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Intraspecific variability among Chilean strains of the astaxanthin-producing microalga Haematococcus pluvialis (Chlorophyta): an opportunity for its genetic improvement by simple selection

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Abstract

The unicellular green alga Haematococcus pluvialis accumulates large quantities of astaxanthin, a highly valuable carotenoid pigment in the aquaculture, food, and pharmaceutical industries. Biological diversity within a species with a biotechnological interest allows applying strain selection procedures avoiding genetic manipulation. The aim of this study was to determine growth and carotenogenic capacity among 13 strains isolated from a latitudinal range throughout south-central and southern Chile, in order to know their biological diversity and biotechnological potential. Strains were isolated from rain pools located in public squares and cemeteries of the cities: Concepción, Valdivia, Osorno, Puerto Varas, and Castro. All the Chilean strains were more carotenogenic than the reference strain Steptoe. Physiological attributes differed greatly among the strains. Principal component analysis (PCA) of growth and carotenogenesis parameters grouped the strains into four groups, two of them composed by only one strain (CCM-UdeC-038 and CCM-UdeC-039). These latter strains were also the most carotenogenic ones, being strain CCM-UdeC-039 the one that accumulated the highest amount of astaxanthin (7 mg astaxanthin L−1 culture) associated to the highest total carotenoid content (1.1 % by dry biomass) and carotenoids/chlorophyll ratio (2.6). These results demonstrate that a great physiological diversity exists at intraspecific level in H. pluvialis (even among strains coming from the same geographical origin), which allows performing genetic improvement by means of simple selection of new strains from nature. Further research will be focused on finding out the culture conditions that optimize the astaxanthin production of the most promising strains.

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References

  • Behra R, Genoni GP, Joseph AL (1999) Effect of atrazine on growth, photosynthesis, and between-strain variability in Scenedesmus subspicatus (Chlorophyceae). Arch Environ Contam Toxicol 37:36–41

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (1992) Comparing carotenogenesis in Dunaliella and Haematococcus: implications for commercial production strategies. In: Villa TG, Abalde J (eds) Profiles on biotechnology. Universidad de Santiago de Compostela, Santiago de Compostela, pp 301–310

    Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis 1. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304

    Article  CAS  Google Scholar 

  • Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plantarum 108:111–117

    Article  CAS  Google Scholar 

  • Bubrick P (1991) Production of astaxanthin from Haematococcus. Bioresource Technol 38:237–239

    Article  CAS  Google Scholar 

  • Carvalho AP, Monteiro CM, Malcata FX (2009) Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavovla lutheri. J Appl Phycol 21:543–552

    Article  Google Scholar 

  • Chen Y, Li D, Lu W, Xing J, Hui B, Han Y (2003) Screening and characterization of astaxanthin-hyperproducing mutants of Haematococcus pluvialis. Biotechnol Lett 25:527–529

    Article  CAS  PubMed  Google Scholar 

  • Christiansen R, Lie O, Torrisen OJ (1995) Growth and survival of Atlantic salmon, Salmo salar L., fed different dietary levels of astaxanthin. First-feeding fry. Aquacult Nutr 1:189–198

    Article  Google Scholar 

  • Christiansen R, Torrissen OJ (1997) Effects of dietary astaxanthin supplementation on fertilization and egg survival in Atlantic salmon (Salmo salar L.). Aquaculture 153:51–62

    Article  CAS  Google Scholar 

  • Cifuentes AS, González M, Conejeros M, Dellarossa V, Parra O (1992) Growth and carotenogenesis in eight strains of Dunaliella salina Teodoresco from Chile. J Appl Phycol 4:111–118

    Article  CAS  Google Scholar 

  • Del Campo JA, Rodríguez H, Moreno J, Vargas MA, Rivas J, Guerrero MG (2004) Accumulation of astaxanthin and lutein in Chlorella zofingensis (Chlorophyta). Appl Microbiol Biot 64:848–854

    Article  Google Scholar 

  • Del Río E, Acién FG, García-Malea MC, Rivas J, Molina-Grima E, Guerrero MG (2005) Efficient one-step production of astaxanthin by the microalga Haematococcus pluvialis in continuous culture. Biotechnol Bioeng 91:808–15

    Article  PubMed  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG, González L, Tablada M, Robledo CW (2011) InfoStat versión. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina, http://www.infostat.com.ar

    Google Scholar 

  • Fujii K, Imazato E, Nakashima H, Ooi O, Saeki A (2006) Isolation of the non- fastidious microalga with astaxanthin-accumulating property and its potential for application to aquaculture. Aquaculture 262:285–293

    Article  Google Scholar 

  • Gallagher JC (1980) Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay. J Phycol 16:464–474

    Article  Google Scholar 

  • Gallagher JC (1982) Physiological variation and electrophoretic banding patterns of genetically different seasonal populations of Skeletonema costatum (Bacillariophyceae). J Phycol 18:148–162

