primary metabolism and astaxanthin production by Phaffia rhodozyma in batch and fed-batch cultures: kinetic and stoichiometric analysis. Applied and Environmental Microbiology 63:4471-4478.
Zhang C, Seow VY, Chen X, Too HP (2018). Multidimensional heuristic process for high-yield production of astaxanthin and fragrance molecules in Escherichia coli. Nature Communications 9:1858.
Zhou P, Xie W, Li A, Wang F, Yao Z, Bian Q, … Ye L (2017). Alleviation of metabolic bottleneck by combinatorial engineering enhanced astaxanthin synthesis in Saccharomyces cerevisiae. Enzyme and Microbial Technology 100:28-36.
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.