Exploiting the potential of Cyanidiales as a valuable resource for biotechnological applications

Figures & data

Figure 1. Graphic illustrating the biotechnological potential of Galdieria and Cyanidioschyzon. The remediation of waste streams (wastewater, flue gas, organic C) allows a valorization to products, such as pigments, lipids and polysaccharides. A toolbox for genetic engineering will render Cyanidioschyzon a heterologous expression platform.

Table 1. Accessibility of Galdieria and Cyanidioschyzon for biotechnological applications.

	Galdieria	Cyanidioschyzon	References
Heterotrophic growth	Yes	Yes	Gross & Schnarrenberger, 1995; Oesterhelt et al., 1999; Schonknecht et al., 2013; Moriyama et al., 2015; Sloth et al., 2017
C-PC production	Yes	Yes	Schmidt et al., 2005; Sloth et al., 2006, Sloth et al., 2017; Graverholt & Eriksen, 2007; Wan et al., 2016; Carfagna et al., 2018; Wang et al., 2019; Rahman et al., 2020
C-PC extraction	Yes	Yes	Sørensen et al., 2013; Moon et al., 2014; Rahman et al., 2017; Imbimbo et al., 2019
Waste stream treatment	Yes	N.A.	Kurano et al., 1995; Selvaratnam et al., 2014; Minoda et al., 2015; Vítová et al., 2019
Human food and health	Yes	N.A.	Graziani et al., 2013; Carfagna et al., 2015; Bottone et al., 2018; Massa et al., 2019; Modeste et al., 2019
Floridoside	Yes	N.A.	Martinez-Garcia & van der Maarel, 2016
Genome sequences	Yes	Yes	Ohta et al., 1998; 2003; Matsuzaki et al., 2004; Barbier et al., 2005; Schonknecht et al., 2013; Rossoni et al., 2019a
Auxotrophic mutant strains	N.A.	Yes	Minoda et al., 2004
Nuclear transformation	N.A.	Yes	Ohnuma et al., 2008; Fujiwara et al., 2013
Selective markers	N.A.	Yes	Moriyama et al., 2015; Fujiwara et al., 2017; 2015; 2013
Expression vectors	N.A.	Yes	Ohnuma et al., 2008
Stable expression vectors	N.A.	N.A.

Gross, W., & Schnarrenberger, C. (1995). Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant & Cell Physiology, 36, 633–638.

 Google Scholar

Oesterhelt, C., Schnarrenberger, C., & Gross, W. (1999). Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. European Journal of Phycology, 34, 271–277.

 Google Scholar

Schonknecht, G., Chen, W.-H., Ternes, C. M., Barbier, G. G., Shrestha, R. P., Stanke, M., … Weber, A. P. M. (2013). Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science (80-), 339, 1207–1210.

 Google Scholar

Moriyama, T., Mori, N., & Sato, N. (2015). Activation of oxidative carbon metabolism by nutritional enrichment by photosynthesis and exogenous organic compounds in the red alga Cyanidioschyzon merolae: Evidence for heterotrophic growth. Springerplus, 4, 559.

 Google Scholar

Sloth, J. K., Jensen, H. C., Pleer, D., & Eriksen, N. T. (2017). Growth and phycocyanin synthesis in the heterotrophic microalga Galdieria sulphuraria on substrates made of food waste from restaurants and bakeries. Bioresource Technology, 238, 296–305.

 Google Scholar

Schmidt, R. A., Wiebe, M. G., & Eriksen, N. T. (2005). Heterotrophic high cell-density fed-batch cultures of the phycocyanin-producing red alga Galdieria sulphuraria. Biotechnology and Bioengineering, 90, 77–84.

 Google Scholar

Sloth, J. K., Wiebe, M. G., & Eriksen, N. T. (2006). Accumulation of phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzyme and Microbial Technology, 38, 168–175.

