Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications

Veronica da Silva Ferreira1, Celso Sant’Anna1
1Laboratory of Microscopy Applied to Life Science - Lamav, National Institute of Metrology, Quality and Technology – Inmetro, Duque de Caxias, Brazil

Tóm tắt

Chlorophyll is a commercially important natural green pigment responsible for the absorption of light energy and its conversion into chemical energy via photosynthesis in plants and algae. This bioactive compound is widely used in the food, cosmetic, and pharmaceutical industries. Chlorophyll has been consumed for health benefits as a nutraceutical agent with antioxidant, anti-inflammatory, antimutagenic, and antimicrobial properties. Microalgae are photosynthesizing microorganisms which can be extracted for several high-value bioproducts in the biotechnology industry. These microorganisms are highly efficient at adapting to physicochemical variations in the local environment. This allows optimization of culture conditions for inducing microalgal growth and biomass production as well as for changing their biochemical composition. The modulation of microalgal culture under controlled conditions has been proposed to maximize chlorophyll accumulation. Strategies reported in the literature to promote the chlorophyll content in microalgae include variation in light intensity, culture agitation, and changes in temperature and nutrient availability. These factors affect chlorophyll concentration in a species-specific manner; therefore, optimization of culture conditions has become an essential requirement. This paper provides an overview of the current knowledge on the effects of key environmental factors on microalgal chlorophyll accumulation, focusing on small-scale laboratory experiments.