    Article  CAS  Google Scholar 

  • Giannelli L, Yamada H, Katsuda T, Yamaji H (2015) Effects of temperature on the astaxanthin productivity and light harvesting characteristics of the green alga Haematococcus pluvialis. J Biosci Bioeng 119(3):345–350

    Article  CAS  PubMed  Google Scholar 

  • Gómez P, González M (2001) Genetic polymorphism in eight Chilean strains of the carotenogenic microalga Dunaliella salina Teodoresco (Chlorophyta). Biol Res 34:23–30

    Article  PubMed  Google Scholar 

  • Gómez P, González M (2004) Genetic variation among seven strains of Dunaliella salina (Chlorophyta) with industrial potential based on RAPD banding patterns and on nuclear ITS rDNA sequences. Aquaculture 233:149–162

    Article  Google Scholar 

  • Gómez P, González M (2005) The effect of temperature and irradiance on the growth and carotenogenic capacity of seven strains of Dunaliella salina (Chlorophyta) cultivated under laboratory conditions. Biol Res 38:151–162

    Article  PubMed  Google Scholar 

  • Gómez PI, Inostroza I, Pizarro M, Pérez J (2013) From genetic improvement to commercial-scale mass culture of a Chilean strain of the green microalga Haematococcus pluvialis with enhanced productivity of the red ketocarotenoid astaxanthin. AoB Plants 5:plt026

    Article  PubMed  PubMed Central  Google Scholar 

  • González MA, Cifuentes AS, Gómez PI (2009) Growth and total carotenoid content in four Chilean strains of Haematococcus pluvialis Flotow, under laboratory conditions. Gayana Bot 66:58–70

    Article  Google Scholar 

  • Guillard RRL (1973) Division rates. In: Stein JR (ed) Handbook of phycological methods. Culture Methods and Growth Measurements. Cambridge University Press, New York, pp 290–311

    Google Scholar 

  • Gutiérrez CL, Escobar C, Marshall SH (2012) Chloroplast genetic tool for the green microalgae Haematococcus pluvialis (Chlorophyceae, Volvocales). J Phycol 48:976–983

    Article  PubMed  Google Scholar 

  • Hallmann A (2007) Algal transgenics and biotechnology. Transgenic Plant J 1:81–98

    Google Scholar 

  • Hoshaw RW, Rosowski JR (1973) Methods for microscopic algae. In: Stein JR (ed) Handbook of phycological methods. Culture Methods and Growth Measurements. Cambridge University Press, New York, pp 53–68

    Google Scholar 

  • Izquierdo A (1906) Ensayo sobre los Protozoos de las aguas dulce de Chile. Imprenta Cervantes, Santiago de Chile, p 228, 10 plates

    Google Scholar 

  • Kang CD, Lee JS, Park TH, Sim SJ (2005) Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biot 68:237–241

    Article  CAS  Google Scholar 

  • Kim ZH, Kim SH, Lee HS, Lee CG (2006) Enhanced production of astaxanthin by flashing light using Haematococcus pluvialis. Enzyme Microb Tech 39:414–419

    Article  CAS  Google Scholar 

  • Kobayashi M, Kakizono T, Nishio N, Nagai S, Kurimura Y, Tsuji Y (1997) Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl Microbiol Biot 48:351–356

    Article  CAS  Google Scholar 

  • León-Bañares R, González D, Galván A, Fernández E (2004) Transgenic microalgae as green cell-factories. Trends Biotechnol 22:45–52

    Article  PubMed  Google Scholar 

  • Li J, Zhu D, Niu J, Shen S, Wang G (2011) An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotech Adv 29:568–574

    Article  CAS  Google Scholar 

  • Liang Y, Mai K, Sun S (2005) Differences in growth, total lipid content and fatty acid composition among 60 clones of Cylindrotheca fusiformis. J Appl Phycol 17:61–65

    Article  CAS  Google Scholar 

  • López Alonso D, Molina Grima E, Sánchez Pérez JA, García Sánchez JL, García Camacho F (1992a) Fatty acid variation among different isolates of a single strain of Isochrysis galbana. Phytochemistry 31:3901–3904

    Article  Google Scholar 

  • López Alonso D, Molina Grima E, Sánchez Pérez JA, García Sánchez JL, García Camacho F (1992b) Isolation of clones of Isochrysis galbana rich in eicosapentaenoic acid. Aquaculture 102:363–371

    Article  Google Scholar 

  • López Alonso D, Segura del Castillo CI, García Sánchez JL, Sánchez Pérez JA, Camacho FG (1994) Quantitative genetics of fatty acid variation in Isochrysis galbana (Prymnesiophyceae) and Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 30:553–558