 Google Scholar

Graverholt, O. S., & Eriksen, N. T. (2007). Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Applied Microbiology and Biotechnology, 77, 69–75.

 Google Scholar

Wan, M., Wang, Z., Zhang, Z., Wang, J., Li, S., Yu, A., & Li, Y. (2016). A novel paradigm for the high-efficient production of phycocyanin from Galdieria sulphuraria. Bioresource Technology, 218, 272–278.

 Google Scholar

Carfagna, S., Landi, V., Coraggio, F., Salbitani, G., Vona, V., Pinto, G., … Ciniglia, C. (2018). Different characteristics of C-phycocyanin (C-PC) in two strains of the extremophilic Galdieria phlegrea. Algal Research, 31, 406–412.

 Google Scholar

Wang, H., Zhang, Z., Wan, M., Wang, R., Huang, J., Zhang, K., Guo, J., Bai, W., & Li, Y. (2019).Comparative study on light attenuation models of Galdieria sulphuraria for efficient production of phycocyanin. Journal of Applied Phycology, 37, 165-174.

 Google Scholar

Razzak, S. A., Hossain, M. M., Lucky, R. A., Bassi, A. S., & de Lasa, H. (2013). Integrated CO2 capture, wastewater treatment and biofuel production by microalgae culturing—A review. Renewable and Sustainable Energy Reviews, 27, 622–653.

 Google Scholar

Sørensen, L., Hantke, A., & Eriksen, N. T. (2013). Purification of the photosynthetic pigment C-phycocyanin from heterotrophic Galdieria sulphuraria. Journal of the Science of Food and Agriculture, 93, 2933–2938.

 Google Scholar

Moon, M., Mishra, S. K., & Kim, C. W. (2014). Isolation and characterization of thermostable phycocyanin from Galdieria sulphuraria. Korean Journal of Chemical Engineering, 29, 490–495.

 Google Scholar

Rahman, D. Y., Sarian, F. D., van Wijk, A., Martinez-Garcia, M., & van der Maarel, M. J. E. C. (2017). Thermostable phycocyanin from the red microalga Cyanidioschyzon merolae, a new natural blue food colorant. Journal of Applied Phycology, 29, 1233–1239.

 Google Scholar

Imbimbo, P., Romanucci, V., Pollio, A., Fontanarosa, C., Amoresano, A., Zarrelli, A., & Monti, D. M. (2019). A cascade extraction of active phycocyanin and fatty acids from Galdieria phlegrea. Applied Microbiology and Biotechnology, 103, 9455–9464.

 Google Scholar

Kurano, N., Ikemoto, H., Miyashita, H., Hasegawa, T., Hata, H., & Miyachi, S. (1995). Fixation and utilization of carbon dioxide by microalgal photosynthesis. Energy Conversion and Management, 36, 689–692.

 Google Scholar

Selvaratnam, T., Pegallapati, A. K., Montelya, F., Rodriguez, G., Nirmalakhandan, N., Van Voorhies, W., & Lammers, P. J. (2014). Evaluation of a thermo-tolerant acidophilic alga, Galdieria sulphuraria, for nutrient removal from urban wastewaters. Bioresource Technology, 156, 395–399.

 Google Scholar

Minoda, A., Sawada, H., Suzuki, S., Miyashita, S.-I., Inagaki, K., Yamamoto, T., & Tsuzuki, M. (2015). Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Applied Microbiology and Biotechnology, 99, 1513–1519.

 Google Scholar

Vítová, M., Čížková, M., & Zachleder, V. (2019). Lanthanides and algae. In Lanthanides. IntechOpen.

 Google Scholar

Graziani, G., Schiavo, S., Nicolai, M. A., Buono, S., Fogliano, V., Pinto, G., & Pollio, A. (2013). Microalgae as human food: chemical and nutritional characteristics of the thermo-acidophilic microalga Galdieria sulphuraria. Food Function, 4, 144–152.