Tài liệu tham khảo

Abad R (1996) Therapeutic and cosmetic compositions for treatment of skin. United States patent US 5538740A Azizullah A, Rehman ZU, Ali I, Murad W, Muhammad N, Ullah W, Häder D (2014) Chlorophyll derivatives can be an efficient weapon in the fight against dengue. Parasitol Res 113:4321–4326 Bachvaroff TR, Puerta MVS, Delwiche CF (2005) Chlorophyll c—containing plastid relationships based on analyses of a multigene data set with all four Chromalveolate Lineages. Mol Biol Evol 22:1772–1782 Bhatnagar A, Chinnasamy S, Singh M, Das KC (2011) Renewable biomass production by mixotrophic algae in the presence of various carbon sources and wastewaters. Appl Energy 88:3425–3431 Bonente G, Pippa S, Castellano S, Bassi R, Ballottari M (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J Biol Chem 287:5833–5847 Cakmak T, Angun P, Demiray YE, Ozkan AD, Elibol Z, Tekinay T (2012) Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng 109:1947–1957 Carvalho AP, Monteiro CM, Malcata FX (2009) Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavlova lutheri. J Appl Phycol 21:543–552 Chauhan UK, Pathak N (2010) Effect of different conditions on the production of chlorophyll by Spirulina platensis. J Algal Biomass Utln 1:89–99 Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516 Chen M (2014) Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu Rev Biochem 83:26.1–26.24 Chen M, Schliep M, Willows RD, Cai Z, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329:1318–1319 Chen M, Li J, Dai X, Sun Y, Chen F (2011) Effect of phosphorus and temperature on chlorophyll a contents and cell sizes of Scenedesmus obliquus and Microcystis aeruginosa. Limnology 12:187–192 Chen M, Li Y, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. FEBS Lett 586:3249–3254 Chen S, Chen M, Wang Z, Qiu W, Wang J, Shen Y, Wang Y, Ge S (2016) Toxicological effects of chlorpyrifos on growth, enzyme activity and chlorophyll a synthesis of freshwater microalgae. Environ Toxicol Pharmacol 45:179–186 Darley WM (1982) Chapter 3: phytoplankton: environmental factors affecting growth. In: Darley WM (ed) Algal biology: a physiological approach. Blackwell Scientific Publications, Belgium, pp 921–952 Dean AP, Sigee DC, Estrada B, Pittman JK (2010) Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae. Bioresour Technol 101:4499–4507 Encarnação T, Burrows HD, Pais AC, Campos MG, Kremer A (2012) Effect of N and P on the uptake of magnesium and iron and on the production of carotenoids and chlorophyll by the microalgae Nannochloropsis sp. J Agric Sci Technol A 2:824–832 Esakkimuthu S, Krishnamurthy V, Govindarajan R, Swaminathan K (2016) Zugmentation and starvation of calcium, magnesium, phosphate on lipid production of Scenedesmus obliquus. Biomass Bioenergy 88:126–134 Fan J, Cui Y, Wan M, Wang W, Li Y (2014) Lipid accumulation and biosynthesis genes response of the oleaginous Chlorella pyrenoidosa under three nutrition stressors. Biotechnol Biofuels 7:17 Ferreira VS, Pinto RF, Sant’Anna C (2016) Low light intensity and nitrogen starvation modulate the chlorophyll content of Scenedesmus dimorphus. J Appl Microbiol 120:661–670 Fujimoto Y, Sakamoto J (1955) The influence of magnesium deficiency on the growth of chlorella. Bull Agric Chem Soc Jpn 19:253–257 Gaur N, Bhardwaj V, Rathi M (2013) Heavy metals and their effects. PR:BioMedRx: An Int J 1:928–933 George M, Reddick RS (2013) Chlorophyll cooling agent for synthetic turf components. United States patent US 20130034671A1 George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus—a potential strain for bio-fuel production. Bioresour Technol 171:367–374 Ghaeni M, Roomiani L, Moradi Y (2015) Evaluation of carotenoids and chlorophyll as catural resources for food in Spirulina microalgae. Appl Food Biotechnol 2:39–44 Ghafari M, Rashidi B, Haznedaroglu BZ (2016) Effects of macro and micronutrients on neutral lipid accumulation in oleaginous microalgae. Biofuels. doi:10.1080/17597269.2016.1221644 Gim GH, Ryu J, Kim MJ, Kim PI, Kim SW (2016) Effects of carbon source and light intensity on the growth and total lipid production of three microalgae under different culture conditions. J Ind Microbiol Biotechnol 43:605–616 Halfhide T, Åkerstrøm A, Lekang OI, Gislerød HR, Ergas SJ (2014) Production of algal biomass, chlorophyll, starch and lipids using aquaculture wastewater under axenic and non-axenic conditions. Algal Res 6:152–159 Harun R, Singh M, Forde GM, Danquah MK (2010) Bioprocess engineering of microalgae to produce a variety of consumer products. Renew Sustain Energy Rev 14:1037–1047 He Q, Yang H, Wua L, Hua C (2015) Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresour Technol 191:219–228 Hiramoto T, Takeuchi R (2014) Deodorant composition. United States patent US 8778320B2 Ho M, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353. doi:10.1126/science.aaf9178 Humphrey AM (1980) Chlorophyll. Food Chem 5:57–67 Jerez CG, Malapascua JR, Sergejevová M, Figueroa FL (2016) Effect of nutrient starvation under high irradiance on lipid and starch accumulation in Chlorella fusca (Chlorophyta). Mar Biotechnol 18:24–36 Kagalou I, Beza P, Perdikaris C, Petridis D (2002) Effects of cooper and lead on microalgae (Isochrysis galbana) growth. Fresenius Environ Bull 11:233–236 Kennedy SR (1940) The influence of magnesium deficiency, chlorophyll concentration, and heat treatments on the rate of photosynthesis of Chlorella. Am J Bot 27:68–73 Kong W, Song H, Cao Y, Yang H, Hua S, Xia C (2011) The characteristics of biomass production, lipid accumulation and chlorophyll biosynthesis of Chlorella vulgaris under mixotrophic cultivation. Afr J Biotechnol 10:11620–11630 Lanfer-Marquez UM, Barros RMC, Sinnecker P (2005) Antioxidant activity of chlorophylls and their derivatives. Food Res Int 38:885–891 Li WK (1980) Temperature adaptation in phytoplankton: cellular and photosynthetic characteristics. Prim Product Sea (Springer) 19:259–279 Li Y, Chen M (2015) Novel chlorophylls and new directions in photosynthesis research. Funct Plant Biol 42:493–501 Li M, Hu C, Zhu Q, Chen L, Kong Z, Liu Z (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572 Liang K, Zhang Q, Gu M, Cong W (2013) Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp. J Appl Phycol 25:311–318 Lourenço SO, Barbarino E, Lavín PL, Marquez UML, Aidar E (2004) Distribution of intracellular nitrogen in marine microalgae: calculation of new nitrogen-to-protein conversion factors. Eur J Phycol 39:17–32 Lowrey J, Brooks MS, McGinn PJ (2015) Heterotrophic and mixotrophic cultivation of microalgae for biodiesel production in agricultural wastewaters and associated challenges—a critical review. J Appl Phycol 27:1485–1498 Lv J, Cheng L, Xu X, Zhang L, Chen H (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804 Manning WM, Strait HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151:1–19 Martínez ME, Sánchez S, Jimánez JM, Yousfi FE, Muñoz L (2000) Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus. Bioresour Technol 73:263–272 Mohsenpour SF, Richards B, Willoughby N (2012) Spectral conversion of light for enhanced microalgae growth rates and photosynthetic pigment production. Bioresour Technol 125:75–81 Mulders KJM, Lamers PP, Martens DE, Wijffels RH (2014) Phototrophic pigment production with microalgae: biological constraints and opportunities. J Phycol 50:229–242 Rieblinger K, Moosheimer U, Ziegleder G (2003) Transparent or partially transparent packaging materials that are coloured by means of colours. United States patent US 20030138653A1 Roopnarain A, Gray VM, Sym SD (2014) Phosphorus limitation and starvation effects on cell growth and lipid accumulation in Isochrysis galbana U4 for biodiesel production. Bioresour Technol 156:408–411 Rose B (2000) Compositions containing chlorophyll derivatives for permanent waving of hair. United States patent US 006024949A Schiraldi RJ (1964) Chlorophyll dentifrice compositions. United States patent US 3137632A Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553 Song BH, Lee DH, Kim BC, Ku SH, Park EJ, Kwon IH, Kim KH, Kim KJ (2014) Photodynamic therapy using chlorophyll—a in the treatment of acne vulgaris: a randomized, single-blind, split-face study. J Am Acad Dermatol 71:764–771 Subramoniam A, Asha VV, Nair SA, Sasidharan SP, Sureshkumar PK, Rajendran KN, Karunagaran D, Ramalingam K (2012) Chlorophyll revisited: anti-inflammatory activities of chlorophyll a and inhibition of expression of TNF-α gene by the same. Inflammation 35:959–966 Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum. Plant Physiol 95:1089–1095 Timberlake CF, Henry BS (1986) Plant pigments as natural food colours. Endeavour 10:31–36 Vesenick DC, Paula NA, Niwa AM, Mantovani MS (2012) Evaluation of the effects of chlorophyllin on apoptosis induction, inhibition of cellular proliferation and mRNA expression of CASP8, CASP9, APC and b-catenin. Curr Res J Biol Sci 4:315–322 Zeligman I (1949) Topical chlorophyll therapy in the dermatoses. J Invest Dermatol 13:111–113 Zhang L, He M, Liu J (2014) The enhancement mechanism of hydrogen photoproduction in Chlorella protothecoides under nitrogen limitation and sulfur deprivation. Int J Hydrogen Energy 39:8969–8976