    Article  Google Scholar 

  • Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167

    Article  CAS  PubMed  Google Scholar 

  • Mendes-Pinto M, Raposo M, Bowen J, Young A, Morais R (2001) Evaluation of different cell disruption processes on encysted cells of Haematococcus pluvialis: effects on astaxanthin recovery and implications for bio-availability. J Appl Phycol 13:19–24

    Article  Google Scholar 

  • Mostafa N, Omar H, Tan SG, Napis S (2011) Studies on the genetic variation of the green unicellular alga Haematococcus pluvialis (Chlorophyceae) obtained from different geographical locations using ISSR and RAPD molecular marker. Molecules 16:2598–2608

    Article  CAS  Google Scholar 

  • Park E, Lee CG (2001) Astaxanthin production by Haematococcus pluvialis under various light intensities and wavelengths. J Microbiol Biotech 11:1024–1030

    CAS  Google Scholar 

  • Proctor VW (1957) Some controlling factors in the distribution of Haematococcus pluvialis. Ecology 38:457–462

    Article  Google Scholar 

  • Sarada R, Tripathi U, Ravishankar GA (2002a) Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions. Process Biochem 37:623–627

    Article  CAS  Google Scholar 

  • Sarada R, Bhattacharya S, Ravishankar GA (2002b) Optimization of culture conditions for growth of the green alga Haematococcus pluvialis. World J Microb Biot 18:517–521

    Article  CAS  Google Scholar 

  • Sharon-Gojman R, Maimon E, Leu S, Zarka A, Boussiba S (2015) Advanced methods for genetic engineering of Haematococcus pluvialis (Chlorophyceae, Volvocales). Algal Res 10:8–15

    Article  Google Scholar 

  • Shaw PM, Jones GJ, Smith JD, Johns RB (1989) Intraspecific variations in the fatty acids of the diatom Skeletonema costatum. Phytochemistry 28:811–815

    Article  CAS  Google Scholar 

  • Starr RC, Zeikus JA (1993) UTEX-The culture collection of algae at the University of Texas at Austin. J Phycol 29(Suppl):1–106

    Article  Google Scholar 

  • Sun H, Komg Q, Geng Z, Duan L, Yang M, Guan B (2015) Enhancement of cell biomass and cell activity of astaxanthin-rich Haematococcus pluvialis. Bioresource Technol 186:67–73

    Article  CAS  Google Scholar 

  • Torzillo G, Goksan T, Faraloni C, Kopecky J, Masojídek 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

    Article  CAS  Google Scholar 

  • Tripathi U, Venkateshwaran G, Sarada R, Ravishankar GA (2001) Studies on Haemococcus pluvialis for improve production of astaxanthin by mutagenesis. World J Microb Biot 17:143–148

    Article  CAS  Google Scholar 

  • Wegmann K, Metzner H (1971) Synchronization of Dunaliella salina cultures. Arch Mikrobiol 78:360–367

    Article  Google Scholar 

  • Yong YYR, Lee KK (1991) Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris (Chlorophyta)? Phycologia 30:257–261

    Article  Google Scholar 

  • Zhang BY, Geng YH, Li ZK, Hu HJ, Li YG (2009) Production of astaxanthin from Haematococcus in open pond by two-stage growth one step process. Aquaculture 295:275–281

    Article  CAS  Google Scholar 

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Acknowledgments

This investigation was supported by grants from the Dirección de Investigación, Universidad de Concepción, Chile (Project DIUC No. 204.111.040-1.0), and Fundación Andes, Chile (Project No. C-14055-7).

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Authors and Affiliations

  1. Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Grupo de Investigación Microalgal FICOLAB, Universidad de Concepción, Casilla 160-C, Concepción, Chile

    Patricia I. Gómez, Paola Haro, Jennifer Torres, Pablo Castro, Víctor González, Ingrid Inostroza & Mariela A. González

  2. Centro de Investigaciones Biomédicas, Universidad Andrés Bello, Avenida República 239, Santiago, Chile

    Priscilla Lagos

  3. School of Biological Sciences, Monash University, Clayton campus, Melbourne, 3800, Australia

    Yussi Palacios

  4. Departamento de Estadística, Facultad de Ciencias Físicas y Matemáticas, Universidad de Concepción, Casilla 160-C, Concepción, Chile

    Katia Sáez

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  1. Patricia I. Gómez
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  2. Paola Haro
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  3. Priscilla Lagos
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  5. Jennifer Torres
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  7. Pablo Castro
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  10. Mariela A. González
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Correspondence to Patricia I. Gómez.

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Gómez, P.I., Haro, P., Lagos, P. et al. Intraspecific variability among Chilean strains of the astaxanthin-producing microalga Haematococcus pluvialis (Chlorophyta): an opportunity for its genetic improvement by simple selection. J Appl Phycol 28, 2115–2122 (2016). https://doi.org/10.1007/s10811-015-0777-0

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