 Google Scholar

Carfagna, S., Napolitano, G., Barone, D., Pinto, G., Pollio, A., & Venditti, P. (2015). Dietary supplementation with the microalga Galdieria sulphuraria (rhodophyta) reduces prolonged exercise-induced oxidative stress in rat tissues. Oxidative Medicine and Cellular Longevity, 2015, 732090.

 Google Scholar

Bottone, C., Camerlingo, R., Miceli, R., Salbitani, G., Sessa, G., Pirozzi, G., & Carfagna, S. (2018). Antioxidant and anti-proliferative properties of extracts from heterotrophic cultures of Galdieria sulphuraria. Natural Product Research, 1–5.

 Google Scholar

Massa, M., Buono, S., Langellotti, A. L., Martello, A., Russo, G. L., Troise, D. A., Sacchi, R., Vitaglione, P., & Fogliano, V. (2019). Biochemical composition and in vitro digestibility of Galdieria sulphuraria grown on spent cherry-brine liquid. New Biotechnol ogy, 53, 9–15. (2019).

 Google Scholar

Modeste, V., Brient, A., Thirion-Delalande, C., Forster, R., Aguenou, C., Griffiths, H., & Cagnac, O. (2019). Safety evaluation of Galdieria high-protein microalgal biomass. Toxicology Research and Application, 3.

 Google Scholar

Martinez-Garcia, M., & van der Maarel, M. J. E. C. (2016). Floridoside production by the red microalga Galdieria sulphuraria under different conditions of growth and osmotic stress. AMB Express, 6, 71.

 Google Scholar

Ohta, N., Sato, N., & Kuroiwa, T. (1998). Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Research, 26, 5190–5198.

 Google Scholar

Ohta, N., Matsuzaki, M., & Misumi, O. (2003). Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Research, 10, 67–77.

 Google Scholar

Matsuzaki, M., Misumi, O., Shin-I, T., Maruyama, S., Takahara, M., Miyagishima, S.-Y., … Kuroiwa, T. (2004). Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature, 428, 653–657.

 Google Scholar

Barbier, G., Oesterhelt, C., Larson, M. D., Halgren, R. G., Wilkerson, C., Garavito, R. M., … Weber, A. P. M. (2005). Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiology, 137, 460–474.

 Google Scholar

Rossoni, A. W., Price, D. C., Seger, M., et al. (2019a). The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions. Elife, 8.

 Google Scholar

Minoda, A., Sakagami, R., Yagisawa, F., Kuroiwa, T., & Tanaka, K. (2004). Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant and Cell Physiology, 45, 667–671.

 Google Scholar

Ohnuma, M., Yokoyama, T., Inouye, T., Sekine, Y., & Tanaka, K. (2008). Polyethylene glycol (PEG)-mediated transient gene expression in a red alga, Cyanidioschyzon merolae 10D. Plant and Cell Physiology, 49, 117–120.

 Google Scholar

Fujiwara, T., Ohnuma, M., Yoshida, M., Kuroiwa, T., & Hirano, T. (2013). Gene targeting in the red alga Cyanidioschyzon merolae: Single- and multi-copy insertion using authentic and chimeric selection markers. PloS One, 8, e73608.

 Google Scholar

Fujiwara, T., Ohnuma, M., Kuroiwa, T., Ohbayashi, R., Hirooka, S., & Miyagishima, S.-Y. (2017). Development of a double nuclear gene-targeting method by two-step transformation based on a newly established chloramphenicol-selection system in the red alga Cyanidioschyzon merolae. Frontiers in Plant Science, 8, 343. PM - 28352279 M4 - Citavi.

 Google Scholar

Fujiwara, T., Kanesaki, Y., Hirooka, S., Era, A., Sumiya, N., Yoshikawa, H., & Miyagishima, S.-Y. (2015). A nitrogen source-dependent inducible and repressible gene expression system in the red alga Cyanidioschyzon merolae. Frontiers in Plant Science, 6, 657.

 Google Scholar